1 s2.0 S004896971830425X Main

Science of the Total Environment 628–629 (2018) 1582–1599
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
Review
Microbe and plant assisted-remediation of organic xenobiotics and its

enhancement by genetically modified organisms and recombinant
technology: A review
Imran Hussain a,b,1, Gajender Aleti a,1, Ravi Naidu c, Markus Puschenreiter d, Qaisar Mahmood f,
Mohammad Mahmudur Rahman c, Fang Wang e, Shahida Shaheen f,
Jabir Hussain Syed g,h,⁎, Thomas G. Reichenauer a,⁎⁎
a
AIT Austrian Institute of Technology, Centre for Energy, Environmental Resources and Technologies, Tulln, Austria
b
Department of Molecular Systems Biology, Faculty of Life Sciences, University of Vienna, Austria
c
Global Centre for Environmental Remediation (GCER), Faculty of Science, The University of Newcastle, Callaghan, New South Wales, Australia
d
Institute of Soil Research, University of Natural Resources and Life Sciences, Vienna, Austria
e
Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China
f
Department of Environmental Sciences, COMSATS Institute of Information Technology, Abbottabad, Pakistan
g
Department of Meteorology, COMSATS Institute of Information Technology, Park Road Tarlai Kalan 45550, Islamabad, Pakistan
h
Department of Civil and Environmental Engineering, Hong Kong Polytechnic University, Hong Kong
H I G H L I G H T S G R A P H I C A L A B S T R A C T
• This review offers details on enhanced

remediation by transgenic plants and
microbes.
• Use of transgenic plants for remediation
of organic compounds has enormous
potential.
• Synergistic interaction between recom-
binant bacteria and genetically modified
plants may enhance the remediation.
• Potential risks associated with altered
microbes and plants can be tackled by
abiding regulatory guidelines.
• Full scale remediation system may be
obtained by using biotechnological tools.
a r t i c l e i n f o a b s t r a c t
Article history: Environmental problems such as the deterioration of groundwater quality, soil degradation and various threats
Received 22 September 2017 to human, animal and ecosystem health are closely related to the presence of high concentrations of organic xe-
Received in revised form 31 January 2018 nobiotics in the environment. Employing appropriate technologies to remediate contaminated soils is crucial due
Accepted 3 February 2018
to the site-specificity of most remediation methods. The limitations of conventional remediation technologies in-
Available online 22 February 2018
clude poor environmental compatibility, high cost of implementation and poor public acceptability. This raises
Editor: P Holden the call to employ biological methods for remediation. Bioremediation and microbe-assisted bioremediation
(phytoremediation) offer many ecological and cost-associated benefits. The overall efficiency and performance
of bio- and phytoremediation approaches can be enhanced by genetically modified microbes and plants.
⁎ Correspondence to: J.H. Syed, Department of Meteorology, COMSATS Institute of Information Technology, Park Road Tarlai Kalan 45550, Islamabad, Pakistan.
⁎⁎ Correspondence to: T.G. Reichenauer, AIT Austrian Institute of Technology, Centre for Energy, Environmental Resources and Technologies, Tulln, Austria.
E-mail addresses: [email protected] (J.H. Syed), [email protected] (T.G. Reichenauer).
1
Authors making an equal contribution.
https://doi.org/10.1016/j.scitotenv.2018.02.037
0048-9697/© 2018 Elsevier B.V. All rights reserved.
I. Hussain et al. / Science of the Total Environment 628–629 (2018) 1582–1599 1583
Keywords: Moreover, phytoremediation can also be stimulated by suitable plant-microbe partnerships, i.e. plant-endophytic
Organics or plant-rhizospheric associations. Synergistic interactions between recombinant bacteria and genetically mod-
Plant-rhizospheric partnership ified plants can further enhance the restoration of environments impacted by organic pollutants. Nevertheless,
Genetically modified plants
releasing genetically modified microbes and plants into the environment does pose potential risks. These can
Microbes
Recombinant technology
be minimized by adopting environmental biotechnological techniques and guidelines provided by environmen-
Health risks tal protection agencies and other regulatory frameworks. The current contribution provides a comprehensive
overview on enhanced bioremediation and phytoremediation approaches using transgenic plants and microbes.
It also sheds light on the mitigation of associated environmental risks.
© 2018 Elsevier B.V. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1583
2. Microorganisms for the clean-up of contaminated environments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1584
2.1. Enhancement of bioremediation with engineered microbes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1584
2.2. Enhancement of bioremediation with recombinant technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1584
3. Plant-assisted bioremediation of organic contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1586
3.1. Phytoremediation and its processes/techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1586
3.2. Degradation mechanisms in plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1587
3.3. Phytoremediation technology for remediation of organics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1587
4. Plant-bacterial partnership for improved remediation of organic xenobiotics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1588
4.1. Endophytic-plant partnerships . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1589
4.2. Rhizosphere-plant partnership . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1590
4.3. Prediction and annotation of genome sequences of xenobiotic-degrading bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . 1590
5. Transgenic plants for remediation of organic contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1591
5.1. Transgenic plants for stimulated phytodegradation/rhizodegradation of organic pollutants . . . . . . . . . . . . . . . . . . . . . . . 1591
5.1.1. Herbicides and pesticides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1591
5.1.2. Halogenated organic compounds and explosives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1592
6. Risks and mitigation through biotechnological advances associated with using genetically modified plants and microbes . . . . . . . . . . . . . 1593
7. Conclusions and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1593
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1594
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1594
1. Introduction pollutants (POPs) (Fernández-Cruz et al., 2017), which are lipophilic or-
ganic compounds that can resist photochemical degradation. They typ-
The post-World War II era witnessed a substantial increase in the ically show a tendency to accumulate and persist in the environment for
production and release of organic contaminants into the environment longer periods (Cetin et al., 2017; Sharma et al., 2014a, 2014b). Most
around the globe. This increase corresponded with rapid industrializa- POPs fall into three categories: organochlorine pesticides, industrial
tion, population growth, mechanized agricultural practices and military chemicals and their by-products (Arslan et al., 2015; Beyer et al.,
activities (Arslan et al., 2015). Although certain organic compounds are 2000; Muir and Howard, 2006). Within the domain of POPs, a “dirty
beneficial for industry and agricultural productivity, their excessive dozen” showing pronounced persistence, toxicity, as well as bioaccu-
usage creates many environmental problems. Kang (2014) noted the mulation and biomagnification in human and animal fatty tissues was
detrimental implications of such organic contaminants in the environ- defined (Xu et al., 2013; Martin et al., 2016). The pesticides and insecti-
ment and on human health. Many other researchers highlighted the ad- cides on the list exhibit persistence and toxicity (Haffner and Schecter,
verse consequences of organic contaminants on plants (Copaciu et al., 2014; Tavakoly Sany et al., 2015).
2016; Noguera-Oviedo and Aga, 2016), soils (Pinedo et al., 2013; Teng Explosives comprise another class of organic contaminants that
et al., 2014) and humans (Cachada et al., 2012; Malchi et al., 2014). heavily pollute the environment due to their industrial-scale production
Most organic contaminants are hydrophobic in character and can re- and exploitation (Kiiskila et al., 2015). Explosives are found at former
duce the quality of soils/sediments, pollute groundwater and cause se- war zones, military firing ranges and their production plants. The most
vere health risks for humans and animals (Liu et al., 2016; Ramadass prevalent contaminants associated with such areas are 2,4,6-trinitrotolu-
et al., 2015). Additionally, some organic contaminants (chlorinated sol- ene (TNT), hexahydro-1,3,5-trinitro-1,3,5-triazine, hexogen (RDX) and
vents, persistent organic pollutants (POPs) and explosives) have proved octahydro-1,3,5,7 tetranitro-1,3,5,7-tetrazocine, octogen (HMX) (Ali et
to be carcinogenic, mutagenic and neurotoxic (Gilden et al., 2010; al., 2014; Douglas et al., 2012). These four explosives along with their
Tabrez and Ahmad, 2009; Wasi et al., 2013). transformation products can cause toxic, lethal and detrimental effects
The various classes and groups of organic contaminants differ in in many organisms, including humans (Wang et al., 2017). Direct contact
their bioavailability and persistence in the environment. Chlorinated may cause severe health problems such as liver, skin and immune system
solvents are the most common and widely distributed organic contam- disorders. Lastly, pollution associated with petroleum hydrocarbons and
inants in the environment (Matteucci et al., 2015). They include trichlo- their derivatives is a well-established concern worldwide (Gerhardt et
roethylene (TCE), perchloroethylene (PCE), carbon tetrachloride and al., 2017). Crude oil, gasoline, creosote and diesel are major constituents
chloroform. Most chlorinated hydrocarbons are of anthropogenic origin of this group commonly designated as total petroleum hydrocarbons
and can spread throughout the environment via plastics, paints, adhe- (TPHs) (Yousaf et al., 2011; Afzal et al., 2014). All these organic xenobi-
sive materials and gasoline (Rosner and Markowitz, 2013). Another no- otics are linked to cancer, mutations, immune system disorders, as well
torious group of organic contaminants consists of persistent organic as reproduction and birth defects (Gilden et al., 2010; Kang, 2014).
1584 I. Hussain et al. / Science of the Total Environment 628–629 (2018) 1582–1599
The development of remediation technologies to reclaim contami- and environmental health” (Viana and Sant'ana, 2017; Daar et al.,
nated sites is of paramount importance to protect human lives. A set 2002). The discovery of many microbes and their unique catabolic char-
of physical, chemical, biological and integrated approaches are available acteristics has boosted the application of bioremediation. Microbes can
to remediate the pollution caused by organic xenobiotics (Gomes et al., degrade a large variety of organic xenobiotics by specific biochemical
2013; Abhilash et al., 2009; Khan et al., 2004). The conventional mea- processes under anaerobic or aerobic conditions (Kumar and Philip,
sures usually involve high application costs and energy inputs 2017; Collins, 2001). Distinctive features of microbes (e.g. catabolic po-
(Kuppusamy et al., 2017). This has triggered intensified efforts to de- tential, adaptation and surfactant production) render them favorable
velop more efficient, ecologically sustainable, environmentally friendly candidates for contaminant transformation (Le et al., 2017; Schenk et
and cost-effective remediation technologies utilizing advanced biotech- al., 2012). Various factors – soil pH, nutritional status, moisture, temper-
nological tools and rhizosphere engineering (Kuppusamy et al., 2017; ature, redox potential and chemical composition of pollutants – can in-
Ibañez et al., 2016; Dixit et al., 2015; Truu et al., 2015). Bioremediation fluence and potentially limit bioremediation efficiency (Shukla et al.,
involves using specific microbes to degrade organic contaminants – a 2013). This calls for the need to improve bioremediation processes. Ap-
reasonable and effective method based on the unique catabolic poten- plication of microbes alone has shown limited efficiency due to multiple
tial of microbes (Cheng et al., 2017). Within the scope of bioremedia- factors including poor competitiveness and excessive contaminant con-
tion, phytoremediation offers promising advantages with the centrations in soil. Efficiency can be enhanced by applying various
synergistic use of plants and microbes (Vergani et al., 2017; Thijs et amendments such as inorganic nutrients, surfactants, bulking agents,
al., 2016). Moreover, plants exhibit an array of additional decontamina- compost as well as biochar (Wiszniewska et al., 2016). Such amend-
tion mechanisms in comparison to microbes alone (Gerhardt et al., ments have been comprehensively reviewed in recent studies
2016, 2009; Singh et al., 2016). (Kästner and Miltner, 2016, Lukić et al., 2016; Truu et al., 2015). The
This review discusses the enhanced bioremediation and present review focuses on improved bioremediation using transgenic
phytoremediation of organic contaminants. It focuses on recent ad- microbes. The development and use of transgenic microbes through re-
vances in augmented bioremediation involving recombinant technolo- combinant technology is a straightforward approach.
gies and phytoremediation with plant-endophytic/rhizospheric
partnerships, along with its further improvements using genetically 2.1. Enhancement of bioremediation with engineered microbes
modified plants. Finally, also discussed here are the risks associated
with engineered plants and microbes along with their mitigation Engineered microbes for the transformation of organic xenobiotics
using biotechnological advances. are constantly being developed to overcome the limitations of bioreme-
diation. During the early 1990s, genetic engineering techniques were
2. Microorganisms for the clean-up of contaminated environments applied to exploit microbial metabolism for this purpose (Zwillich,
2000). This led to a rapid growth in biodegradation enterprises and ex-
The term bioremediation implies the conversion of organic contam- panded the research in this emerging field (Jagtap and Bapat, 2017). The
inants into carbon dioxide, water and a transformed product created by regulatory challenges and enormous expenses involved in transgenic
the actions of specific microbes (Hlihor et al., 2017a, 2017b; Chaudhry et research affected many companies. Over time, experiments and re-
al., 2005; Sarkar, 2018). Principally, it involves the transformation of or- search on genetically modified microorganisms gradually became con-
ganic contaminants by the concerted action of microorganisms as part fined to academic and research institutes. Some studies such as Abril
of their metabolic processes (Ghosal et al., 2016). Both aerobic and et al. (1989) and Brinkmann and Reineke (1992) reported increased
non-aerobic degradation pathways have been reported in the minerali- degradation of 3- and 4-chlorotoluene and 3-chlorotoluene over the
zation and stabilization of organic contaminants. Many bioremediation control by inoculation of a genetically modified Pseudomonas sp. B13
systems operate under aerobic conditions; anaerobic conditions, how- strain. Some genetically engineered microorganisms outside the field
ever, may be advantageous in degrading recalcitrant molecules such of bioremediation have also been reported (Coleman et al., 1997;
as PCBs and PAHs (Passatore et al., 2014). Various bacterial genera Pieper and Reineke, 2000; Sandermann, 1994; Yang et al., 2010). The ra-
such as Pseudomonas, Alcaligenes, Sphingomonas, Rhodococcus and My- diation-tolerant microbe Deinococcus radiodurans has been genetically
cobacterium degrade pesticides and hydrocarbons under aerobic condi- engineered for toluene degradation; it has not, however, been commer-
tions (Vergani et al., 2017). These heterotrophic bacterial genera utilize cialized to date for bioremediation purposes due to anticipated risks and
contaminants as their sole source of carbon and energy. Anaerobic mi- regulatory challenges (Ezezika and Singer, 2010; Lang and Wullbrandt,
crobes have been frequently used to degrade PCBs as well as dechlori- 1999). Failure to advance from research to commercialization is attrib-
nate TCE and chloroform (Hlihor et al., 2017c). uted to several factors such as challenges in gaining approval from reg-
The bioremediation efficiency may be limited especially when soils ulatory bodies prior to release in the environment, public acceptability
are polluted with recalcitrant organic molecules. In such cases, the com- and safety risks associated with engineered bacteria.
bined use of microbes and plants (rhizoremediation) can enhance the
efficiency (Thijs et al., 2016). Plant roots provide microaerophilic condi- 2.2. Enhancement of bioremediation with recombinant technology
tions, and root exudates additionally enhance the degradation of or-
ganic contaminants. Root exudates accelerate the degradability and The microbial metabolic potential can be exploited for environmen-
bioavailability of organic xenobiotics to microbes by: firstly, providing tal remediation and is a very economical and safe alternative compared
substrate for microbial metabolism; and secondly, altering soil pH or to other physicochemical techniques (Liu et al., 2017). Despite the pres-
contaminant solubility. Four possible pathways have been reported for ence of highly diverse and specialized microbial communities in the en-
enhancing the biodegradation of organic contaminants by root exu- vironment that can break down many pollutants, the natural
dates: 1) direct degradation by plant enzymes; 2) enhanced pollutant remediation process may be quite slow. This may lead to the accumula-
bioavailability via secreting surfactants; 3) exploitation of structural tion of pollutants in the environment, which can be hazardous (Ijoma
analogy and co-metabolic processes; and 4) stimulation by providing and Tekere, 2017; Cheng et al., 2017; Perpetuo et al., 2011). With the ad-
a nutrient and energy flow (Martin et al., 2014). vent of the latest biotechnological techniques such as natural gene
Bioremediation is an attractive option for remediating organic con- transfer or recombinant DNA methods, bacterial strains (rhizospheric
taminants because it offers many benefits, for instance cost-effective- and/or endophytic) can be engineered to produce specific enzymes
ness, efficiency, and environmental “friendliness” (Kästner and that promote the degradation of toxic organic substances (Pandotra et
Miltner, 2016; Chen et al., 2015; Kang et al., 2012). It has also been in- al., 2018; Chakraborty and Das, 2016). Genetic engineering has the po-
cluded in the list of the “top ten technologies for improving human tential to improve soil bioremediation technologies, and applying this
approach to plant-associated endophytic and rhizospheric bacteria can A genetically engineered poplar endophytic Pseudomonas putida
help enhance the degradation of toxic compounds in contaminated VM1441 (pNAH7) protected pea plants against the toxic effects of naph-
sites by phytoremediation (Fasani et al., 2017). thalene. Furthermore, plants inoculated with that strain indicated an in-
Previous studies (Gao et al., 2017; Chebbi et al., 2017) clearly re- crease in naphthalene degradation rates (up to 40%) compared to un-
vealed oil biodegradation capabilities of four Pseudomonas strains and, inoculated plants in artificially contaminated soil (Germaine et al.,
interestingly, genes encoding degradation enzymes were found on 2009). In one greenhouse study, a genetically modified endophyte
extra-chromosomal plasmids. Four plasmids were isolated and intro- Burkholderia cepacia G4 showed increased toluene tolerance in the
duced in Pseudomonas spp., which enhanced the oil degradation poten- yellow lupine plant and decreased phytovolatilization of toluene by
tial by 10–100 times compared to natural isolates (Time Magazine, 70%. Natural endophyte was conjugated by a plasmid (pTOM)
1975). Studies related to the degradation of toxic organic contaminants encoding enzymes that made toluene degradation possible (Barac
using genetically engineered microbes have been recently summarized et al., 2004). Nonetheless, subsequent studies on poplar trees
by Kumar et al. (Kumar et al., 2013). Agent Orange is one of the toxic suggested that the plasmid was prone to horizontal gene transfer
herbicides and defoliants used by the U.S. military during the Vietnam (Taghavi et al., 2005).
War, and it was closely linked to increased incidences of cancer A specific bacterial glutathione-S-transferase (GST) isolated from
(Ezezika and Singer, 2010). Agent Orange is a mixture of equal parts Burkholderia xenovorans LB400, BphKLB400 removed toxic chlorines
of phenyl herbicides including 2,4-dichlorophenoxyacetic acid (2,4-D) from organic pesticides and provided resistance to chloromequat chlo-
and 2,4,5-trichlorophenoxyacetic acid (2,4,5-T). A recombinant strain ride in pea plants (McGuinness et al., 2007). Further mutations in the
of Burkholderia cepacia was tested for the degradation of Agent Orange conserved amino acid site of GST involving substitution of Ala by Pro re-
at the storage site of the U.S. Air Force in Pensacola, Florida (Chauhan sulted in a 2-fold increase in GST activity towards a number of com-
et al., 2008). monly used chlorinated pesticides (McGuinness et al., 2006, 2007).
Cytochrome P450 monooxygenases (CYPs) are associated with the That study suggested that genetically modified endophytic or
degradation of the most toxic pollutants, for example naphthalene, fluo- rhizospheric bacteria are promising bioremediation agents for
rine, acenaphthalene, acenaphthylene, and 9-methylanthracene. Previ- dehalogenation of organic pollutants. Atrazine (2-chloro-4-
ous studies (Chica et al., 2005; Pleiss, 2012) suggested that enzyme ethylamino-6-isopropylamino-1, 3, 5-s-triazine), with a half-life of
activity could be increased by altering the active site through rational 170 days is used to control weeds. Pseudomonas sp. ADP was reported
design. Alterations at the F87 and Y96 sites within the CYP101 enzyme to enzymatically stabilize atrazine to the final, less toxic product called
tripled the oxidation potential of the enzyme in Pseudomonas putida cyanuric acid. Pseudomonas sp. ADP produced two forms of atrazine-
(Harford-Cross et al., 2000). Mutations at R47L and Y51F sites enhanced degrading enzymes – Atz (A, B, and C) and TriA – which may have dif-
the oxidation potential of the CYP102 enzyme for phenanthrene and ferent action mechanisms and produced cyanuric acid as the final deg-
fluoranthene 40-fold and 10-fold, respectively, in Bacillus megaterium radation product. Atz and TriA enzymes may have evolved recently to
(Carmichael and Wong, 2001). Moreover, a 30-fold increase in the degrade atrazine (De Souza et al., 1998).
degradation potential of polyaromatic hydrocarbons was achieved Comamonas testosterone strain VP44 was transformed by two plas-
when CYP was mutated at three active sites (A74G/F87V/L188Q). A mids: pE43 comprising oxygenolytic ortho-dechlorination ohb gene;
simultaneous increase in the nicotinamide adenine dinucleotide and pPC3 comprising the hydrolytic para-dechlorination fcb gene. The
phosphate (NADPH) consumption rate was observed as well (Liu et resulting two recombinants C. testosterone VP44 (pE43) and VP44
al., 2006). (pPC3) displayed affinity to cometabolite 95% concentrations of ortho-
PCBs are a class of aromatic chemicals encompassing 209 different and para-chlorobiphenyls as sole carbon sources (Hrywna et al.,
chemical structures (congeners). PCBs are used in a wide range of appli- 1999). Sphingomonas sp. CDS-1 was genetically modified to degrade or-
cations such as the manufacture of insecticides and electrical insulating ganophosphate- and carbamate. In Pseudomonas putida DLL-1, a methyl
fluids in capacitors and transformers (Das and Adholeya, 2012). PCBs parathion hydrolase gene (mpd) with cognate regulator of a methyl
also adversely affect human and environmental health. The biphenyl parathion (MP) was prepared by shotgun cloning. The DNA fragment
dioxygenase enzyme degrades PCBs under aerobic conditions (Ang et was further cloned into a broad host vector pBBR1MCS-2 to produce
al., 2005). During this process, the enzyme incorporates two hydroxyl pBBR-mpd (Liu et al., 2006). CDS-pBBR-mpd recombinant strain was
groups into the aromatic ring of a PCB's congener, yielding a tricarbox- produced by transforming the recombinant plasmid into the
ylic acid cycle intermediate (chlorobenzoate). The biphenyl carbofuran-degrading strain Sphingomonas sp. CDS-1. The resulting ge-
dioxygenase consists of a terminal dioxygenase, ferredoxin, and ferre- netically engineered organism mediated methyl parathion degradation
doxin reductase encoded by the bph operon (Erickson and Mondello, nearly 7 times faster than the wild type strain (Liu et al., 2006).
1992). Variants of bphA with increased capacities for PCB degradation Organophosphates such as paraoxon, parathion, chlorpyrifos disul-
were produced from Burkholderia cepacia strain LB400, C. testosterone foton, ruelene, carbophenothion, and dimeton are potent neurotoxins
B-365, and Rhodococcus globerulus P6 via the family shuffling approach that interfere with the breakdown of acetylcholinesterase at the synap-
(Barriault et al., 2002). The hybrid bphA, in particular II-9 genes, were re- tic junction and are involved in chromosomal aberrations and bladder
ported to oxygenate persistent 2,6-dichlorobiphenyl up to 58%, while cancer (Das and Adholeya, 2012; Webster et al., 2002). Bacterial en-
the control oxygenated only up to 10% (Suenaga et al., 2002). Geneti- zymes including phosphotriesterase (PTE) and organophosphorus hy-
cally modified strains of the plant-associated rhizospheric bacteria Pseu- drolase (OPH) catalyze the hydrolysis of these toxic organophosphates
domonas fluorescens F113rifbph and Pseudomonas fluorescens by cleaving P\\O, P\\F, or P\\S bonds. The analysis of the three-dimen-
F113:1180 colonized plant roots similar to the wild-type rhizospheric sional structure of PTE from Pseudomonas diminuta with a structural an-
bacteria (Brazil et al., 1995; Villacieros et al., 2005). Both genetically alogue diethyl 4-methylbenzylphosphonate revealed three
modified strains, however, showed a significantly increased degrada- hydrophobic binding pockets that were necessary for the orientation
tion capacity for PCBs compared with wildtype rhizospheric bacteria. of the substrate in the active site (Chen-Goodspeed et al., 2001a,
This makes the manipulation of the rhizospheric bacteria a substantial 2001b). Moreover, triple mutations at key sites Ile106, F132G, and
future prospect for bioremediation. Furthermore, the Pseudomonas His257 enhanced the catalytic properties. For example, substitution of
fluorescens F113: 1180 strain was tested negatively for antibiotic resis- Ile106 by Ala eliminated organophosphates 90-fold; Sp-enantiomer
tance and the strain was considered suitable for in situ applications mutations at I106G/F132G showed 270-fold enhancements in Kcat
(Villacieros et al., 2005). Gene bph of Pseudomonas fluorescens f113: and Rp-enantiomers with a stable Kcat for Sp-enantiomers. Further-
1180 is stable and therefore it is not clear if a horizontal gene transfer more its substitution by His257 resulted in the reduced kinetic parame-
among the rhizospheric bacteria will take place (Ramos et al., 1995). ters of PTE (Chen-Goodspeed et al., 2001a). Selected examples of
genetically engineered bacteria that degrade specific organic com- or water bodies contaminated by heavy metals, petroleum hydrocar-
pounds are summarized in Table 1. bons, chlorinated solvents, pesticides, explosives and radionucleotides
(Afzal et al., 2014; Aken and Doty, 2009; Álvarez et al., 2015; Kiiskila
3. Plant-assisted bioremediation of organic contaminants et al., 2015; Zhang et al., 2016). Despite the proven effectiveness of
phytoremediation in different experimental contexts, i.e. laboratory,
3.1. Phytoremediation and its processes/techniques greenhouse and in the field, this technology remains underutilized by
governments and the private sector. Recently, Gerhardt et al. (2017)
Phytoremediation is a set of technologies using the natural potential proposed different steps for commercial utilization of this green and
of specific plants and their associated microbes to detoxify, transform, sustainable technology. Phytoremediation covers many strategies that
extract, sequester, or assimilate various toxic inorganic and organic pol- seek to remediate a wide range of organic and inorganic pollutants
lutants in the environment, especially soil, surface waters, groundwater using different natural processes. These are explained in more detail
and air (Gerhardt et al., 2016). Plants have always been a basic source of below.
food, fuel (energy) and fibre. Over the past three decades, the utilization Phytoextraction refers to the uptake of contaminants through plant
of plants and catabolic potential of their associated microbes have be- roots and their translocation to harvestable plant parts such as shoots
come accepted as a ‘green solution’ for reclaiming contaminated soils (Mahar et al., 2016; Abhilash et al., 2012). It is also typically known as
and water (Truu et al., 2015). It offers many ecological and technical phytoaccumulation or phytosequestration, mostly reported for heavy
benefits over conventional methods for remediating organic contami- metals (Ali et al., 2013). Rhizofiltration involves the removal of pollut-
nants. Phytoremediation is considered to be environmentally friendly, ants from surface water or liquid waste streams by plant roots
sustainable, solar-driven, cost effective and socially acceptable. It does, (Dimitroula et al., 2015; Ali et al., 2013). It can be further classified
however, have certain disadvantages that can limit its applicability, in- into blastofiltration (use of seedlings) and caulofiltration (use of plant
cluding a longer time frame for achieving the remediation target, ineffi- shoots). Phytostabilization or phytoimmobilization is the use of certain
ciency in the presence of high pollutant levels, limited zone of plants to stabilize contaminants in soils in order to reduce their bioavail-
effectiveness and limitations in the case of low bioavailability ability (Burges et al., 2016; Singh et al., 2012). Reduced bioavailability
(Gerhardt et al., 2016). For a detailed description of the advantages may help prevent pollutants enter groundwater and the food chain
and disadvantages of phytoremediation, see earlier reviews (Afzal, (Erakhrumen, 2011). Plant processes such as sorption (by roots), pre-
2010; Ali et al., 2013; Arslan et al., 2015; Asim Shahzad, 2015; cipitation, complexation and metal valence reduction (in rhizosphere)
Chaudhry et al., 2005; Dhankher et al., 2012; Gerhardt et al., 2009; are mainly responsible for immobilizing metals in contaminated soils
Gkorezis et al., 2016; Gerhardt et al., 2017). (Wuana and Okieimen, 2011; Ghosh and Singh, 2005; Yoon et al.,
In 1980 the term phytoremediation was coined, followed by a rapid 2006). Plants can secrete specific sets of redox enzymes that convert
expansion for treating a variety of pollutants in the last three decades more toxic metals species to less toxic species. Thus, it may help avoid
(Schwitzguébel, 2015). To date, it has been applied to remediate soils metal stress and damage in plants and other biota. Phytostabilization
Table 1
Recombinant technologies used for transgenic microbes with their significant findings.
Recombinant strategy Results References
Escherichia coli engineered to overproduce atrazine After 8 weeks, Atrazine concentration decreased by 52% in plots containing (Strong et al., 2000)
chlorohydrolase AtzA killed recombinant E. coli cells, and 77% in combination plots containing
phosphate and the enzyme
Plasmid with a transposon-based bioluminescence producing Higher Naphthalene gene expression lead to enhanced degradation rates of (Sayler and Ripp, 2000)
lux gene fused with a promoter for naphthalene catabolic the pollutant
genes
Engineered endophytic bacteria with toluene degrading The recombinant strain induced up to 50%–70% degradation of toluene. (Barac et al., 2004)
pTOD/pTOM plasmid
pNF142 plasmid, gfp Degradation of naphthalene in soil (Wang et al., 2008)
pTOM-Bu61 plasmid encoding constitutively expressed Inoculation of poplar had increased plant growth in the presence of toluene (Taghavi et al., 2005)
toluene degradation and substantially reduced concentrations of toluene released via
evapotranspiration
Arthrobacter globiformis encoding enzymes responsible for Degraded mixture of PCBs in soil polluted with Aroclor 1242 (Rodrigues et al., 2006)
ortodehalogenation of mono-,di-and trichlorobenzoates
pWW0 plasmid Genetically modified rhizospheric bacteria degraded petroleum (Jussila et al., 2007)
hydrocarbons
Transformed with the degradative plasmid pNB2 Removed 3-chloroaniline pollutant to large extent (Bathe et al., 2009)
Insertion of Azoreductase gene Direct Blue 71 concentration was decreased to 12.6 mg/L in 12 h (Jin et al., 2009)
Recombinant strain was developed by cloning fcb genes Was able to degrade 4-CBA in soil (Massa et al., 2009)
encoding dehalogenase into artificial plasmid pDH5
pWR1 plasmid 3-chlorobenzoate-degradation (Hartmann et al., 1979,
Reineke and Knackmuss,
1980)
TOL plasmid restructured to produce a pathway for processing a new substrate (Ramos et al., 1995)
4-ethylbenzoate
TOL operon of plasmid pWW0 with cognate regulatory gene Conversion of toluene into catechol intermediate was mediated by the TOL (Panke et al., 1998)
xylR enzymes
pPC3 from Arthrobacter globiformis and pE43 from Degradation of ortho and para monochlorobiphenyls (Hrywna et al., 1999)
Pseudomonas aeruginosa encompassing genes for
dehalogenation of chlorobenzoates
Biphenyl dioxygenase, bphA Site-directed mutagenesis of bphA gene resulted in broad congener (Erickson and Mondello, 1992)
specificity with increased activity
bphA1 gene (encoding a large subunit of biphenyl These hybrid strains gained resistance to grow on different aromatic (Suyama et al., 1996)
dioxygenase) is replaced with the todC1 gene (encoding hydrocarbons, and degraded chloroethenes, trichloroethylene and cis-1,
large subunit of toluene dioxygenase) 2-dichloroethylene more efficiently.
Genes coding for toluene 4-monooxygenase were cloned Recombinant organisms showed degradation of TCE (Winter et al., 1989)
is mostly not applicable as a permanent solution because contaminants catalyzed by prominent enzymatic families known as cytochrome
(heavy metals) remain in the soil, albeit with reduced mobility. None- P450 (CYP) and carboxylesterases (CXE) – produce less toxic metabo-
theless, it can be part of a management strategy for potential toxic con- lites (Reichenauer and Germida, 2008). During phase 2 (conjugation),
taminants (Ali et al., 2013; Vangronsveld et al., 2009). metabolites of the previous phase are directly converted into hydro-
Phytovolatilization refers to the most controversial process of philic compounds by conjugating with sugars or amino acids and gluta-
phytoremediation in which plants can be used to take up pollutants thione (Dietz and Schnoor, 2001). Finally, the conjugated molecules are
from contaminated soils and transform them into a volatile form stored in vacuoles (apoplast) or assimilated into the cell wall in lignin,
followed by transfer to the atmosphere (Limmer and Burken, 2016). pectin, and cellulose fractions in phase 3 (compartmentalization)
This technique has limited applications because it can only be utilized (Dietz and Schnoor, 2001). Previous studies (Theodoulou, 2000;
for organic pollutants and certain heavy metals or metalloids (Hg and Schröder, 2007) categorized the final part of the xenobiotic degradation
Se). Critics argued that phytovolatilization is merely the transfer of pol- mechanism into two independent processes. One was responsible for
lutants from one compartment of the environment (soil) to another (at- transport and storage in vacuoles, whereas the second confined mole-
mosphere) (Ali et al., 2013; Padmavathiamma and Li, 2007). Some low cules to the cell wall for binding or excretion. After being translocated
molecular weight volatile hydrocarbons can experience via plant roots, organic xenobiotics undergo different biotransformation
phytovolatilization along the transpiration stream (Yavari et al., 2015). (green-liver model) for detoxification, i.e. sequestration in roots, trans-
Phytodesalination is the use of halophytic plants to remove salts port to aerial plant parts, and finally stored in vacuoles or transformed
from salt-affected soils (Zorrig et al., 2012). Now that water scarcity by volatilization.
and desertification are two threats to human and ecosystem heath,
phytodesalination is emerging as a sustainable option for remediating 3.3. Phytoremediation technology for remediation of organics
salt-affected land (Rabhi et al., 2010). Additionally, halophytic plants
can cope better with heavy metals than glycophytic plants After being taken up by plants, organic pollutants may be
(Manousaki and Kalogerakis, 2011). Thus, halophytes can be used to si- translocated and accumulated in roots or shoots. The extent of plant up-
multaneously remediate salts and heavy metals in co-contaminated take depends on different physicochemical properties (e.g. octanol-
soils. Phytotransformation (sometimes also termed phytodegradation) water partitioning coefficient and acidity constant) of the pollutants
refers to the transformation of organic pollutants by plant enzymes (Gerhardt et al., 2017). The log value of the octanol-water partition co-
(dehalogenase, nitroreductase, laccase and oxygenase) in any aerial efficient (log Kow) provides a direct measure of the hydrophobicity or li-
part of the plants themselves (Siciliano et al., 2002; Germida et al., pophilicity of organic compounds and their tendency to move through
2002). It mainly depends on plant metabolic activities and is not influ- lipid bilayers (Yang et al., 2017). Generally, a higher value of log Kow
enced by rhizospheric microorganisms (Newman and Reynolds, (˃3 to 8) represents low to nil solubility in water – the scenario that pre-
2004). Phytotransformation is applicable only in remediating organic vents their entry in plant roots but shows a tight sorption on soil parti-
pollutants. It has been described in the literature as able to remediate cles and root surfaces. Organic compounds with a medium log Kow value
a variety of pollutants including chlorinated solvents, petroleum hydro- (0.5–3) indicate less hydrophobicity and can be taken up by plants.
carbons and synthetic herbicides or pesticides (Dhankher et al., 2012; Lastly, the lower values of log Kow (˂0.5) reveal higher solubility of or-
Chen et al., 2008; Doty, 2008; Wang et al., 2008). Al-Baldawi et al. ganic compounds in aqueous media (Reichenauer and Germida,
(2015) reported the phytotransformation of diesel-contaminated 2008). Most of the organic pollutants (TPH, polycyclic aromatic hydro-
water using Scirpus grossus; the results showed promising degradation carbons (PAHs), pesticides, chlorinated solvents and POPs) have log
rates. In that study, the maximum total petroleum hydrocarbons Kow values in the 3.0–8.5 range and are subsequently resistant to plant
(TPHs) were recorded in stems and leaf samples (93.72%, C20-C34). uptake. In addition to log Kow values, pollutant concentration and mor-
Finally, Rhizodegradation is the breakdown of organic contaminants phological features of plant species are important factors affecting the
in soils by bacterial and fungal activity enhanced by the rhizospheric ef- translocation of organic xenobiotics (Arslan et al., 2015).
fect of certain vascular plants (Thijs et al., 2016; Truu et al., 2015). Organic pollutants trigger drastic and deleterious effects on soils and
Phytotransformation and rhizodegradation are described in more detail plants (Tao et al., 2017). These include deterioration of soil quality, nu-
in the following sections. trient imbalance and extreme hydrophobic conditions. Reduced seed
germination, lower chlorophyll pigment production, reduced root turn-
3.2. Degradation mechanisms in plants over, disturbed root/shoot growth and disruption of root architecture
are other potential negative outcomes. In this regard, plant selection is
In green plants the main mechanisms responsible for metabolic pro- crucial to phytoremediation strategies. The desirable plant characteris-
cessing of xenobiotic pollutants were termed the “green liver” by tics for successful phytoremediation of organic contaminants are: high
Sandermann (1994) as an analogy for the processing of xenobiotic pol- pollutant tolerance, robust plant growth and an effective enzymatic ac-
lutants in humans and animals. Recent biotechnological approaches for tion for pollutant degradation. It is well established that specific plants
bioremediation include biosorption, phytostabilization, can degrade a variety of organic xenobiotics such as petroleum hydro-
hyperaccumulation, dendroremediation, biostimulation, carbons, PCBs, chlorinated solvents, pesticides, POPs and the aforemen-
mycoremediation, cyanoremediation and genoremediation, which tioned ‘dirty dozen’. A vast body of literature confirms the suitability of
mainly depend on enhancing or preventing specified gene activities grasses, legumes, agronomic crops, ornamentals, herbs and trees for re-
(Mosa et al., 2016; Malik et al., 2016). This successful technique, how- mediation of organics in the environment. Table 2 summarizes different
ever, faces challenges (Mani and Kumar, 2014). In this concept xenobi- plants used in decontaminating organic xenobiotics. In general, each
otic metabolism consists of three biochemical processes: type of plant has a specific set of advantages over the others. Fibrous
transformation (phase 1), conjugation (phase 2) and compartmentali- roots, higher surface area, deeper penetration and more plant-pollutant
zation (phase 3) (Reichenauer and Germida, 2008). Fig. 1 illustrates contact are the typical advantages offered by grasses. Symbiotic nitro-
the fate and degradation processes of a variety of organic xenobiotics gen fixation is typically associated with legumes, which can restore
in plants. The only difference between human, animal and plant path- the nitrogen pool of polluted soils.
ways is that plants lack an excretion system. Ornamentals can be used with no risk of introducing contaminants
During phase 1, hydrophobic xenobiotics are chemically modified to or their metabolites into the food chain, and they help beautify such dis-
less hydrophobic metabolites by oxidation, reduction or hydrolysis, ox- turbed lands. Herbs and trees have additional benefits such as easy
idative desulfuration and reduction by cytochrome P450 (Abhilash et propagation, robust and perennial growth, and phreatophytic roots
al., 2009). In transformation, the most common and vital reactions – with direct contact to the water table (thus facilitating remediation of
Sequestraon,
Phytovolalizaon,
Compartmentalizaon
Aer transport in
shoot Rhizobacteria
and Fungi
Organic pollutants e.g.

Xenobiocs, TNT,
POPs, PCB, VOCs, Rhizodegradaon
Phenols, Dyes,
Hydrocarbons, RDX
Endophyc
Genecally
microbes
Modified Bacteria
Fig. 1. Biochemical/biotechnological treatment of organic pollutants in rhizosphere.
contaminated groundwater as well). Phytoremediation is a site-specific 4. Plant-bacterial partnership for improved remediation of organic
technology utilizing plant species selected specifically for the site condi- xenobiotics
tions. As well, various attempts have been made to increase the effi-
ciency of phytoremediation. These include soil amendments by adding Many reports mentioned the use of plants alone to remediate or-
inorganic fertilizers, nutrients, bulking agents, aeration, compost and ganic pollutants. Nonetheless, the synergistic use of plants with specific
biochar. The use of plants with associated suitable microbes (contami- microbes is recommended for greater efficiency. Bacterial associations
nant degraders and plant growth promoters) is a viable and promising with plants naturally encompass a remarkable catabolic diversity to de-
technology offering a number of benefits. grade, transform or accumulate a broad spectrum of organic compounds
Table 2
Selected case studies (2005–2017) of plants used in different phytoremediation studies for organic pollutants.
Pentachlorophenol Salix Spp. (willow and Plant showed tolerance towards pollutant and degradation in rhizosphere (Mills et al., 2006)
poplar)
Insecticide Poplar and Willow Uptake of dieldrin by plant roots with no biodegradation reported (Skaates et al., 2005)
Chlorinated solvent Poplar Poplar trees reduced TCE evapotranspiration by 90% with specific actions (Weyens et al., 2009)
Explosives(TNT, RDX) Poplar Detoxification of 2, 4, 6-trinitrotoluene (TNT) and 1, 3, 5-Trinitro-1, 3, (Flokstra et al., 2008)
5-triazacyclohexane (RDX). But the plant uptake was very slow
Explosive (TNT) Marigold After 3 months of plant growth more than 90% degradation was reported (Hooda et al., 2016)
Explosives (TNT,RDX) Vetiver grass, canaray Identification of suitable plants for explosive remediation plus specific genes for (Kiiskila et al., 2015)
grass, fox sedge, rice degradation under field conditions
Pesticide (DDT) Willow Uptake and translocation of DDT by plants. Increase availability of DDT by combined (Mitton et al., 2012)
action of Tween 80 and carboxylic acid
Total petroleum Scirpus grossus Phytodegradation variability by mentioned plants under multiple pollutant levels. (Al-Baldawi et al., 2015)
hydrocarbons (TPH)
Polychlorinated biphenyl Zucchini (Cucurbita pepo) The dissipation rates of Aroclor 1242 and soil bacteria abundance were much higher (Qin et al., 2014)
(PCB) with only microbes and control treatments
Organic compounds Multiple plants Phytovolatilization for multiple organic pollutants are reported in review form (Limmer and Burken, 2016)
Explosives Multiple plants A comprehensive review on phytoremediation of explosive contaminated soils are (Kiiskila et al., 2015)
presented
TPH Italian ryegrass Enhancement of phytoremediation efficiency by addition wheat-straw biochar (Cao et al., 2016)
Polycyclic aromatic Medicago sativa Dissipation of selected polycyclic aromatic hydrocarbons (Fu et al., 2012)
hydrocarbons (PAHs)
PAHs Medicago sativa Promotion of rhizodegradtion of pyrene with combined action of plants and microbes (Fan et al., 2008)
TPH Ornamental plants Rhizodegradtion of TPH with ornamental plants; remediation and beatify contaminated (Liu et al., 2008, 2012; Suleiman
soils with specific plants and Bhat, 2003)
such as petroleum hydrocarbons, halogenated hydrocarbons, pesticides, hormones such as ethylene-1-aminocyclopropane-1-carboxylic acid
PCBs and PAHs (Xun et al., 2015; Glick, 2010; Meagher, 2000). In (ACC) deaminase and indole-3-acetic acid (IAA) (Taghavi et al., 2009).
rhizodegradation, microbes mostly target hazardous organic pollutants Diazotrophic bacteria comprise a group of bacteria known for root
that cannot enter the plants due to their hydrophobic nature (Chaudhry nodulation which fixes atmospheric nitrogen. Research (Afzal et al.,
et al., 2005; Gerhardt et al., 2009; Huang et al., 2004, 2005). Bacterial as- 2014; Compant et al., 2005, 2010; Ma et al., 2011; Ryan et al., 2008;
sociations with plants can enhance the phytoremediation of organic Weyens et al., 2009) confirms that cultivable endophytes can been
pollutants in the rhizosphere and stabilize them into less harmful me- screened and isolated from grasses (tall fescue, ryegrass), herbs (penny-
tabolites or even mineralize the complex organic compounds into car- cress, oak, and arabidopsis), woody trees (poplar, pine, forest trees) and
bon dioxide and water (Alexander, 2000; Dzantor, 2007; Macek et al., agronomic crops (wheat, maize and sugarcane). Conventional bioreme-
2000). diation techniques for organic xenobiotics in soils and groundwater
In such plant-bacterial interactions, bacteria may proliferate around such as soil washing, extraction, pump and treat, application of heat/ox-
plant roots (as rhizospheric bacteria) and in the internal tissues (as en- ygen, and the addition of different chemicals or surfactants (Khan et al.,
dophytes) without being pathogenic to their host plant (Compant et al., 2004) may cause secondary pollution. Endophytic bacteria encompass
2005; Ryan et al., 2008; Sessitsch et al., 2005). Plants support bacterial diverse secondary metabolite potentials and have been shown to sup-
growth by providing residence and nutrients; in turn, bacteria metabo- press plant pathogens by antibiosis, competition for ecological space
lize pollutants in the rhizosphere and endosphere. This synergistic rela- or nutrients, and by activating plant-induced systemic resistance
tionship enhances the role of each partner (Feng et al., 2017; Macci et (Álvarez et al., 2015; Doty, 2008; Germaine et al., 2006; Ryan et al.,
al., 2013; Compant et al., 2010). Bacteria help their host plant to over- 2008; Van Aken et al., 2004). Endophytic bacteria have major advan-
come stress caused by pollutants and improve plant growth, thus en- tages over free-living rhizobacteria because they live inside the host tis-
hancing shoot and root biomass, which in turn supports microbial sue and thus have less competition for space and nutrients than the
populations and the degradation of organic pollutants (Weyens et al., rhizobacteria population, which generally competes with a large num-
2013; Arshad et al., 2007). Moreover, rhizoremediation results in ber of soil microorganisms (Compant et al., 2016; Doty, 2008).
broader microbial consortia with a faster degradation rate of contami- The endophytic niche is a hot spot for horizontal gene transfer, and
nants compared to rates achieved by individual strains (Khan et al., this naturally occurring process plays a vital role in the adaptation of mi-
2013). crobial communities to environmental stress (Huang et al., 2015;
Recently, several studies successfully exploited plant and rhizo- Taghavi et al., 2005; Wang et al., 2010). For example, the plasmid
sphere and endophytic bacterial partnerships to efficiently pTOM-Bu61 encoding degradation enzymes can transfer naturally to
phytoremediate organic contaminants from soil and water (Arslan et many plant endophytes and has contributed to efficient degradation
al., 2015; Fatima et al., 2015; Khan et al., 2014). Various bacterial strains of toluene in poplar plants. Pseudomonas endophytes with plasmids
with the metabolic potential to degrade specific toxic organic com- pWWO and pNAH7 also showed high rates of horizontal transfer into
pounds have been successfully isolated and characterized from a wide a number of endophytes (Ryan et al., 2007). In another study, Barac et
range of contaminated environments. Organic compounds can be al. (2004) reported the conjugative transformation of natural endo-
biodegraded aerobically or anaerobically (Ghattas et al., 2017). Anaero- phytes for enhanced toluene degradation. A toluene-degradation plas-
bic bacteria reduced highly chlorinated PCBs into less chlorinated bi- mid (pTOM) of Burkholderia cepacia was transferred by conjugation
phenyls (Matturro et al., 2016). Various aerobic bacterial genera into a natural endophyte inhabiting yellow lupine. Intriguingly,
including Burkholderia, Xenovorans, Pseudomonas, Mycobacterium and engineered endophytic bacteria reduced the plant transpiration to 50%
Rhodococcus were extensively studied for the bioremediation of organic from 70% (as compared to un-inoculated control), and thus reduced
pollutants (Song et al., 2015). Rhizospheric, endospermic and the toxicity in the host plant by degrading toluene. A number of recent
phylospheric microbes can beneficially interact with the host plants, in- studies (Badri et al., 2009; Oliveira et al., 2014; Phillips et al., 2008;
cluding especially mutualism (Berendsen et al., 2012). Special charac- Syranidou et al., 2016; Weyens et al., 2009) confirmed that endophytic
teristics rendering them suitable for remediation purposes are the bacteria perform better in the rhizodegradation of organic pollutants
presence of catabolic genes and enzymes (Gkorezis et al., 2016; Chen than do rhizosphere microbes. They can also facilitate the
et al., 2015; Glick, 2010; Arshad et al., 2007). These specific genes and phytoremediation performance by reducing the biotic and abiotic stress
enzymes make them candidates for utilizing organic xenobiotics as car- of the host plant. The whole stress-reducing process is controlled by the
bon and energy sources. The following section discusses the selected production of ACC-deaminase activity (e.g. Arshad et al., 2007; Saleem
paradigms of potential applications of plant and associated endophytic et al., 2007).
and rhizospheric bacteria, in order to shed light on the improvement The potential advantages of utilizing entophytic bacteria for im-
of rhizoremediation. proved phytoremediation were summarized by Ryan et al. (2008).
They concluded that: a) genetic manipulation of a catabolic pathway in-
volved in xenobiotic degradation was easier in bacteria than in plants;
4.1. Endophytic-plant partnerships b) quantitative gene expression analysis of catabolic genes of endo-
phytic populations related to the degradation of pollutants could help
Endophytic bacteria are known to colonize the internal tissues of to assess the efficiency of the bioremediation process; and c) toxic pol-
plants without serious consequences for their host (Feng et al., 2017; lutants imbibed by the plant could be degraded by endophytes inter-
Mitter et al., 2016). In fact, all plant species harbor endophytic bacteria nally and might reduce phytotoxic effects on herbivorous fauna near
by establishing symbiotic or commensalistic relationships (Lòpez- contaminated sites as well. Other studies address disadvantages
Fernàndez et al., 2016). Endophytic bacteria inhabit several plant tissues (Compant et al., 2016; Ma et al., 2016; Ryan et al., 2008). For instance,
including roots, stems, leaves, flowers and seeds (Hardoim et al., 2015). phytoremediation technology: a) is limited to shallow depths of con-
Such bacteria thrive in the root cortex and xylary elements and, most taminated soil; b) may be slower than chemical treatments; (c) is
importantly, they have a recognized ability to degrade and mineralize greatly influenced by choice of the plant species and may show seasonal
organic pollutants, potentially enhancing phytoremediation (Eevers et variations; (d) is limited by phytotoxic effects of toxic pollutants; and
al., 2016; Fatima et al., 2015; Weyens et al., 2009, 2010a, 2013). Endo- (e) contaminant residues in plants may enter the food chain.
phytic bacteria display beneficial effects on their host plants (Andreolli Another study (Vacheron et al., 2013) provides useful insights into
et al., 2013; Compant et al., 2016; Ma et al., 2016). They assimilate nutri- molecular mechanisms of endophytes' promotion of plant growth.
ents by phosphorous solubilization and synthesize siderophores (Afzal Given that endophytic bacteria harbor essential catabolic genes which
et al., 2014). They also promote plant growth by synthesizing phyto- enhance xenobiotic degradation because they are imbibed and
Table 3
Applications of plant-endophytic bacteria for remediation of organic contaminants in the soils.
Endophytic bacteria Plant association Pollutant type Case studies
Herbaspirillum sp. (K1) Wheat (Triticum aestivum) PCBs, TCP (Männistö et al., 2001)
Pseudomonas aeruginosa (R75) Wild rye (Elymus dauricus) Chlorobenzoic acids (Siciliano and Germida, 1998)
Pseudomonas putida (VM1450) Pea (Pisum sativum) Pesticide-2,4-D (Germaine et al., 2006)
Burkholderia cepacia (G4) Yellow lupine (Lupinus luteus) VOCs and toluene (Barac et al., 2004)
Burkholderia sp. (HU001) Willow (Salix spp.) Toluene (Weyens et al., 2013)
Burkholderia cepacia strain (FX2) Maize (Zea mays) Toluene (Wang et al., 2010)
Wheat (Triticum aestivum)
Pseudomonas sp. Poplar (Populus trichocarpa) MTBE, BTEX and TCE Germaine et al., 2004; (Moore et al., 2006)
Enterobacter sp. (PDN3) Poplar (Populus trichocarpa) BTEX (Kang et al., 2012)
Pseudomonas putida Pea (Pisum sativum) Naphthalene (Germaine et al., 2009)
Pseudomonas putida (W619-TCE) Poplar (Populus trichocarpa) TCE (Weyens et al., 2010a)
Bacillus cepacia (VM1468) Poplar (Populus trichocarpa) TCE (Weyens et al., 2010b)
Pseudomonas sp. (ITRI53 and MixRI75) Italian ryegrass (Lolium multiflorum) TPH (Afzal et al., 2012; Andria et al., 2009)
Enterobacter ludwigii strains Italian ryegrass (Lolium multiflorum) TPH (Yousaf et al., 2011)
Birdsfoot trefoil (Lotus carniculatus)
Alfalfa (Medicago sativa)
Pantoea sp. strain (ITSI10) Italian ryegrass (Lolium multiflorum) TPH (Yousaf et al., 2010)
Methylobacterium populi (BJ001) Poplar tissues (Populus deltoidesnigra) Explosives-TNT, RDX, HMX (Van Aken et al., 2004)
Achromobacter xylosoxidans Phragmites australis, Catechol and phenol (Ho et al., 2009)
Ipomoea aquatica
Vetiveria zizanioides
Sphingomonas sp. (D4) Cytisusstriatus Hexachlorocyclohexane (Becerra-Castro et al., 2013)
Consortium (CAP9) Agrostis 2,4,6-Trinitrotoluene (Thijs et al., 2014)
Enterobacter sp. (12J1) Wheat (Triticum aestivum) Pyrene (Sheng et al., 2008)
Maize (Zea mays)
Stenotrophomonas Sp. Zuchini (Cucurbita pepo) DDE and DDT (Eevers et al., 2016)
Sphingomonas sp.
Mesorhizobium sp. (HN3yfp) Ryegrass (Lolium multiflorum) Chlorpyrifos (Jabeen et al., 2016)
accumulated by the host plant, it is envisaged that the combined use of degradation of organic contaminants by combined usage of plant and
endophytic bacteria and plants would considerably improve remedia- rhizobacteria (Table 4). For example, alfalfa in association with Pseudo-
tion and increase the rate of degradation of a broad spectrum of contam- monas fluorescens sp. F113 and Arabidopsis with Pseudomonas putida
inants. Table 3 highlights the combined use of plants and endophytic Flav1-1 enhanced the degradation of several PCBs (Narasimhan et al.,
bacteria and their potential applications in degrading organic 2003; Villacieros et al., 2005). Mehmannavaz et al. (2002) also reported
contaminants. that the inoculating alfalfa with Sinorhizobium meliloti strain A-025, a
symbiotic N2-fixing rhizobacterium, enhanced the biotransformation
4.2. Rhizosphere-plant partnership of many polychlorinated biphenyls. Especially root exudates tended to
induce catabolic pathways within rhizospheric bacteria, promoting the
The rhizosphere serves as a microhabitat around roots and typically degradation of several organic pollutants. The composition of root exu-
extends 1–2 mm around them (Liu et al., 2014). Generally, vegetated dates differs among plants, and many plant species exude phenols that
soils have higher (10–100 times) microbial numbers and diversity com- enrich organic-pollutant-degrading bacteria in the rhizosphere (Salt et
pared to bulk soils (Hinsinger et al., 2005; Wenzel, 2009). The larger mi- al., 1998).
crobial biomass in the rhizosphere is a function of rhizodeposits – a set In degrading PCBs, the presence of salicylate in root exudates report-
of organic compounds released by plant roots. These organic com- edly induces the expression of the bphA gene encoding biphenyl
pounds are divided into exudates, secretions, mucilages and lysates, dioxygenase in Pseudomonas sp. Cam-1. Conversely, terpenes inhibit
all of which microbes can use as a carbon and energy source (Martin the same gene (Master and Mohn, 2001). The above-mentioned exam-
et al., 2014). Plant roots provide a favorable microenvironment to at- ples underline that plant-microbe interactions often have mutual bene-
tract chemotactic bacteria by secreting these organic compounds. fits for plants and rhizobacteria. Rhizobacteria capable of synthesizing
These organic compounds probably also change the physicochemical bio-surfactants have been shown to enhance the bioavailability of or-
properties of soils and potentially increase the bioavailability of pollut- ganic pollutants by releasing these pollutants from soil particles and ac-
ants. Moreover, plant roots can also secrete specific organic compounds celerating their degradation (Whitfield Åslund et al., 2010). These bio-
(terpenes, flavonoids, phenols) that are structurally analogous to cer- surfactants can help desorb many organic xenobiotics from soil parti-
tain organic contaminants (petroleum hydrocarbons). This phenome- cles. To date, rhizosphere engineering has attracted increasing interest
non can induce the expression of degrading genes and increase the by modifying this microenvironment with nutrient adjustment, exu-
abundance of the associated rhizospheric microbes (Xun et al., 2015). dates regulation and insertion of transgenic strains.
Such enhanced catabolic gene expression has been successfully uti-
lized for the mineralization, degradation and sequestration of many or- 4.3. Prediction and annotation of genome sequences of xenobiotic-
ganic pollutants (Andria et al., 2009; Yousaf et al., 2010; Meier et al., degrading bacteria
2016). Initially, rhizobacteria were extensively studied in agriculture
to improve plant-microbe interactions and help reduce stress and en- Integration of various bioinformatics tools and molecular biology as
hance growth and yield (Bhattacharyya and Jha, 2012; Saleem et al., well as biochemistry databases has recently been discussed by Arora
2007). This concept garnered special attention in remediation trials de- and Bae (2014). The field of bioremediation and biodegradation has en-
signed to improve the phytoremediation efficiency of organic xenobi- tered the (meta) omics era (from genomics to metabolomics) with re-
otics (Yang et al., 2009). Recent studies demonstrated the potential cent advances being made in next generation sequencing (NGS).
application of plant and rhizobacteria partnerships to clean up or- Many contaminant-degrading bacterial genome sequences have been
ganic-contaminated soils (Abhilash et al., 2013; Brink, 2016; Qin et al., subjected to NGS technology, and subsequent genes related to contam-
2014; Singh et al., 2016). Several studies have reported the improved inant degradation have been identified by in silico prediction and
Table 4
Case studies of successful application of plant-rhizosphere bacteria for remediation of organic contaminants in the soils.
Rhizospheric bacteria Plant association Soil contaminant Case studies
Pseudomonas putida (Flav-1-1, PML2) Wall Cress (Arabidopsis thaliana) PCBs (Narasimhan et al., 2003)
Pseudomonas mendocina Black nightshade (Solanum PCBs (Ionescu et al., 2009)
nigrum)
Pseudomonas fluorescens Horseradish (Armoracia rusticana)
Bacillus pumilus Goat willow (Salix caprea)
Sphingobacterium mizutae Tobacco (Nicotiana tabaccum)
Burkholderia cepacia Alfalfa (Medicago sativa)
Burkholderia xenovorans (LB400) Austrian pine (Pinus nigra) PCBs (Leigh et al., 2006)
Goat willow (Salix caprea)
Sphingobium chlorophenolicum (ATCC 39723) Wheat (Triticum aestivum) Pentachlorophenol (Dams et al., 2007)
Streptomyces strains (M7, A5, A2, and A11) Maize (Zea mays) Lindane Pesticides (Álvarez et al., 2015)
Endosulfan degrading rhizospheric strains Khus (Vetiveria zizanioides) Endosulfan Pesticides (Singh et al., 2016)
(EAG-EC-12,13,14,15)
Pesticide tolerant rhizobacterial strains Okra (Abelmoschus esculentus) Bifenthrin Pesticide (Ahmad et al., 2015)
Sphingomonas herbicidovorans (AB042233) Maize (Zea mays) Hexachlorocyclo-hexane (Abhilash et al., 2013)
insecticide
Pseudomonas Sp. (ADP rifR) – Atrazine pesticides (Shaw et al., 2006; Silva et al.,
2004)
Pseudomonas putida (W619-TCE) Poplar (Populus deltoids) TCE (Weyens et al., 2015)
Indigenous degraders Switchgrass (Panicum virogatum) PCBs (Chekol et al., 2004)
Pseudomonas fluorescens (F113 Derivatives) Alfalfa (Medicago sativa) PCBs (Villacieros et al., 2005)
Rhizospheric bacterial strain (TP13) Tomato (Solanum lycopersicon) Phenol (Wang et al., 2014)
Indigenous microbes Alfalfa (Medicago sativa) Benzo[a]pyrene (Fu et al., 2012)
Bacterial consortia Maize (Zea mays) Petroleum hydrocarbons (Shahzad et al., 2016)
Fungal rhizospheric strain (Rhizophagus irregularis) Wheat (Triticum estivum) PAHs (Ingrid et al., 2016)
Indigenous degraders Italian ryegrass (Lolium perenne) Pentachlorophenol (He et al., 2005)
Azospirillum lipoferum Wheat (Triticum estivum) Petroleum hydrocarbons (Muratova et al., 2012)
Azospirillum brasilense Tall fescue (Festuca arundinacea) PAHs (Huang et al., 2004)
Enterobacter cloacae (CAL 2)
Pseudomonas putida (UW3, PCL1444)
Pseudomonas putida PCL1444 Bermuda grass (Lolium Naphthalene (Kuiper et al., 2004)
multiflorum)
annotation of metabolic pathways. This has improved our holistic un- al., 1999). For example, Misra and Gedamu (1989) reported Nicotiana
derstanding of the metabolic network of an interesting bacterium (Lee tabaccum as a transgenic plant expressing a metallotheionein gene for
et al., 2012; Schneiker et al., 2006; Vikram et al., 2013 ; Kumar et al., higher tolerance to and uptake of cadmium. Tobacco (Solanum nigrum)
2012; Vilchez-Vargas et al., 2013). For instance, analysis of the complete was the first to be used as a genetically modified plant for organic xeno-
genome sequence revealed that Cupriavidus necator JMP134, which uti- biotics such as explosives and halogenated organics (French et al., 1999
lizes aromatic substituted compounds as the sole carbon and energy and Doty et al., 2000). This species was modified to contain transgenes
source, encompasses 300 genes related to degradation pathways for for metabolizing xenobiotics and increasing resistance against pollut-
various aromatic contaminants (Perez-Pantoja et al., 2008; Lykidis et ants. The literature extensively documents the efficiency of transgenic
al., 2010). Another in silico study identified aromatic degradation path- plants in removing chlorinated biphenyl, explosives and phenolic com-
ways such as an ortho-pathway for protocatechuate and catechol, pounds (Abhilash et al., 2009; Aken and Doty, 2009; Eapen et al., 2007).
phenylacetate, homogentisate and N-heterocyclic aromatic pathways
in the genome of Pseudomonas putida KT2440 (Jiménez et al., 2002).
The complete genome sequences have not only helped to predict 5.1. Transgenic plants for stimulated phytodegradation/rhizodegradation of
genes and their functions but also to identify novel biocatalysts for bio- organic pollutants
degradation (Vilchez-Vargas et al., 2013). Kim et al. (2008) integrated
genomic, proteomic and metabolomic approaches and identified 27 en- 5.1.1. Herbicides and pesticides
zymes to construct the complete metabolic pathway for pyrene degra- In the agricultural sector, herbicides have become paramount in
dation in Mycobacterium vanbaalenii PYR-1. preventing yield losses of valuable crops by weed infestation
(Kawahigashi et al., 2008; Keller et al., 2014). These herbicides, how-
5. Transgenic plants for remediation of organic contaminants ever, can damage the environment as pollutants (Gill and Garg, 2014;
Seth et al., 2012). Moreover, repeated application and extensive use
Despite many studies having reported the successful transfer of can lead to the development of herbicide-resistant weeds. This phe-
phytoremediation from the greenhouse to the field, this approach still nomenon requires applying ever greater quantities, polluting soils and
lacks widespread application. One possibility to overcome this might nearby water bodies (Kawahigashi et al., 2006, 2007). Consequently,
be to develop transgenic plants to metabolize/degrade organic xenobi- there is an urgent need for the detoxification of herbicides from polluted
otics as well as to improve the ability of plants to complete the whole environments. Transgenic plants tolerant to herbicides have been suc-
process more rapidly. Identifying suitable genes for enhancing the deg- cessfully developed and used in agriculture for many years. Among di-
radation/mineralization of xenobiotic pollutants, followed by their iso- verse enzymatic groups, two major enzymes known as cytochrome
lation and transformation to a candidate plant, are the key steps P450 and glutathione S-transferase are key players for enhanced herbi-
during the development of transgenic plants. Initially, transgenic plants cidal degradation (Duhoux et al., 2015). For example, the chemical con-
were produced to reduce insect damage as well as increase crop yields tamination by agrochemicals can be reduced by introducing transgenic
in agriculture (Abhilash et al., 2009). They later gained acceptance in en- plants (Macek et al., 2008). Similar findings were reported by
vironmental sciences and were initially used in remediating heavy Kawahigashi et al. (2006), who studied rice plants showing overexpres-
metal-contaminated soils (Misra and Gedamu, 1989; Vatamaniuk et sion of transgenes such as CYP1A1, CYP2B6 and CYP2C19. The results
demonstrated that transgenic rice plants were more tolerant to herbi- confirmed the suitability of the bacterial gene (dhlAB) from
cides than non-transgenic plants due to an adapted metabolism. Xanthobacter for removing 1, 2-dichlorethene in plants. After successful
Transgenic rice plants carrying CYP1A1 showed herbicide tolerance metabolism of TCE by transgenic tobacco plants (640-fold increase
towards atrazine, diuron, quizalofop-ethyl, and other herbicides and versus non-transgenic plants), introducing P450 2E1 in deep-rooted,
they reduced the levels of atrazine and simazine in hydroponic solutions fast-growing trees was suggested by Doty et al. (2000). It may stimulate
(Kawahigashi et al., 2007). Small-scale batch and meso-scale green- the uptake and dissipation of these organic contaminants. Use of
house experiments confirmed the ability of transgenic rice plants carry- bacteria genes (XplA and XplB) from Rhodococcus conferred enhanced
ing the CYP2B6 gene to reduce residual quantities of a group of removal of RDX in plants (Jackson et al., 2007). Similarly, a transgenic
herbicides in soil and water (Kawahigashi et al., 2005a,b). Sixteen cyto- hybrid poplar having overexpression of a rabbit gene (CYP450 2E1)
chrome P450 species responsible for herbicide detoxification in Lolium served to boost the removal of TCE, vinyl chloride, carbon tetrachloride,
rigidum were reported by Fischer et al. (2001). Transgenic rice (having benzene and chloroform from hydroponic solution (Doty et al., 2007).
a human gene CYP1A1) showed increased tolerance and degradation Explosive pollutants are toxic and persistent in the environment at
activities on 10 of 13 herbicides belonging to different chemical groups military sites worldwide, where they can cause serious problems in
(Kawahigashi et al., 2008). Transgenic plants used for selected herbi- soil and groundwater (Seth et al., 2012). Among explosives, nitro-
cides and pesticides are summarized in Table 5. substituted compounds such as 2, 4, 6-trinitrotoluene (TNT),
hexahydro-1, 3,5-trinitro-1,3,5-triazine (RDX) and glycerol trinitrate
5.1.2. Halogenated organic compounds and explosives (GTN) are listed as ‘priority pollutants’ and ‘possible human carcino-
Halogenated organic compounds comprise a group of organic com- gens’ by the U.S. EPA (Singh, 2013). Based on the literature, Yew et al.
pounds containing halogen atoms. They include common environmen- (2016) documented that nitro-substituted explosives are toxic for all
tal pollutants such as chloroform, benzene, tetrachloride, vinyl chloride classes of organisms (bacteria, algae, plants and mammals). Traditional
and trichloroethylene (TCE). All can cause serious health problems and remediation techniques of explosives-contaminated sites are costly,
are reported as being carcinogenic, neurotoxic and hepatotoxic (Chiu et damaging to the environment and practically not feasible (Kiiskila et
al., 2013). TCE and its derivative vinyl chloride (produced by microbial al., 2015). As one of the top ten technologies for improving human
respiration) are heavily used in many industries and can persist in the health, phytoremediation is an attractive alternative due to its
environment for decades (Doty et al., 2017). Another very important ecological and environmental benefits (Kiiskila et al., 2015; Daar et al.,
halogenated organic compound, ethylene dibromide (EDB), is used as 2002).
a fumigant and gasoline additive. Chloroform, a famous disinfection For enhanced utilization of phytoremediation in the remediation of
agent to treat drinking water, is also considered a harmful pollutant organic contaminants, different approaches may be combined in an in-
(Huang et al., 2014). A very common pollutant associated with petro- tegrated manner rather than focusing solely on endophytic/
leum industries, benzene, is a proven human carcinogen (Bahadar et rhizospheric plant partnerships and transgenic plants. These
al., 2014). approaches include the use of agronomic practices, omics technolo-
To remediate such pollutants and many others, CYP2E1 is an exten- gies, transgenic, somaclonal variants and mutant lines. Recently,
sively studied cytochrome that can be used in transgenic plants (Zhang Gerhardt et al. (2017) reviewed all the above-mentioned approaches
et al., 2013; Abhilash et al., 2009). Transgenic tobacco plants (having and their usage in phytoremediation. Thijs et al. (2016) recently pro-
human cytochrome) can metabolize TCE, vinyl chloride, chloroform, posed the concept of engineering the metaorganisms to improve
toluene and benzene (Doty et al., 2000; Doty, 2008). The same studies phytoremediation at the field scale.
Table 5
Summary of transgenic plants used for selected herbicides and pesticides.
Target plant Gene (s) Enzymes involved Source Transgene effects References
Nicotiana tabaccum CYP105A1 Cytochrome Streptomyces Resistance to sulfonylurea (O'Keefe et al.,

P450 monoxygenase 1994)
Oryza sativa CYP2B6 Cytochrome Human Tolerance to group of herbicides (Hirose et al.,
P450 monoxygenase 2005)
Oryza sativa CYP2B22,CYP2C49 Cytochrome Pig Tolerance to several herbicides (Kawahigashi et
P450 monoxygenase al., 2006)
Nicotiana tabaccum CYP71A10 Cytochrome Glycine max Tolerance to phenyl urea herbicide (Siminszky et al.,
Arabidopsis thaliana P450 monoxygenase 1999)
Nicotiana tabaccum GstI-6His Glutathione S-transferases Maize Higher tolerance to variety of Aroclor (Karavangeli et al.,
(GST I) 2005)
Medicago sativa atzA Atrazine chlorohydrolase Bacteria Enhanced metabolic activity against atrazine (Wang et al.,
Nicotiana tabaccum 2005)
Arabidopsis thaliana Mn peroxidase Peroxidases Coriolus versicolor Enhanced removal of pentachlorophenol (PCP) (Iimura and Ka,
Nicotiana tabaccum gene 2002)
Oryza sativa Protox Protoporphyrinogen IX Bacillus subtilis Tolerance to diphenyl ether herbicide (Jung et al., 2008)
oxidase
Nicotiana tabaccum CYP1A1 Cytochrome Human Enhanced metabolic activity again metamitron Bode et al.,2004a
CYP1A2 P450 monoxygenase
Nicotiana tabaccum CYP1A1 Cytochrome Human Enhanced metabolic activity again atrazine (Ma et al., 2013)
CYP1A2 P450 monoxygenase
Nicotiana tabaccum CYP76B1 Cytochrome Helianthus tuberosus Tolerance to herbicide (Didierjean, 2002)
Arabidopsis thaliana P450 monoxygenase
Solanum tuberosum CYP1A1 Cytochrome Human Enhanced tolerance and metabolism of (Inui et al., 1999)
P450 monooxygenases herbicides
Solanum tuberosum CYP1A1, CYP2B6, Cytochrome Human Enhanced tolerance and metabolism of (Inui et al., 2000)
CYP2C19 P450 monooxygenases herbicides
Oryza sativa CYP1A1 Cytochrome P450 Human Enhanced herbicide metabolism (Kawahigashi,
monooxygenases 2009)
Nicotiana tabaccum ophc2 Organophosphorus Pseudomonas Enhanced degradation of organophosphorus (Wang et al.,
hydrolase (OPH) pseudoalcaligenes (methyl parathion). 2008)
6. Risks and mitigation through biotechnological advances associ- have degraded the contaminants. The proposed design integrates the
ated with using genetically modified plants and microbes killer–anti-killer genes, whose expression is triggered by the pollutant.
Upon pollutant degradation, killer genes are activated, eradicating the
Although the use of advanced recombinant DNA technology to pro- GEMs. These killer genes, located on plasmids, can also induce death
duce genetically modified organisms and the application of these mod- in the microbial recipient upon a gene transfer, therefore mitigating
ified microorganisms to remove environmental pollutants is very cost- horizontal gene transfer. Such bacterial containment systems are
effective and environmentally friendly approach, field releases of trans- among the most promising approaches to mitigate the undesirable af-
genic microorganisms have been quite limited due to risks in the open fects associated with the release of GEMs in the open environment
environment (Singh, 2013). Since the 1980s, advances in producing re- (Paul et al., 2005). For example, the lethal gef gene is located on the
combinant microbes has generated possible risks associated with the mini-Tn5 transposon regulated by the LacI repressor. Moreover, lacI
release of such genetically engineered microorganisms (GEMs) in the gene activation depends on the XylS positive activator, which is active
open environment (Singh et al., 2011). The regulatory hurdles in the re- only in the presence of 3-methylbenzoate. Therefore, the cell remains
lease of GEMs are mostly due to safety concerns, legislative issues and viable as long as 3-methylbenzoate is present. Depletion of the chemical
potential risks perceived by the public (Kritikos, 2018). For instance, signal may reflect degradation or escape into the environment; the cell
Chakrabarty et al. (1975) genetically engineered Burkholderia cepacia is killed by the action of the lethal gene gef (Davison et al., 2002; Torres
to remove Agent Orange at the U.S. Air Force storage facility but failed et al., 2003).
to receive approval for a field application because it raised concerns re- A major drawback of the containment systems is that cells in some
garding its potential impact on the environment. Two international or- cases may cease to respond to the toxic effect of the lethal gene if muta-
ganizations, the United Nations Environmental Program (UNEP) and tion occurs. To circumvent this problem, double-contained strains have
the Organization for Economic Co-operation and Development been designed. For example the asd gene encodes diaminopimelic acid
(OECD), are involved in the regulatory framework of genetically modi- synthesis, which is essential for cell wall synthesis. Pseudomonas putida
fied organisms (GMOs) or living modified organisms (LMOs). In prac- with a deletion of the asd gene was complemented with an external asd
tice, experimental studies related to the risk assessment often do not gene under an XylS positive activator, the same activator that sup-
incorporate all the norms suggested by regulatory agencies. It was presses gef expression as described above. Thus, a strain deprived of 3-
strongly suggested that the fate of the recombinant genes of the candi- methylbenzoate would die not only as a result of the lethal activity of
date strain has to be assessed in comparison to the corresponding wild- the gef protein but also due to the lack of diaminopimelic acid
type strain in the containment system (characterized by all relevant (Ronchel and Ramos, 2001). These advanced technologies serve as a
field conditions) prior to its release. More importantly, the heterologous good platform for future studies and may be introduced in the environ-
gene in the host genome should not display horizontal transfer to any ment to control the proliferation of genetically modified microorgan-
large extent (Smith et al., 1992). The other challenges include assessing isms after they fulfill the purpose of biodegrading pollutants.
the possible risks on ecosystem diversity and function.
Many microbial organisms commonly used for bioremediation may
have harmful impacts. For example, Burkholderia cepacia has bioremedi- 7. Conclusions and recommendations
ation potential for toxic nitro-compounds; however, it has also been
identified as a causative agent of cystic fibrosis in humans and also pre- Organic xenobiotics are ever-increasing in the environment due to
sented multiple antibiotic resistances. For this reason the U.S. EPA raised rapid industrialization, population increase, mechanized agricultural
concerns over its use as an environmental protection agent. Another ex- practices and military activities. Rapid environmental clean-up and sta-
ample is the biodegradation of toluene, which is mediated by the unreg- bilization of organic xenobiotics is highly desirable to support the sus-
ulated activity of efflux pumps in Pseudomonas. Since these pumps tainability of natural ecosystems. The presence of plants and
pump out various antibiotics and biocides (Davison, 2005), selecting associated microbes in contaminated areas is due to the xenobiotic-re-
such microbes may increase the risk of introducing multidrug-resistant sistant genes they naturally contain; these genes help chelate, traffic
bacteria into the environment and may eventually spread and produce and sequestrate xenobiotics. The biological approaches involving use
more virulent progeny (Davison, 2005). Another major concern in the of efficient plants and rhizobacteria/genetically engineered microbes
development of recombinant microbial systems is the horizontal trans- are always safer and preferable over costly physicochemical methods
fer of heterologous genes among the host organism and other closely re- of environmental remediation.
lated species living nearby. This may involve transduction and The bottleneck in using such biological techniques is the slow
conjugation. DNA transfer may occur even among interspecies under growth kinetics of microbial metabolism, which may be caused by envi-
different ecological conditions. ronmental factors or even inhibited by pollutants. The result is an accu-
One of the major challenges related to both the public and scientific mulation of these pollutants of concern. To overcome these challenges,
communities is the containment of recombinant microbes after comple- future research must be directed towards developing efficiently grow-
tion of the bioremediation process to minimize undesirable environ- ing rhizobacterial species capable of promoting growth of associated
mental outcomes (Khan et al., 2016; Prakash et al., 2011). These plant species. Such combinations would greatly improve environmental
concerns reflect the capability of such GEMs to disrupt ecosystems by remediation. Bioremediation efficiency can be optimized by inserting
further spreading after the degradation of the pollutant. To tackle special features into the respective microbes. The required traits in mi-
these risks, attempts are being made to control and track GEMs, and a crobes can be inserted via natural gene transfer or recombinant DNA/
set of guidelines has been proposed by the International Technical RNA technology. Phytoremediation efficiency can be augmented by im-
Guidelines for Safety in Biotechnology for microorganisms. proving plant-microbe interactions via rhizosphere engineering. Syner-
Designing GEMs by applying suitable genetic approaches to contain gistic use of suitable plants and efficient microbes can greatly enhance
the bacterial system may help minimize the anticipated risks. For in- remediation efficiency. Furthermore, this partnership can also be in-
stance, transposition vectors constructed without antibiotic-resistant creased by inoculating seeds/plants with specific endophytic and
genes are considered to be safe in the environment. Another contain- rhizospheric microbes. Microbial strains having both features – plant-
ment approach mainly involves designing “suicidal GEMs”, but the tech- growth-promoting as well as contaminant-degrading abilities – offer
nology has yet to be put into practice (Chamekh, 2015). This concept an efficient, cost-effective and environmentally safer option for biore-
involves programming the death of GEMs after toxin degradation in mediation and phytoremediation. Lastly, the use of genetically modified
the target site (Paul et al., 2005). Based on this concept, a genetic design plants can further exploit this plant microbe partnership and offer time-
model was recently developed to control the fate of the GEMs after they efficient remediation options.
Environmental biotechnology can promote the study of the specific Álvarez, A., Benimeli, C.S., Saez, J.M., Giuliano, A., Amoroso, M.J., 2015. Lindane removal
using Streptomyces strains and maize plants: a biological system for reducing pesti-
genes responsible for xenobiotic resistance and for the nature of the up- cides in soils. Plant Soil 395, 401–413.
take, accumulation and detoxification pathways of xenobiotics. There- Andreolli, M., Lampis, S., Poli, M., Gullner, G., Biró, B., Vallini, G., 2013. Endophytic
fore, xenobiotic-resistant and tolerant accumulator plants and Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic
aromatic hydrocarbons. Chemosphere 92, 688–694.
associated microbial species can be isolated and further modified for Andria, V., Reichenauer, T.G., Sessitsch, A., 2009. Expression of alkane monooxygenase
the decontamination of polluted sites by using DNA and RNA recombi- (alkB) genes by plant-associated bacteria in the rhizosphere and endosphere of Ital-
nant technologies, which tackle xenobiotics by activating the responsive ian ryegrass (Lolium multiflorum L.) grown in diesel contaminated soil. Environ.
Pollut. 157, 3347–3350.
genes of the respective organisms. Another helpful approach for the ex- Ang, E.L., Zhao, H., Obbard, J.P., 2005. Recent advances in the bioremediation of persistent
ploration and activation of stress-related genes is to investigate extra- organic pollutants via biomolecular engineering. Enzym. Microb. Technol. 37,
cellular and intracellular signal transduction processes of such plants 487–496.
Arora, P.K., Bae, H., 2014. Bacterial degradation of chlorophenols and their derivatives.
and microbes. This can be done by using the Ca calmodulin system, hor-
Microb. Cell Factories 13 (1), 31.
mones, ROS signaling, and the mitogen-activated protein kinase Arshad, M., Saleem, M., Hussain, S., 2007. Perspectives of bacterial ACC deaminase in
(MAPK) phosphorylation flow. Such strategies can open a gateway for phytoremediation. Trends Biotechnol. 25, 356–362.
a more thorough understanding and improvement of phytoremediation Arslan, M., Imran, A., Khan, Q.M., Afzal, M., 2015. Plant–bacteria partnerships for the re-
mediation of persistent organic pollutants. Environ. Sci. Pollut. Res. 15 (276(2)),
techniques. 83–94.
Another challenge of future research will be to counteract the pro- Asim Shahzad, A.B., 2015. Rhizodegradation of hydrocarbon from oily sludge.
duction of undesirable proteins (enzymes) that potentially disturb the J. Bioremediation Biodegrad. 6.
Badri, D.V., Weir, T.L., van der Lelie, D., Vivanco, J.M., 2009. Rhizosphere chemical dia-
functioning of the rhizosphere community or the metabolism in plants. logues: plant–microbe interactions. Curr. Opin. Biotechnol. 20, 642–650.
Using genetically modified microbes and plants poses risks in the open Bahadar, H., Mostafalou, S., Abdollahi, M., 2014. Current understandings and perspectives
environment. The regulatory hurdles regarding their release are mostly on non-cancer health effects of benzene: a global concern. Toxicol. Appl. Pharmacol.
276 (2), 83–94.
due to safety concerns, legislative issues and public perceptions. The po- Barac, T., Taghavi, S., Borremans, B., Provoost, A., Oeyen, L., Colpaert, J.V., Vangronsveld, J.,
tential risks associated with altered microbes and plants can be tackled van der Lelie, D., 2004. Engineered endophytic bacteria improve phytoremediation of
by adhering to regulatory guidelines and applying biotechnological ad- water-soluble, volatile, organic pollutants. Nat. Biotechnol. 22, 583–588.
Barriault, D., Plante, M.-M., Sylvestre, M., 2002. Family shuffling of a targeted bphA region
vances. Certain risks may still come to light and would then require fur- to engineer biphenyl dioxygenase. J. Bacteriol. 184, 3794–3800.
ther investigation to generate appropriate technical regulatory Bathe, S., Schwarzenbeck, N., Hausner, M., 2009. Bioaugmentation of activated sludge to-
guidelines. wards 3-chloroaniline removal with a mixed bacterial population carrying a degrada-
tive plasmid. Bioresour. Technol. 100, 2902–2909.
Becerra-Castro, C., Kidd, P.S., Rodríguez-Garrido, B., Monterroso, C., Santos-Ucha, P.,
Prieto-Fernández, Á., 2013. Phytoremediation of hexachlorocyclohexane (HCH)-con-
Acknowledgments taminated soils using Cytisus striatus and bacterial inoculants in soils with distinct or-
ganic matter content. Environ. Pollut. 178, 202–210.
Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and
This work was partly funded by AIT Austrian Institute of Technology plant health. Trends Plant Sci. 17, 478–486.
(project number 1.G2.00126.0.0) Vienna, Austria, Department of Health Beyer, A., Mackay, D., Matthies, M., Wania, F., Webster, E., 2000. Assessing long-range
and Environment, under the umbrella of business unit Environmental transport potential of persistent organic pollutants. Environ. Sci. Technol. 34,
699–703.
Resources and Technologies. Imran Hussain gratefully acknowledges Bhattacharyya, P.N., Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR): emer-
the Higher Education Commission (HEC Overseas Scholarship Phase I, gence in agriculture. World J. Microbiol. Biotechnol. 28, 1327–1350.
Batch 4) of Pakistan for financial support during his four-year stay for Brazil, G.M., Kenefick, L., Callanan, M., Haro, A., De Lorenzo, V., Dowling, D.N., O'gara, F.,
1995. Construction of a rhizosphere pseudomonad with potential to degrade
undertaking a doctoral degree in Vienna. polychlorinated biphenyls and detection of bph gene expression in the rhizosphere.
Appl. Environ. Microbiol. 61, 1946–1952.
References Brink, S.C., 2016. Unlocking the secrets of the rhizosphere. Trends Plant Sci. 21, 169–170.
Brinkmann, U., Reineke, W., 1992. Degradation of chlorotoluenes by in vivo constructed
Abhilash, P.C., Jamil, S., Singh, N., 2009. Transgenic plants for enhanced biodegradation hybrid strains: problems of enzyme specificity, induction and prevention of meta-
and phytoremediation of organic xenobiotics. Biotechnol. Adv. 27, 474–488. pathway. FEMS Microbiol. Lett. 96, 81–87.
Abhilash, P.C., Powell, J.R., Singh, H.B., Singh, B.K., 2012. Plant–microbe interactions: novel Burges, A., Epelde, L., Benito, G., Artetxe, U., Becerril, J.M., Garbisu, C., 2016. Enhancement
applications for exploitation in multipurpose remediation technologies. Trends of ecosystem services during endophyte-assisted aided phytostabilization of metal
Biotechnol. 30, 416–420. contaminated mine soil. Sci. Total Environ. 562, 480–492.
Abhilash, P.C., Singh, B., Srivastava, P., Schaeffer, A., Singh, N., 2013. Remediation of lin- Cachada, A., Pato, P., Rocha-Santos, T., da Silva, E.F., Duarte, A.C., 2012. Levels, sources and
dane by Jatropha curcas L: utilization of multipurpose species for rhizoremediation. potential human health risks of organic pollutants in urban soils. Sci. Total Environ.
Biomass Bioenergy 51, 189–193. 430, 184–192.
Abril, M.A., Michan, C., Timmis, K.N., Ramos, J.L., 1989. Regulator and enzyme specificities Cao, Y., Yang, B., Song, Z., Wang, H., He, F., Han, X., 2016. Wheat straw biochar amend-
of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocar- ments on the removal of polycyclic aromatic hydrocarbons (PAHs) in contaminated
bons and expansion of the substrate range of the pathway. J. Bacteriol. 171, soil. Ecotoxicol. Environ. Saf. 130, 248–255.
6782–6790. Carmichael, A.B., Wong, L.-L., 2001. Protein engineering of Bacillus megaterium CYP102:
Afzal, M., 2010. Plant-Microbe Interactions for the Remediation of Hydrocarbon Contam- the oxidation of polycyclic aromatic hydrocarbons. Eur. J. Biochem. 268, 3117–3125.
inated Soil. Austrian Institute of Technology. Cetin, B., Ozturk, F., Keles, M., Yurdakul, S., 2017. PAHs and PCBs in an Eastern Mediterra-
Afzal, M., Yousaf, S., Reichenauer, T.G., Sessitsch, A., 2012. The inoculation method affects nean megacity, Istanbul: their spatial and temporal distributions, air-soil exchange
colonization and performance of bacterial inoculant strains in the phytoremediation and toxicological effects. Environ. Pollut. 220, 1322–1332.
of soil contaminated with diesel oil. Int. J. Phytoremediation 14, 35–47. Chakrabarty, A.M., Mylroie, J.R., Friello, D.A., Vacca, J.G., 1975. Transformation of Pseudo-
Afzal, M., Khan, Q.M., Sessitsch, A., 2014. Endophytic bacteria: prospects and applications monas putida and Escherichia coli with plasmid-linked drug-resistance factor DNA.
for the phytoremediation of organic pollutants. Chemosphere 117, 232–242. Proc. Natl. Acad. Sci. 72 (9), 3647–3651.
Ahmad, M., Akhtar, M.F.-Z., Jamil, M., Latif, M., Ahmad, I., et al., 2015. Pesticide tolerant plant Chakraborty, J., Das, S., 2016. Molecular perspectives and recent advances in microbial re-
growth promoting rhizobacteria isolated from rhizosphere of okra. Soil Environ. 32. mediation of persistent organic pollutants. Environ. Sci. Pollut. Res. 23 (17),
Aken, B.V., Doty, S.L., 2009. Transgenic plants and associated bacteria for 16883–16903.
phytoremediation of chlorinated compounds. Biotechnol. Genet. Eng. Rev. 26, 43–64. Chamekh, M., 2015. Genetically engineered bacteria in gene therapy—hopes and chal-
Al-Baldawi, I.A., Abdullah, S.R.S., Anuar, N., Suja, F., Mushrifah, I., 2015. Phytodegradation lenges. Gene Therapy-Principles and Challenges. InTech.
of total petroleum hydrocarbon (TPH) in diesel-contaminated water using Scirpus Chaudhry, Q., Blom-Zandstra, M., Gupta, S.K., Joner, E., 2005. Utilising the synergy be-
grossus. Ecol. Eng. 74, 463–473. tween plants and rhizosphere microorganisms to enhance breakdown of organic pol-
Alexander, M., 2000. Aging, bioavailability, and overestimation of risk from environmen- lutants in the environment (15 pp). Environ. Sci. Pollut. Res. Int. 12, 34–48.
tal pollutants. Environ. Sci. Technol. 34, 4259–4265. Chauhan, A., Fazlurrahman, Oakeshott, J.G., Jain, R.K., 2008. Bacterial metabolism of poly-
Ali, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metals—concepts and appli- cyclic aromatic hydrocarbons: strategies for bioremediation. Indian J. Microbiol. 48,
cations. Chemosphere 91, 869–881. 95–113.
Ali, A., Zinnert, J.C., Muthukumar, B., Peng, Y., Chung, S.-M., Stewart, C.N., 2014. Chebbi, A., Hentati, D., Zaghden, H., Baccar, N., Rezgui, F., Chalbi, M., Chamkha, M., 2017.
Physiological and transcriptional responses of Baccharis halimifolia to the Polycyclic aromatic hydrocarbon degradation and biosurfactant production by a
explosive “composition B” (RDX/TNT) in amended soil. Environ. Sci. Pollut. Res. newly isolated Pseudomonas sp. strain from used motor oil-contaminated soil. Int.
21, 8261–8270. Biodeterior. Biodegrad. 122, 128–140.
Chekol, T., Vough, L.R., Chaney, R.L., 2004. Phytoremediation of polychlorinated biphenyl- Eapen, S., Singh, S., D'Souza, S.F., 2007. Advances in development of transgenic plants for
contaminated soils: the rhizosphere effect. Environ. Int. 30, 799–804. remediation of xenobiotic pollutants. Biotechnol. Adv. 25, 442–451.
Chen, B., Zhou, D., Zhu, L., Shen, X., 2008. Sorption characteristics and mechanisms of or- Eevers, N., Hawthorne, J.R., White, J.C., Vangronsveld, J., Weyens, N., 2016. Exposure of
ganic contaminant to carbonaceous biosorbents in aqueous solution. Sci. China Ser. B Cucurbita pepo to DDE-contamination alters the endophytic community: a cultivation
Chem. 51, 464–472. dependent vs a cultivation independent approach. Environ. Pollut. 209, 147–154.
Chen, M., Xu, P., Zeng, G., Yang, C., Huang, D., Zhang, J., 2015. Bioremediation of soils con- Erakhrumen, A.A., 2011. Research advances in bioremediation of soils and groundwater
taminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, using plant-based systems: a case for enlarging and updating information and knowl-
chlorophenols and heavy metals by composting: applications, microbes and future edge in environmental pollution management in developing countries. In: Khan, M.S.,
research needs. Biotechnol. Adv. 33, 745–755. Zaidi, A., Goel, R., Musarrat, J. (Eds.), Biomanagement of Metal-Contaminated Soils.
Cheng, M., Zeng, G., Huang, D., Yang, C., Lai, C., Zhang, C., Liu, Y., 2017. Tween 80 surfac- Dordrecht, Springer Netherlands, pp. 143–166.
tant-enhanced bioremediation: toward a solution to the soil contamination by hy- Erickson, B.D., Mondello, F.J., 1992. Nucleotide sequencing and transcriptional mapping of
drophobic organic compounds. Crit. Rev. Biotechnol. 1–14. the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphe-
Chen-Goodspeed, M., Sogorb, M.A., Wu, F., Raushel, F.M., 2001a. Enhancement, relaxation, nyl-degrading enzyme in Pseudomonas strain LB400. J. Bacteriol. 174, 2903–2912.
and reversal of the stereoselectivity for phosphotriesterase by rational evolution of Ezezika, O.C., Singer, P.A., 2010. Genetically engineered oil-eating microbes for bioremedi-
active site residues. Biochemistry (Mosc) 40, 1332–1339. ation: prospects and regulatory challenges. Technol. Soc. 32, 331–335.
Chen-Goodspeed, M., Sogorb, M.A., Wu, F., Hong, S.-B., Raushel, F.M., 2001b. Structural de- Fan, S., Li, P., Gong, Z., Ren, W., He, N., 2008. Promotion of pyrene degradation in rhizo-
terminants of the substrate and stereochemical specificity of phosphotriesterase. Bio- sphere of alfalfa (Medicago sativa L.). Chemosphere 71, 1593–1598.
chemistry (Mosc) 40, 1325–1331. Fasani, E., Manara, A., Martini, F., Furini, A., DalCorso, G., 2017. The potential of genetic en-
Chica, R.A., Doucet, N., Pelletier, J.N., 2005. Semi-rational approaches to engineering engineering of plants for the remediation of soils contaminated with heavy metals.
zyme activity: combining the benefits of directed evolution and rational design. Plant Cell Environ. https://doi.org/10.1111/pce.12963.
Curr. Opin. Biotechnol. 16, 378–384. Fatima, K., Afzal, M., Imran, A., Khan, Q.M., 2015. Bacterial rhizosphere and Endosphere
Chiu, W.A., Jinot, J., Scott, C.S., Makris, S.L., Cooper, G.S., Dzubow, R.C., ... Lipscomb, J.C., populations associated with grasses and trees to be used for phytoremediation of
2013. Human health effects of trichloroethylene: key findings and scientific issues. crude oil contaminated soil. Bull. Environ. Contam. Toxicol. 94, 314–320.
Environ. Health Perspect. 121 (3), 303. Feng, N.X., Yu, J., Zhao, H.M., Cheng, Y.T., Mo, C.H., Cai, Q.Y., Wong, M.H., 2017. Efficient
Coleman, J., Blake-Kalff, M., Davies, E., 1997. Detoxification of xenobiotics by plants: phytoremediation of organic contaminants in soils using plant–endophyte partner-
chemical modification and vacuolar compartmentation. Trends Plant Sci. 2 (4), ships. Sci. Total Environ. 583, 352–368.
144–151. Fernández-Cruz, T., Martínez-Carballo, E., Simal-Gándara, J., 2017. Perspective on pre-and
Collins, C.D., 2001. Implementing phytoremediation of petroleum hydrocarbons. post-natal agro-food exposure to persistent organic pollutants and their effects on
Phytoremediation - Methods and Reviews. 23, pp. 99–108. quality of life. Environ. Int. 100, 79–101.
Compant, S., Clément, C., Sessitsch, A., 2010. Plant growth-promoting bacteria in the Fischer, T.C., Klattig, J.T., Gierl, A., 2001. A general cloning strategy for divergent plant cy-
rhizo-and endosphere of plants: their role, colonization, mechanisms involved and tochrome P450 genes and its application in Lolium rigidum and Ocimum basilicum.
prospects for utilization. Soil Biol. Biochem. 42 (5), 669–678. Theor. Appl. Genet. 103 (6-7), 1014–1021.
Compant, S., Reiter, B., Sessitsch, A., Nowak, J., Clement, C., Ait Barka, E., 2005. Endophytic Flokstra, B.R., Aken, B.V., Schnoor, J.L., 2008. Microtox® toxicity test: detoxification of TNT
colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. and RDX contaminated solutions by poplar tissue cultures. Chemosphere 71,
strain PsJN. Appl. Environ. Microbiol. 71, 1685–1693. 1970–1976.
Compant, S., Saikkonen, K., Mitter, B., Campisano, A., Mercado-Blanco, J., 2016. Editorial French, C.E., Rosser, S.J., Davies, G.J., Nicklin, S., Bruce, N.C., 1999. Biodegradation of explo-
special issue: soil, plants and endophytes. Plant Soil 405, 1–11. sives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat.
Copaciu, F., Opriş, O., Niinemets, Ü., Copolovici, L., 2016. Toxic influence of key organic soil Biotechnol. 17 (5), 491.
pollutants on the total flavonoid content in wheat leaves. Water Air Soil Pollut. 227. Fu, D., Teng, Y., Luo, Y., Tu, C., Li, S., Li, Z., Christie, P., 2012. Effects of alfalfa and organic
Daar, A.S., Thorsteinsdóttir, H., Martin, D.K., Smith, A.C., Nast, S., Singer, P.A., 2002. Top ten fertilizer on benzo[a]pyrene dissipation in an aged contaminated soil. Environ. Sci.
biotechnologies for improving health in developing countries. Nat. Genet. 32, Pollut. Res. 19, 1605–1611.
229–232. Gao, G., Clare, A.S., Rose, C., Caldwell, G.S., 2017. Ulva rigida in the future ocean: potential
Dams, R.I., Paton, G.I., Killham, K., 2007. Rhizoremediation of pentachlorophenol by for carbon capture, bioremediation, and biomethane production. Gcb Bioenergy.
Sphingobium chlorophenolicum ATCC 39723. Chemosphere 68, 864–870. Gerhardt, K.E., Huang, X.-D., Glick, B.R., Greenberg, B.M., 2009. Phytoremediation and
Das, M., Adholeya, A., 2012. Role of microorganisms in remediation of contaminated soil. rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci.
In: Prakash, Anil, Satyanarayana, T., Johri, B.N. (Eds.), Microorganisms in Environmen- 176, 20–30.
tal Management. Springer Netherlands, Dordrecht, pp. 81–111. Gerhardt, K.E., Gerwing, P.D., Greenberg, B.M., 2016. Opinion: taking phytoremediation
Davison, J., 2005. Risk mitigation of genetically modified bacteria and plants designed for from proven technology to accepted practice. Plant Sci. 256, 170–185.
bioremediation. J. Ind. Microbiol. Biotechnol. 32 (11-12), 639–650. Gerhardt, K.E., MacNeill, G.J., Gerwing, P.D., Greenberg, B.M., 2017. Phytoremediation of
Davison, P.A., Hunter, C.N., Horton, P., 2002. Overexpression of β-carotene hydroxylase salt-impacted soils and use of plant growth-promoting rhizobacteria (PGPR) to en-
enhances stress tolerance in Arabidopsis. Nature 418 (6894), 203. hance phytoremediation. Phytoremediation. Springer International Publishing,
De Souza, M.L., Seffernick, J., Martinez, B., Sadowsky, M.J., Wackett, L.P., 1998. The atrazine pp. 19–51.
catabolism genes atzABC are widespread and highly conserved. J. Bacteriol. 180, Germida, J.J., Frick, C.M., Farrell, R.E., 2002. Phytoremediation of oil-contaminated soils.
1951–1954. Developments in soil science Vol. 28. Elsevier, pp. 169–186.
Dhankher, O.P., Pilon-Smits, E.A.H., Meagher, R.B., Doty, S., 2012. Biotechnological ap- Germaine, K., Keogh, E., Garcia-Cabellos, G., Borremans, B., Van Der Lelie, D., Barac, T.,
proaches for phytoremediation. Plant Biotechnology and Agriculture. Elsevier, Campbell, C.D., 2004. Colonisation of poplar trees by gfp expressing bacterial endo-
pp. 309–328. phytes. FEMS Microbiol. Ecol. 48 (1), 109–118.
Didierjean, L., 2002. Engineering herbicide metabolism in tobacco and arabidopsis with Germaine, K.J., Liu, X., Cabellos, G.G., Hogan, J.P., Ryan, D., Dowling, D.N., 2006. Bacterial
CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiol. 130, endophyte-enhanced phytoremediation of the organochlorine herbicide 2,4-
179–189. dichlorophenoxyacetic acid: bacterial endophyte-enhanced phytoremediation.
Dietz, A.C., Schnoor, J.L., 2001. Advances in phytoremediation. Environ. Health Perspect. FEMS Microbiol. Ecol. 57, 302–310.
109, 163. Germaine, K.J., Keogh, E., Ryan, D., Dowling, D.N., 2009. Bacterial endophyte-mediated
Dimitroula, H., Syranidou, E., Manousaki, E., Nikolaidis, N.P., Karatzas, G.P., Kalogerakis, N., naphthalene phytoprotection and phytoremediation. FEMS Microbiol. Lett. 296,
2015. Mitigation measures for chromium-VI contaminated groundwater – the role of 226–234.
endophytic bacteria in rhizofiltration. J. Hazard. Mater. 281, 114–120. Ghattas, A.K., Fischer, F., Wick, A., Ternes, T.A., 2017. Anaerobic biodegradation of (emerg-
Dixit, R., Malaviya, D., Pandiyan, K., Singh, U.B., Sahu, A., Shukla, R., ... Paul, D., 2015. Bio- ing) organic contaminants in the aquatic environment. Water Res. 116, 268–295.
remediation of heavy metals from soil and aquatic environment: an overview of prin- Ghosal, D., Ghosh, S., Dutta, T.K., Ahn, Y., 2016. Current state of knowledge in microbial degra-
ciples and criteria of fundamental processes. Sustainability 7 (2), 2189–2212. dation of polycyclic aromatic hydrocarbons (PAHs): a review. Front. Microbiol. 7.
Doty, S.L., 2008. Enhancing phytoremediation through the use of transgenics and endo- Ghosh, M., Singh, S.P., 2005. A comparative study of cadmium phytoextraction by accu-
phytes. New Phytol. 179 (2), 318–333. mulator and weed species. Environ. Pollut. 133, 365–371.
Doty, S.L., Freeman, J.L., Cohu, C.M., Burken, J.G., Firrincieli, A., Simon, A., ... Blaylock, M.J., Gilden, R.C., Huffling, K., Sattler, B., 2010. Pesticides and health risks. J. Obstet. Gynecol.
2017. Enhanced degradation of TCE on a superfund site using endophyte-assisted Neonatal. Nurs. 39, 103–110.
poplar tree phytoremediation. Environ. Sci. Technol. 51 (17), 10050–10058. Gill, H.K., Garg, H., 2014. Pesticides: environmental impacts and management strategies.
Doty, S.L., Shang, T.Q., Wilson, A.M., Tangen, J., Westergreen, A.D., Newman, L.A., ... Pesticides-toxic Aspects. InTech https://doi.org/10.5772/57399.
Gordon, M.P., 2000. Enhanced metabolism of halogenated hydrocarbons in trans- Gkorezis, P., Daghio, M., Franzetti, A., Van Hamme, J.D., Sillen, W., Vangronsveld, J., 2016.
genic plants containing mammalian cytochrome P450 2E1. Proc. Natl. Acad. Sci. 97 The interaction between plants and bacteria in the remediation of petroleum hydro-
(12), 6287–6291. carbons: an environmental perspective. Front. Microbiol. 7.
Douglas, T.A., Walsh, M.E., Weiss, C.A., McGrath, C.J., Trainor, T.P., 2012. Desorption and Glick, B.R., 2010. Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv. 28,
transformation of nitroaromatic (TNT) and nitramine (RDX and HMX) explosive res- 367–374.
idues on detonated pure mineral phases. Water Air Soil Pollut. 223, 2189–2200. Gomes, H.I., Dias-Ferreira, C., Ribeiro, A.B., 2013. Overview of in situ and ex situ remedia-
Duhoux, A., Carrère, S., Gouzy, J., Bonin, L., Délye, C., 2015. RNA-Seq analysis of rye-grass tion technologies for PCB-contaminated soils and sediments and obstacles for full-
transcriptomic response to an herbicide inhibiting acetolactate-synthase identifies tran- scale application. Sci. Total Environ. 445, 237–260.
scripts linked to non-target-site-based resistance. Plant Mol. Biol. 87 (4–5), 473–487. Haffner, D., Schecter, A., 2014. Persistent organic pollutants (POPs): a primer for practic-
Dzantor, E.K., 2007. Phytoremediation: the state of rhizosphere “engineering” for acceler- ing clinicians. Curr. Environ. Health Rep. 1, 123–131.
ated rhizodegradation of xenobiotic contaminants. J. Chem. Technol. Biotechnol. 82, Hardoim, P.R., Van Overbeek, L.S., Berg, G., Pirttilä, A.M., Compant, S., Campisano, A., ...
228–232. Sessitsch, A., 2015. The hidden world within plants: ecological and evolutionary
considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Jussila, M.M., Zhao, J., Suominen, L., Lindström, K., 2007. TOL plasmid transfer during bac-
Rev. 79 (3), 293–320. terial conjugation in vitro and rhizoremediation of oil compounds in vivo. Environ.
Harford-Cross, C.F., Carmichael, A.B., Allan, F.K., England, P.A., Rouch, D.A., Wong, L.L., Pollut. 146, 510–524.
2000. Protein engineering of cytochrome P450cam (CYP101) for the oxidation of Kang, J.W., 2014. Removing environmental organic pollutants with bioremediation and
polycyclic aromatic hydrocarbons. Protein Eng. 13 (2), 121–128. phytoremediation. Biotechnol. Lett. 36, 1129–1139.
Hartmann, J., Reineke, W., Knackmuss, H.J., 1979. Metabolism of 3-chloro-, 4-chloro-, Kang, J.W., Khan, Z., Doty, S.L., 2012. Biodegradation of trichloroethylene by an endophyte
and 3, 5-dichlorobenzoate by a pseudomonad. Appl. Environ. Microbiol. 37 (3), of hybrid poplar. Appl. Environ. Microbiol. 78, 3504–3507.
421–428. Karavangeli, M., Labrou, N.E., Clonis, Y.D., Tsaftaris, A., 2005. Development of transgenic
He, Y., Xu, J., Tang, C., Wu, Y., 2005. Facilitation of pentachlorophenol degradation in tobacco plants overexpressing maize glutathione S-transferase I for chloroacetanilide
the rhizosphere of ryegrass (Lolium perenne L.). Soil Biol. Biochem. 37, herbicides phytoremediation. Biomol. Eng. 22, 121–128.
2017–2024. Kästner, M., Miltner, A., 2016. Application of compost for effective bioremediation of or-
Hinsinger, P., Gobran, G.R., Gregory, P.J., Wenzel, W.W., 2005. Rhizosphere geometry and ganic contaminants and pollutants in soil. Appl. Microbiol. Biotechnol. 100 (8),
heterogeneity arising from root-mediated physical and chemical processes: research 3433–3449.
review. New Phytol. 168, 293–303. Kawahigashi, H., Hirose, S., Inui, H., Ohkawa, H., Ohkawa, Y., 2005a. Enhanced herbicide
Hirose, S., Kawahigashi, H., Ozawa, K., Shiota, N., Inui, H., Ohkawa, H., Ohkawa, Y., 2005. cross-tolerance in transgenic rice plants co-expressing human CYP1A1, CYP2B6,
Transgenic rice containing human CYP2B6 detoxifies various classes of herbicides. and CYP2C19. Plant Sci. 168 (3), 773–781.
J. Agric. Food Chem. 53, 3461–3467. Kawahigashi, H., Hirose, S., Ozawa, K., Ido, Y., Kojima, M., Ohkawa, H., Ohkawa, Y., 2005b.
Hlihor, R.M., Apostol, L.C., Gavrilescu, M., 2017a. Environmental bioremediation by Analysis of substrate specificity of pig CYP2B22 and CYP2C49 towards herbicides by
biosorption and bioaccumulation: principles and applications. Enhancing Cleanup transgenic rice plants. Transgenic Res. 14 (6), 907–917.
of Environmental Pollutants. Springer International Publishing, pp. 289–315. Kawahigashi, H., 2009. Transgenic plants for phytoremediation of herbicides. Curr. Opin.
Hlihor, R.M., Gavrilescu, M., Tavares, T., Favier, L., Olivieri, G., 2017b. Bioremediation: an Biotechnol. 20, 225–230.
overview on current practices, advances, and new perspectives in environmental pol- Kawahigashi, H., Hirose, S., Ohkawa, H., Ohkawa, Y., 2006. Phytoremediation of the herbi-
lution treatment. Biomed. Res. Int. 2017. cides atrazine and metolachlor by transgenic rice plants expressing human CYP1A1,
Hlihor, R.M., Figueiredo, H., Tavares, T., Gavrilescu, M., 2017c. Biosorption potential of CYP2B6, and CYP2C19. J. Agric. Food Chem. 54 (8), 2985–2991.
dead and living Arthrobacter viscosus biomass in the removal of Cr (VI): batch and Kawahigashi, H., Hirose, S., Iwai, T., Ohashi, Y., Sakamoto, W., Maekawa, M., Ohkawa, Y.,
column studies. Process. Saf. Environ. Prot. 108, 44–56. 2007. Chemically induced expression of rice OSB2 under the control of the OsPR1.
Ho, Y.-N., Shih, C.-H., Hsiao, S.-C., Huang, C.-C., 2009. A novel endophytic bacterium, 1 promoter confers increased anthocyanin accumulation in transgenic rice. J. Agric.
Achromobacter xylosoxidans, helps plants against pollutant stress and improves Food Chem. 55 (4), 1241–1247.
phytoremediation. J. Biosci. Bioeng. 108, 9. Kawahigashi, H., Hirose, S., Ohkawa, H., Ohkawa, Y., 2008. Transgenic rice plants express-
Hooda, L., Celin, S.M., Singh, S.K., 2016. Phytoremediation of 2, 4, 6-trinitrotoluene (TNT) ing human P450 genes involved in xenobiotic metabolism for phytoremediation.
by Tagetes patula. Eur. J. Adv. Eng. Technol. 3, 60–63. J. Mol. Microbiol. Biotechnol. 15 (2-3), 212–219.
Hrywna, Y., Tsoi, T.V., Maltseva, O.V., Quensen, J.F., Tiedje, J.M., 1999. Construction and Keller, M., Böhringer, N., Möhring, J., Rueda-Ayala, V., Gutjahr, C., Gerhards, R., 2014. Long-
characterization of two recombinant bacteria that grow on ortho-and para- term changes in weed occurrence, yield and use of herbicides in maize in south-west-
substituted chlorobiphenyls. Appl. Environ. Microbiol. 65, 2163–2169. ern Germany, with implications for the determination of economic thresholds. Weed
Huang, X.-D., El-Alawi, Y., Penrose, D.M., Glick, B.R., Greenberg, B.M., 2004. A multi-pro- Res. 54 (5), 457–466.
cess phytoremediation system for removal of polycyclic aromatic hydrocarbons Khan, F.I., Husain, T., Hejazi, R., 2004. An overview and analysis of site remediation tech-
from contaminated soils. Environ. Pollut. 130, 465–476. nologies. J. Environ. Manag. 71, 95–122.
Huang, X.-D., El-Alawi, Y., Gurska, J., Glick, B.R., Greenberg, B.M., 2005. A multi-process Khan, S., Afzal, M., Iqbal, S., Khan, Q.M., 2013. Plant–bacteria partnerships for the remedi-
phytoremediation system for decontamination of persistent total petroleum hydro- ation of hydrocarbon contaminated soils. Chemosphere 90, 1317–1332.
carbons (TPHs) from soils. Microchem. J. 81, 139–147. Khan, Z., Roman, D., Kintz, T., delas Alas, M., Yap, R., Doty, S., 2014. Degradation,
Huang, B., Lei, C., Wei, C., Zeng, G., 2014. Chlorinated volatile organic compounds (Cl- phytoprotection and phytoremediation of phenanthrene by endophyte pseudomo-
VOCs) in environment—sources, potential human health impacts, and current reme- nas putida, PD1. Environ. Sci. Technol. 48, 12221–12228.
diation technologies. Environ. Int. 71, 118–138. Khan, S., Ullah, M.W., Siddique, R., Nabi, G., Manan, S., Yousaf, M., Hou, H., 2016. Role of
Huang, K., Chen, C., Shen, Q., Rosen, B.P., Zhao, F.-J., 2015. Genetically engineering Bacillus recombinant DNA technology to improve life. Int. J. Genom. 2016.
subtilis with a heat-resistant Arsenite methyltransferase for bioremediation of arse- Kiiskila, J.D., Das, P., Sarkar, D., Datta, R., 2015. Phytoremediation of explosive-contami-
nic-contaminated organic waste. Appl. Environ. Microbiol. 81, 6718–6724. nated soils. Curr. Pollut. Rep. 1 (1), 23–34.
Ibañez, S., Talano, M., Ontañon, O., Suman, J., Medina, M.I., Macek, T., Agostini, E., 2016. Kim, S.J., Kweon, O., Jones, R.C., Edmondson, R.D., Cerniglia, C.E., 2008. Genomic analysis of
Transgenic plants and hairy roots: exploiting the potential of plant species to remedi- polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1.
ate contaminants. New Biotechnol. 33(5, 625–635. Biodegradation 19 (6), 859–881.
Iimura, Y., I., S., S., T., H., T., K., S., K., K., T., K., Ka, Y., 2002. Expression of a gene for Mn-per- Kritikos, M., 2018. Developing a regulatory framework on GMO releases. EU Policy-Mak-
oxidase from Coriolus versicolor in transgenic tobacco generates potential tools for ing on GMOs. Palgrave Macmillan, London, pp. 59–111.
phytoremediation. Appl. Microbiol. Biotechnol. 59, 246–251. Kuiper, I., Lagendijk, E.L., Bloemberg, G.V., Lugtenberg, B.J.J., 2004. Rhizoremediation: A
Ijoma, G.N., Tekere, M., 2017. Potential microbial applications of co-cultures involving Beneficial Plant-Microbe Interaction. 17 pp. 6–15.
ligninolytic fungi in the bioremediation of recalcitrant xenobiotic compounds. Int. Kumar, M., Philip, L., 2017. Remediation of endosulfan contaminated system by microbes.
J. Environ. Sci. Technol. 1–20. Microbe-Induced Degradation of Pesticides. Springer International Publishing,
Ingrid, L., Lounès-Hadj Sahraoui, A., Frédéric, L., Yolande, D., Joël, F., 2016. Arbuscular my- pp. 59–81.
corrhizal wheat inoculation promotes alkane and polycyclic aromatic hydrocarbon Kumar, P., Dubey, R.C., Maheshwari, D.K., 2012. Bacillus strains isolated from rhizosphere
biodegradation: microcosm experiment on aged-contaminated soil. Environ. Pollut. showed plant growth promoting and antagonistic activity against phytopathogens.
213, 549–560. Microbiol. Res. 167 (8), 493–499.
Inui, H., Ueyama, Y., Shiota, N., Ohkawa, Y., Ohkawa, H., 1999. Herbicide metabolism and Kumar, S., Dagar, V., Khasa, Y., Kuhad, R.C., R., 2013. Genetically modified microorganisms
cross-tolerance in transgenic potato plants expressing human CYP1A1. Pestic. (GMOs) for bioremediation. Biotechnology for Environmental Management and Re-
Biochem. Physiol. 64, 33–46. source Recovery. Springer, India, pp. 191–218.
Inui, H., Kodama, T., Ohkawa, Y., Ohkawa, H., 2000. Herbicide metabolism and cross-toler- Kuppusamy, S., Thavamani, P., Venkateswarlu, K., Lee, Y.B., Naidu, R., Megharaj, M., 2017.
ance in transgenic potato plants co-expressing human CYP1A1, CYP2B6, and Remediation approaches for polycyclic aromatic hydrocarbons (PAHs) contaminated
CYP2C19. Pestic. Biochem. Physiol. 66, 116–129. soils: technological constraints, emerging trends and future directions. Chemosphere
Ionescu, M., Beranova, K., Dudkova, V., Kochankova, L., Demnerova, K., Macek, T., 168, 944–968.
Mackova, M., 2009. Isolation and characterization of different plant associated bacte- Lang, S., Wullbrandt, D., 1999. Rhamnose lipids–biosynthesis, microbial production and
ria and their potential to degrade polychlorinated biphenyls. Int. Biodeterior. application potential. Appl. Microbiol. Biotechnol. 51 (1), 22–32.
Biodegrad. 63, 667–672. Lee, J.W., Na, D., Park, J.M., Lee, J., Choi, S., Lee, S.Y., 2012. Systems metabolic engineering of
Jabeen, H., Iqbal, S., Ahmad, F., Afzal, M., Firdous, S., 2016. Enhanced remediation of chlor- microorganisms for natural and non-natural chemicals. Nat. Chem. Biol. 8 (6), 536.
pyrifos by ryegrass (Lolium multiflorum) and a chlorpyrifos degrading bacterial endo- Le, T.T., Son, M.H., Nam, I.H., Yoon, H., Kang, Y.G., Chang, Y.S., 2017. Transformation of
phyte Mezorhizobium sp. HN3. Int. J. Phytoremediation 18, 126–133. hexabromocyclododecane in contaminated soil in association with microbial diver-
Jackson, R.G., Rylott, E.L., Fournier, D., Hawari, J., Bruce, N.C., 2007. Exploring the biochem- sity. J. Hazard. Mater. 325, 82–89.
ical properties and remediation applications of the unusual explosive-degrading Leigh, M.B., Prouzova, P., Mackova, M., Macek, T., Nagle, D.P., Fletcher, J.S., 2006.
P450 system XplA/B. Proc. Natl. Acad. Sci. 104 (43), 16822–16827. Polychlorinated biphenyl (PCB)-degrading bacteria associated with trees in a PCB-
Jagtap, U.B., Bapat, V.A., 2017. Transgenic approaches for building plant armor and weaponry to contaminated site. Appl. Environ. Microbiol. 72, 2331–2342.
combat xenobiotic pollutants: current trends and future prospects. Xenobiotics in the Soil Limmer, M., Burken, J., 2016. Phytovolatilization of organic contaminants. Environ. Sci.
Environment. Springer International Publishing, pp. 197–215. Technol. 50 (13), 6632–6643.
Jiménez, J.I., Miñambres, B., García, J.L., Díaz, E., 2002. Genomic analysis of the aromatic catabolic Liu, Z., Hong, Q., Xu, J.-H., Jun, W., Li, S.-P., 2006. Construction of a genetically engineered
pathways from Pseudomonas putida KT2440. Environ. Microbiol. 4 (12), 824–841. microorganism for degrading organophosphate and carbamate pesticides. Int.
Jin, R., Yang, H., Zhang, A., Wang, J., Liu, G., 2009. Bioaugmentation on decolorization of C.I. Biodeterior. Biodegrad. 58, 65–69.
Direct Blue 71 by using genetically engineered strain Escherichia coli JM109 (pGEX- Liu, J.-N., Zhou, Q.-X., Sun, T., Ma, L.Q., Wang, S., 2008. Identification and chemical en-
AZR). J. Hazard. Mater. 163, 1123–1128. hancement of two ornamental plants for phytoremediation. Bull. Environ. Contam.
Jung, H.I., Kuk, Y.I., Back, K., Burgos, N.R., 2008. Resistance pattern and antioxidant enzyme Toxicol. 80, 260–265.
profiles of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice. Liu, R., Jadeja, R.N., Zhou, Q., Liu, Z., 2012. Treatment and remediation of petroleum-con-
Pestic. Biochem. Physiol. 91, 53–65. taminated soils using selective ornamental plants. Environ. Eng. Sci. 29, 494–501.
Liu, R., Xiao, N., Wei, S., Zhao, L., An, J., 2014. Rhizosphere effects of PAH-contaminated soil Mills, T., Arnold, B., Sivakumaran, S., Northcott, G., Vogeler, I., Robinson, B., Norling, C.,
phytoremediation using a special plant named fire phoenix. Sci. Total Environ. 473, Leonil, D., 2006. Phytoremediation and long-term site management of soil contami-
350–358. nated with pentachlorophenol (PCP) and heavy metals. J. Environ. Manag. 79,
Liu, G., Niu, J., Guo, W., An, X., Zhao, L., 2016. Ecological and health risk-based character- 232–241.
ization of agricultural soils contaminated with polycyclic aromatic hydrocarbons in Misra, S., Gedamu, L., 1989. Heavy metal tolerant transgenic Brassica napus L. and Nicoti-
the vicinity of a chemical plant in China. Chemosphere 163, 461–470. ana tabacum L. plants. Theor. Appl. Genet. 78 (2), 161–168.
Liu, S., Qureshi, N., Hughes, S.R., 2017. Progress and perspectives on improving butanol Mitter, B., Pfaffenbichler, N., Sessitsch, A., 2016. Plant–microbe partnerships in 2020.
tolerance. World J. Microbiol. Biotechnol. 33 (3), 51. Microb. Biotechnol. 9 (5), 635–640.
Lòpez-Fernàndez, S., Compant, S., Vrhovsek, U., Bianchedi, P.L., Sessitsch, A., Pertot, I., Mitton, F.M., Gonzalez, M., Peña, A., Miglioranza, K.S.B., 2012. Effects of amendments on
Campisano, A., 2016. Grapevine colonization by endophytic bacteria shifts secondary soil availability and phytoremediation potential of aged p,p'-DDT, p,p'-DDE and p,
metabolism and suggests activation of defense pathways. Plant Soil 405 (1–2), p'-DDD residues by willow plants (Salix sp.). J. Hazard. Mater. 203–204, 62–68.
155–175. Moore, F.P., Barac, T., Borremans, B., Oeyen, L., Vangronsveld, J., van der Lelie, D., Campbell,
Lukić, B., Huguenot, D., Panico, A., Fabbricino, M., Van Hullebusch, E.D., Esposito, G., 2016. C.D., Moore, E.R.B., 2006. Endophytic bacterial diversity in poplar trees growing on a
Importance of organic amendment characteristics on bioremediation of PAH-con- BTEX-contaminated site: the characterisation of isolates with potential to enhance
taminated soil. Environ. Sci. Pollut. Res. 23 (15), 15041–15052. phytoremediation. Syst. Appl. Microbiol. 29, 539–556.
Lykidis, A., Perez-Pantoja, D., Ledger, T., Mavromatis, K., Anderson, I.J., Ivanova, N.N., ... Mosa, K.A., Saadoun, I., Kumar, K., Helmy, M., Dhankher, O.P., 2016. Potential biotechno-
Kyrpides, N.C., 2010. The complete multipartite genome sequence of Cupriavidus logical strategies for the cleanup of heavy metals and metalloids. Front. Plant Sci. 7.
necator JMP134, a versatile pollutant degrader. PLoS One 5 (3), e9729. Muir, D.C.G., Howard, P.H., 2006. Are there other persistent organic pollutants? A chal-
Ma, Y., Prasad, M.N.V., Rajkumar, M., Freitas, H., 2011. Plant growth promoting lenge for environmental chemists†. Environ. Sci. Technol. 40, 7157–7166.
rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Muratova, A.Y., Golubev, S.N., Dubrovskaya, E.V., Pozdnyakova, N.N., Panchenko, L.V.,
Biotechnol. Adv. 29, 248–258. Pleshakova, E.V., Chernyshova, M.P., Turkovskaya, O.V., 2012. Remediating abilities
Ma, R., Kaundun, S.S., Tranel, P.J., Riggins, C.W., McGinness, D.L., Hager, A.G., Hawkes, T., of different plant species grown in diesel-fuel-contaminated leached chernozem.
McIndoe, E., Riechers, D.E., 2013. Distinct detoxification mechanisms confer resis- Appl. Soil Ecol. 56, 51–57.
tance to Mesotrione and atrazine in a population of Waterhemp. Plant Physiol. 163, Narasimhan, K., Basheer, C., Bajic, V.B., Swarup, S., 2003. Enhancement of plant-microbe
363–377. interactions using a rhizosphere metabolomics-driven approach and its application
Ma, Y., Rajkumar, M., Zhang, C., Freitas, H., 2016. Beneficial role of bacterial endophytes in in the removal of polychlorinated biphenyls. Plant Physiol. 132, 146–153.
heavy metal phytoremediation. J. Environ. Manag. 174, 14–25. Newman, L.A., Reynolds, C.M., 2004. Phytodegradation of organic compounds. Curr. Opin.
Macek, T., Mackova, M., Káš, J., 2000. Exploitation of plants for the removal of organics in Biotechnol. 15, 225–230.
environmental remediation. Biotechnol. Adv. 18 (1), 23–34. Noguera-Oviedo, K., Aga, D.S., 2016. Lessons learned from more than two decades of re-
Macek, B., Gnad, F., Soufi, B., Kumar, C., Olsen, J.V., Mijakovic, I., Mann, M., 2008. search on emerging contaminants in the environment. J. Hazard. Mater. 316,
Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial 242–251.
Ser/Thr/Tyr phosphorylation. Mol. Cell. Proteomics 7 (2), 299–307. O'Keefe, D.P., Tepperman, J.M., Dean, C., Leto, K.J., Erbes, D.L., Odell, J.T., 1994. Plant expres-
Macci, C., Doni, S., Peruzzi, E., Bardella, S., Filippis, G., Ceccanti, B., Masciandaro, G., 2013. A sion of a bacterial cytochrome P450 that catalyzes activation of a sulfonylurea pro-
real-scale soil phytoremediation. Biodegradation 24, 521–538. herbicide. Plant Physiol. 105, 473–482.
Mahar, A., Wang, P., Ali, A., Awasthi, M.K., Lahori, A.H., Wang, Q., ... Zhang, Z., 2016. Chal- Oliveira, V., Gomes, N.C.M., Almeida, A., Silva, A.M.S., Simões, M.M.Q., Smalla, K., Cunha, Â.,
lenges and opportunities in the phytoremediation of heavy metals contaminated 2014. Hydrocarbon contamination and plant species determine the phylogenetic and
soils: a review. Ecotoxicol. Environ. Saf. 126, 111–121. functional diversity of endophytic degrading bacteria. Mol. Ecol. 23, 1392–1404.
Malchi, T., Maor, Y., Tadmor, G., Shenker, M., Chefetz, B., 2014. Irrigation of root vegetables Padmavathiamma, P.K., Li, L.Y., 2007. Phytoremediation technology: hyper-accumulation
with treated wastewater: evaluating uptake of pharmaceuticals and the associated metals in plants. Water Air Soil Pollut. 184, 105–126.
human health risks. Environ. Sci. Technol. 48, 9325–9333. Pandotra, P., Raina, M., Salgotra, R.K., Ali, S., Mir, Z.A., Bhat, J.A., ... Upadhahy, D., 2018.
Malik, S., Andrade, S.A.L., Mirjalili, M.H., Arroo, R.R., Bonfill, M., Mazzafera, P., 2016. Bio- Plant-bacterial partnership: a major pollutants remediation approach. Modern Age
technological approaches for bioremediation: in vitro hairy root culture. Transgenesis Environmental Problems and their Remediation. Springer, Cham, pp. 169–200.
and Secondary Metabolism. 1–23. Panke, S., Witholt, B., Schmid, A., Wubbolts, M.G., 1998. Towards a biocatalyst for (S)-sty-
Mani, D., Kumar, C., 2014. Biotechnological advances in bioremediation of heavy metals rene oxide production: characterization of the styrene degradation pathway of Pseu-
contaminated ecosystems: an overview with special reference to phytoremediation. domonas sp. strain VLB120. Appl. Environ. Microbiol. 64 (6), 2032–2043.
Int. J. Environ. Sci. Technol. 11, 843–872. Passatore, L., Rossetti, S., Juwarkar, A.A., Massacci, A., 2014. Phytoremediation and biore-
Männistö, M.K., Tiirola, M.A., Puhakka, J.A., 2001. Degradation of 2, 3, 4, 6- mediation of polychlorinated biphenyls (PCBs): state of knowledge and research per-
tetrachlorophenol at low temperature and low dioxygen concentrations by phyloge- spectives. J. Hazard. Mater. 278, 189–202.
netically different groundwater and bioreactor bacteria. Biodegradation 12, 291–301. Paul, D., Pandey, G., Jain, R.K., 2005. Suicidal genetically engineered microorganisms for
Manousaki, E., Kalogerakis, N., 2011. Halophytes—an emerging trend in bioremediation: need and perspectives. BioEssays 27 (5), 563–573.
phytoremediation. Int. J. Phytoremediation 13, 959–969. Perpetuo, E. A., Souza, C. B., and Nascimento, C. A. O., 2011. Engineering bacteria for bio-
Martin, B.C., George, S.J., Price, C.A., Ryan, M.H., Tibbett, M., 2014. The role of root exuded remediation, In “Progress in Molecular and Environmental Bioengineering - From
low molecular weight organic anions in facilitating petroleum hydrocarbon degrada- Analysis and Modeling to Technology Applications”, Carpi, A., (Ed.) (ISBN 978-953-
tion: current knowledge and future directions. Sci. Total Environ. 472, 642–653. 307-268-5, Published: August 1, 2011 under CC BY-NC-SA 3.0 license).
Martin, B.C., George, S.J., Price, C.A., Shahsavari, E., Ball, A.S., Tibbett, M., Ryan, M.H., 2016. Perez-Pantoja, D., De la Iglesia, R., Pieper, D.H., González, B., 2008. Metabolic reconstruc-
Citrate and malonate increase microbial activity and alter microbial community com- tion of aromatic compounds degradation from the genome of the amazing pollut-
position in uncontaminated and diesel-contaminated soil microcosms. Soil 2 (3), 487. ant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol. Rev. 32 (5),
Massa, V., Infantino, A., Radice, F., Orlandi, V., Tavecchio, F., Giudici, R., Conti, F., Urbini, G., 736–794.
Di Guardo, A., Barbieri, P., 2009. Efficiency of natural and engineered bacterial strains Phillips, L., Germida, J., Farrell, R., Greer, C., 2008. Hydrocarbon degradation potential and
in the degradation of 4-chlorobenzoic acid in soil slurry. Int. Biodeterior. Biodegrad. activity of endophytic bacteria associated with prairie plants. Soil Biol. Biochem. 40,
63, 112–115. 3054–3064.
Master, E.R., Mohn, W.W., 2001. Induction of bphA, encoding biphenyl dioxygenase, in Pieper, D.H., Reineke, W., 2000. Engineering bacteria for bioremediation. Curr. Opin.
two polychlorinated biphenyl-degrading bacteria, Psychrotolerant pseudomonas Biotechnol. 11, 262–270.
strain Cam-1 and mesophilic Burkholderia strain LB400. Appl. Environ. Microbiol. Pinedo, J., Ibáñez, R., Lijzen, J.P.A., Irabien, á., 2013. Assessment of soil pollution based on total
67, 2669–2676. petroleum hydrocarbons and individual oil substances. J. Environ. Manag. 130, 72–79.
Matteucci, F., Ercole, C., del Gallo, M., 2015. A study of chlorinated solvent contamination Pleiss, J., 2012. Rational design of enzymes. In: Gröger, H., Olivery, M. (Eds.), Enzyme Ca-
of the aquifers of an industrial area in central Italy: a possibility of bioremediation. talysis in Organic Synthesis. Wiley-VCH Verlag GmbH & Co. KGaA, pp. 89–117.
Front. Microbiol. 6, 924. Prakash, D., Verma, S., Bhatia, R., Tiwary, B.N., 2011. Risks and precautions of genetically
Matturro, B., Ubaldi, C., Grenni, P., Caracciolo, A.B., Rossetti, S., 2016. Polychlorinated bi- modified organisms. ISRN Ecol. 2011:1–13. https://doi.org/10.5402/2011/369573
phenyl (PCB) anaerobic degradation in marine sediments: microcosm study and (Article ID 369573).
role of autochthonous microbial communities. Environ. Sci. Pollut. Res. 23 (13), Qin, H., Brookes, P.C., Xu, J., Feng, Y., 2014. Bacterial degradation of Aroclor 1242 in the
12613–12623. mycorrhizosphere soils of zucchini (Cucurbita pepo L.) inoculated with arbuscular
McGuinness, M., Ivory, C., Gilmartin, N., Dowling, D.N., 2006. Investigation of substrate mycorrhizal fungi. Environ. Sci. Pollut. Res. 21, 12790–12799.
specificity of wildtype and mutant BphKLB400 (a glutathione S-transferase) from Rabhi, M., Ferchichi, S., Jouini, J., Hamrouni, M.H., Koyro, H.-W., Ranieri, A., Abdelly, C.,
Burkholderia LB400. Int. Biodeterior. Biodegrad. 58, 203–208. Smaoui, A., 2010. Phytodesalination of a salt-affected soil with the halophyte
McGuinness, M.C., Mazurkiewicz, V., Brennan, E., Dowling, D.N., 2007. Dechlorination of Sesuvium portulacastrum L. to arrange in advance the requirements for the successful
pesticides by a specific bacterial GlutathioneS-transferase, BphKLB400: potential for growth of a glycophytic crop. Bioresour. Technol. 101, 6822–6828.
bioremediation. Eng. Life Sci. 7, 611–615. Ramadass, K., Megharaj, M., Venkateswarlu, K., Naidu, R., 2015. Ecological implications of
Meagher, R.B., 2000. Phytoremediation of toxic elemental and organic pollutants. Curr. motor oil pollution: earthworm survival and soil health. Soil Biol. Biochem. 85, 72–81.
Opin. Plant Biol. 3, 153–162. Ramos, J.L., Duque, E., Huertas, M.J., HaÏDour, A.L.I., 1995. Isolation and expansion of the
Mehmannavaz, R., Prasher, S.O., Ahmad, D., 2002. Rhizospheric effects of alfalfa on bio- catabolic potential of a Pseudomonas putida strain able to grow in the presence of
transformation of polychlorinated biphenyls in a contaminated soil augmented high concentrations of aromatic hydrocarbons. J. Bacteriol. 177 (14), 3911–3916.
with Sinorhizobium meliloti. Process Biochem. 37, 955–963. Reichenauer, T.G., Germida, J.J., 2008. Phytoremediation of organic contaminants in soil
Meier, M.J., Paterson, E.S., Lambert, I.B., 2016. Metagenomic analysis of an aromatic hydro- and groundwater. ChemSusChem 1, 708–717.
carbon contaminated soil using substrate-induced gene expression. Appl. Environ. Reineke, W., Knackmuss, H.J, 1980. Hybrid pathway for chlorobenzoate metabolism in
Microbiol. 82, 3897–3909 (AEM-03306). Pseudomonas sp. B13 derivatives. Journal of bacteriology 142 (2), 467–473.
Rodrigues, J.L.M., Kachel, C.A., Aiello, M.R., Quensen, J.F., Maltseva, O.V., Tsoi, T.V., Tiedje, J. (PBDEs), and microbial community dynamics of electronic waste-contaminated
M., 2006. Degradation of aroclor 1242 dechlorination products in sediments by soil. Sci. Total Environ. 502, 426–433.
Burkholderia xenovorans LB400(ohb) and Rhodococcus sp. strain RHA1(fcb). Appl. En- Strong, L.C., McTavish, H., Sadowsky, M.J., Wackett, L.P., 2000. Field-scale remediation of
viron. Microbiol. 72, 2476–2482. atrazine-contaminated soil using recombinant Escherichia coli expressing atrazine
Ronchel, M.C., Ramos, J.L., 2001. Dual system to reinforce biological containment of re- chlorohydrolase. Environ. Microbiol. 2, 91–98.
combinant bacteria designed for rhizoremediation. Appl. Environ. Microbiol. 67 (6), Suenaga, H., Watanabe, T., Sato, M., Ngadiman, and Furukawa, K., 2002. Alteration of
2649–2656. regiospecificity in biphenyl dioxygenase by active-site engineering. J. Bacteriol. 184,
Rosner, D., Markowitz, G., 2013. Persistent pollutants: a brief history of the discovery of the 3682–3688.
widespread toxicity of chlorinated hydrocarbons. Environ. Res. 120, 126–133. Suleiman, M.K., Bhat, N.R., 2003. Performance of ornamental plantsin bioremediated soil.
Ryan, R.P., Ryan, D., Dowling, D.N., 2007. Plant protection by the recombinant, root-colo- Arid Land Res. Manag. 17, 169–176.
nizing Pseudomonas fluorescens F113rifPCB strain expressing arsenic resistance: im- Suyama, A., Iwakiri, R., Kimura, N., Nishi, A., Nakamura, K., Furukawa, K., 1996. Engineer-
proving rhizoremediation. Lett. Appl. Microbiol. 45, 668–674. ing hybrid pseudomonads capable of utilizing a wide range of aromatic hydrocarbons
Ryan, R.P., Germaine, K., Franks, A., Ryan, D.J., Dowling, D.N., 2008. Bacterial endophytes: and of efficient degradation of trichloroethylene. J. Bacteriol. 178 (14), 4039–4046.
recent developments and applications. FEMS Microbiol. Lett. 278, 1–9. Syranidou, E., Christofilopoulos, S., Gkavrou, G., Thijs, S., Weyens, N., Vangronsveld, J.,
Saleem, M., Arshad, M., Hussain, S., Bhatti, A.S., 2007. Perspective of plant growth promot- Kalogerakis, N., 2016. Exploitation of endophytic bacteria to enhance the
ing rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. phytoremediation potential of the wetland helophyte Juncus acutus. Front. Microbiol. 7.
Microbiol. Biotechnol. 34, 635–648. Tabrez, S., Ahmad, M., 2009. Toxicity, biomarkers, genotoxicity, and carcinogenicity of tri-
Salt, D.E., Smith, R.D., Raskin, I., 1998. Phytoremediation. Annu. Rev. Plant Biol. 49 (1), chloroethylene and its metabolites: a review. J. Environ. Sci. Health Part C 27,
643–668. 178–196.
Sandermann, J.H., 1994. Higher plant metabolism of xenobiotics: the green liver concept. Taghavi, S., Barac, T., Greenberg, B., Borremans, B., Vangronsveld, J., van der Lelie, D., 2005.
Pharmacogenetics 4 (5), 225–241. Horizontal gene transfer to endogenous endophytic bacteria from poplar improves
Sayler, G.S., Ripp, S., 2000. Field applications of genetically engineered microorganisms for phytoremediation of toluene. Appl. Environ. Microbiol. 71, 8500–8505.
bioremediation processes. Curr. Opin. Biotechnol. 11, 286–289. Taghavi, S., Garafola, C., Monchy, S., Newman, L., Hoffman, A., Weyens, N., Barac, T.,
Sarkar, S.K., 2018. Phytoremediation of Trace Metals by Mangrove Plants of Sundarban Vangronsveld, J., van der Lelie, D., 2009. Genome survey and characterization of en-
Wetland. Trace Metals in a Tropical Mangrove Wetland. Springer, Singapore, dophytic bacteria exhibiting a beneficial effect on growth and development of poplar
pp. 209–247. trees. Appl. Environ. Microbiol. 75, 748–757.
Schenk, P.M., Carvalhais, L.C., Kazan, K., 2012. Unraveling plant–microbe interactions: can Tao, N., Liu, G., Bai, L., Tang, L., Guo, C., 2017. Genotoxicity and growth inhibition effects of
multi-species transcriptomics help? Trends Biotechnol. 30, 177–184. aniline on wheat. Chemosphere 169, 467–473.
Schneiker, S., dos Santos, V.A.M., Bartels, D., Bekel, T., Brecht, M., Buhrmester, J., ... Tavakoly Sany, S.B., Hashim, R., Rezayi, M., Rahman, M.A., Razavizadeh, B.B.M., Abouzari-
Goesmann, A., 2006. Genome sequence of the ubiquitous hydrocarbon-degrading lotf, E., Karlen, D.J., 2015. Integrated ecological risk assessment of dioxin compounds.
marine bacterium Alcanivorax borkumensis. Nat. Biotechnol. 24 (8), 997. Environ. Sci. Pollut. Res. 22, 11193–11208.
Schwitzguébel, J.-P., 2015. Phytoremediation of soils contaminated by organic com- Teng, Y., Wu, J., Lu, S., Wang, Y., Jiao, X., Song, L., 2014. Soil and soil environmental quality
pounds: hype, hope and facts. J. Soils Sediments 17 (5), 1492–1502. monitoring in China: a review. Environ. Int. 69, 177–199.
Schröder, P., 2007. Exploiting plant metabolism for the phytoremediation of organic xe- Theodoulou, F.L., 2000. Plant ABC transporters. Biochim. Biophys. Acta Biomembr. 1465,
nobiotics. Phytoremediation. Humana Press, pp. 251–263. 79–103.
Sessitsch, A., Coenye, T., Sturz, A.V., Vandamme, P., Barka, E.A., Salles, J.F., Wang-Pruski, G., Thijs, S., Weyens, N., Sillen, W., Gkorezis, P., Carleer, R., Vangronsveld, J., 2014. Potential
2005. Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with for plant growth promotion by a consortium of stress-tolerant 2,4-dinitrotoluene-
plantbeneficial properties. Int. J. Syst. Evol. Microbiol. 55 (3), 1187–1192. degrading bacteria: isolation and characterization of a military soil: plant growth pro-
Seth, C.S., Remans, T., Keunen, E., Jozefczak, M., Gielen, H., Opdenakker, K., Cuypers, A., motion by DNT-degrading bacteria. Microb. Biotechnol. 7, 294–306.
2012. Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Envi- Thijs, S., Sillen, W., Rineau, F., Weyens, N., Vangronsveld, J., 2016. Towards an enhanced
ron. 35 (2), 334–346. understanding of plant–microbiome interactions to improve phytoremediation: en-
Shahzad, A., Saddiqui, S., Bano, A., 2016. The response of maize (Zea mays L.) plant gineering the metaorganism. Front. Microbiol. 7.
assisted with bacterial consortium and fertilizer under oily sludge. Int. Time Magazine, 1975. Environment: Oil-Eating Bug.
J. Phytoremediation 18, 521–526. Truu, J., Truu, M., Espenberg, M., Nõlvak, H., Juhanson, J., 2015. Phytoremediation and
Sharma, B.M., Bharat, G.K., Tayal, S., Nizzetto, L., Čupr, P., Larssen, T., 2014a. Environment plant-assisted bioremediation in soil and treatment wetlands: a review. Open
and human exposure to persistent organic pollutants (POPs) in India: a systematic Biotechnol. J. 9, 85–92.
review of recent and historical data. Environ. Int. 66, 48–64. Torres, G.E., Gainetdinov, R.R., Caron, M.G., 2003. Plasma membrane monoamine trans-
Sharma, B.M., Bharat, G.K., Tayal, S., Nizzetto, L., Larssen, T., 2014b. The legal framework to porters: structure, regulation and function. Nat. Rev. Neurosci. 4 (1), 13.
manage chemical pollution in India and the lesson from the persistent organic pollut- Vacheron, J., Desbrosses, G., Bouffaud, M.-L., Touraine, B., Moënne-Loccoz, Y., Muller, D.,
ants (POPs). Sci. Total Environ. 490, 733–747. Legendre, L., Wisniewski-Dyé, F., Prigent-Combaret, C., 2013. Plant growth-promot-
Shaw, L.J., Morris, P., Hooker, J.E., 2006. Perception and modification of plant flavonoid sig- ing rhizobacteria and root system functioning. Front. Plant Sci. 4.
nals by rhizosphere microorganisms. Environ. Microbiol. 8, 1867–1880. Van Aken, B., Yoon, J.M., Just, C.L., Schnoor, J.L., 2004. Metabolism and mineralization of
Sheng, X., Chen, X., He, L., 2008. Characteristics of an endophytic pyrene-degrading bacte- Hexahydro-1,3,5-trinitro-1,3,5-triazine inside poplar tissues (Populus deltoides
rium of Enterobacter sp. 12J1 from Allium macrostemon Bunge. Int. Biodeterior. × nigra DN-34). Environ. Sci. Technol. 38, 4572–4579.
Biodegrad. 62, 88–95. Vangronsveld, J., Herzig, R., Weyens, N., Boulet, J., Adriaensen, K., Ruttens, A., Thewys, T.,
Shukla, K.P., Sharma, S., Singh, N.K., Singh, V., Bisht, S., Kumar, V., 2013. Rhizoremediation: Vassilev, A., Meers, E., Nehnevajova, E., et al., 2009. Phytoremediation of contami-
a promising rhizosphere technology. Ed. Yogesh B. Patil and Prakash Rao, 331. nated soils and groundwater: lessons from the field. Environ. Sci. Pollut. Res. 16,
Siciliano, S.D., and Germida, J.J. (1998). Biolog analysis and fatty acid methyl ester 765–794.
profiles indicate that pseudomonad inoculants that promote phytoremediation Vatamaniuk, O.K., Mari, S., Lu, Y.-P., Rea, P.A., 1999. AtPCS1, a phytochelatin synthase from
alter the root-associated microbial community of Bromus biebersteinii. Soil Biol. Arabidopsis: isolation and in vitro reconstitution. Proc. Natl. Acad. Sci. 96, 7110–7115.
Biochem. 30, 1717–1723. Vergani, L., Mapelli, F., Zanardini, E., Terzaghi, E., Di Guardo, A., Morosini, C., ... Borin, S.,
Siciliano, S.D., Germida, J.J., Banks, K., Greer, C.W., 2002. Changes in microbial community 2017. Phyto-rhizoremediation of polychlorinated biphenyl contaminated soils: an
composition and function during a polyaromatic hydrocarbon phytoremediation outlook on plant-microbe beneficial interactions. Sci. Total Environ. 575, 1395–1406.
field trial. Appl. Environ. Microbiol. 69, 483–489. Viana, M.L., Sant’ana, L.P., 2017. Biotechnology: the role of science and technology upon
Silva, E., Fialho, A.M., Sá-Correia, I., Burns, R.G., Shaw, L.J., 2004. Combined bioaugmenta- society. Unisanta Sci. Technol. 5 (2), 63–65.
tion and biostimulation to cleanup soil contaminated with high concentrations of at- Vikram, S., Kumar, S., Vaidya, B., Pinnaka, A.K., Raghava, G.P.S., 2013. Draft genome se-
razine. Environ. Sci. Technol. 38, 632–637. quence of the 2-chloro-4-nitrophenol-degrading bacterium Arthrobacter sp. strain
Siminszky, B., Corbin, F.T., Ward, E.R., Fleischmann, T.J., Dewey, R.E., 1999. Expression of a SJCon. Genome Announc. 1 (2), e00058–13.
soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the Vilchez-Vargas, R., Geffers, R., Suárez-Diez, M., Conte, I., Waliczek, A., Kaser, V.S., Pieper, D.
metabolism of phenylurea herbicides. Proc. Natl. Acad. Sci. 96, 1750–1755. H., 2013. Analysis of the microbial gene landscape and transcriptome for aromatic
Singh, J.S., Abhilash, P.C., Singh, H.B., Singh, R.P., Singh, D.P., 2011. Genetically engineered pollutants and alkane degradation using a novel internally calibrated microarray sys-
bacteria: an emerging tool for environmental remediation and future research per- tem. Environ. Microbiol. 15 (4), 1016–1039.
spectives. Gene 480 (1), 1–9. Villacieros, M., Whelan, C., Mackova, M., Molgaard, J., Sanchez-Contreras, M., Lloret, J.,
Singh, D., Tiwari, A., Gupta, R., 2012. Phytoremediation of lead from wastewater using Aguirre de Carcer, D., Oruezabal, R.I., Bolanos, L., Macek, T., et al., 2005.
aquatic plants. J. Agricult. Technol. 8 (1), 1–11. Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 deriva-
Singh, S.N. (Ed.), 2013. Biological Remediation of Explosive Residues. Springer Science & tives, using a sinorhizobium meliloti nod system to drive bph gene expression. Appl.
Business Media. Environ. Microbiol. 71, 2687–2694.
Singh, V., Singh, P., Singh, N., 2016. Synergistic influence of Vetiveria zizanioides and se- Wang, D., Boukhalfa, H., Marina, O., Ware, D.S., Goering, T.J., Sun, F., Starkenburg, S.R.,
lected rhizospheric microbial strains on remediation of endosulfan contaminated 2017. Biostimulation and microbial community profiling reveal insights on RDX
soil. Ecotoxicology 25, 1327–1337. transformation in groundwater. Microbiol. Open 6 (2).
Skaates, S.V., Ramaswami, A., Anderson, L.G., 2005. Transport and fate of dieldrin in poplar Wang, L., Samac, D.A., Shapir, N., Wackett, L.P., Vance, C.P., Olszewski, N.E., Sadowsky, M.J.,
and willow trees analyzed by SPME. Chemosphere 61, 85–91. 2005. Biodegradation of atrazine in transgenic plants expressing a modified bacterial
Smith, M.W., Feng, D.F., Doolittle, R.F., 1992. Evolution by acquisition: the case for hori- atrazine chlorohydrolase (atzA) gene. Plant Biotechnol. J. 3, 475–486.
zontal gene transfers. Trends Biochem. Sci. 17 (12), 489–493. Wang, X., Wu, N., Guo, J., Chu, X., Tian, J., Yao, B., Fan, Y., 2008. Phytodegradation of organ-
Song, M., Luo, C., Li, F., Jiang, L., Wang, Y., Zhang, D., Zhang, G., 2015. Anaerobic degrada- ophosphorus compounds by transgenic plants expressing a bacterial organophos-
tion of polychlorinated biphenyls (PCBs) and polychlorinated biphenyls ethers phorus hydrolase. Biochem. Biophys. Res. Commun. 365, 453–458.
Wang, Y., Li, H., Zhao, W., He, X., Chen, J., Geng, X., Xiao, M., 2010. Induction of toluene Xu, W., Wang, X., Cai, Z., 2013. Analytical chemistry of the persistent organic pollutants
degradation and growth promotion in corn and wheat by horizontal gene transfer identified in the Stockholm convention: a review. Anal. Chim. Acta 790, 1–13.
within endophytic bacteria. Soil Biol. Biochem. 42, 1051–1057. Xun, F., Xie, B., Liu, S., Guo, C., 2015. Effect of plant growth-promoting bacteria (PGPR) and
Wang, Y., Jiang, Q., Zhou, C., Chen, B., Zhao, W., Song, J., Fang, R., Chen, J., Xiao, M., 2014. In- arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contam-
situ remediation of contaminated farmland by horizontal transfer of degradative inated by petroleum to enhance phytoremediation. Environ. Sci. Pollut. Res. 22,
plasmids among rhizosphere bacteria. Soil Use Manag. 30 (2), 303–309. 598–608.
Wasi, S., Tabrez, S., Ahmad, M., 2013. Toxicological effects of major environmental pollut- Yang, J., Kloepper, J.W., Ryu, C.-M., 2009. Rhizosphere Bacteria Help Plants Tolerate Abiotic
ants: an overview. Environ. Monit. Assess. 185, 2585–2593. Stress. Cell Press.
Webster, L.R., McKenzie, G.H., Moriarty, H.T., 2002. Organophosphate-based pesticides Yang, C., Xu, L., Yan, L., Xu, Y., 2010. Construction of a genetically engineered microorgan-
and genetic damage implicated in bladder cancer. Cancer Genet. Cytogenet. 133, ism with high tolerance to arsenite and strong arsenite oxidative ability. J. Environ.
112–117. Sci. Health Part A 45, 740–745.
Wenzel, W.W., 2009. Rhizosphere processes and management in plant-assisted bioreme- Yang, C.Y., Chang, M.L., Wu, S.C., Shih, Y.H., 2017. Partition uptake of a brominated
diation (phytoremediation) of soils. Plant Soil 321, 385–408. diphenyl ether by the edible plant root of white radish (Raphanus sativus L.). Environ.
Weyens, N., van der Lelie, D., Artois, T., Smeets, K., Taghavi, S., Newman, L., Carleer, R., Pollut. 223, 178–184.
Vangronsveld, J., 2009. Bioaugmentation with engineered endophytic bacteria im- Yavari, S., Malakahmad, A., Sapari, N.B., 2015. A review on phytoremediation of crude oil
proves contaminant fate in phytoremediation. Environ. Sci. Technol. 43, 9413–9418. spills. Water Air Soil Pollut. 226.
Weyens, N., Croes, S., Dupae, J., Newman, L., van der Lelie, D., Carleer, R., Vangronsveld, J., Yew, Y.T., Ambrosi, A., Pumera, M., 2016. Nitroaromatic explosives detection using elec-
2010a. Endophytic bacteria improve phytoremediation of Ni and TCE co-contamina- trochemically exfoliated graphene. Sci. Rep. 6.
tion. Environ. Pollut. 158, 2422–2427. Yoon, J., Cao, X., Zhou, Q., Ma, L.Q., 2006. Accumulation of Pb, Cu, and Zn in native plants
Weyens, N., Truyens, S., Dupae, J., Newman, L., Taghavi, S., van der Lelie, D., Carleer, R., growing on a contaminated Florida site. Sci. Total Environ. 368 (2-3), 456–464.
Vangronsveld, J., 2010b. Potential of the TCE-degrading endophyte Pseudomonas Yousaf, S., Ripka, K., Reichenauer, T.G., Andria, V., Afzal, M., Sessitsch, A., 2010. Hydrocar-
putida W619-TCE to improve plant growth and reduce TCE phytotoxicity and evapo- bon degradation and plant colonization by selected bacterial strains isolated from
transpiration in poplar cuttings. Environ. Pollut. 158, 2915–2919. Italian ryegrass and birdsfoot trefoil: bacterial hydrocarbon degradation and plant
Weyens, N., Schellingen, K., Beckers, B., Janssen, J., Ceulemans, R., van der Lelie, D., colonization. J. Appl. Microbiol. 109, 1389–1401.
Taghavi, S., Carleer, R., Vangronsveld, J., 2013. Potential of willow and its genetically Yousaf, S., Afzal, M., Reichenauer, T.G., Brady, C.L., Sessitsch, A., 2011. Hydrocarbon degra-
engineered associated bacteria to remediate mixed Cd and toluene contamination. dation, plant colonization and gene expression of alkane degradation genes by endo-
J. Soils Sediments 13, 176–188. phytic Enterobacter ludwigii strains. Environ. Pollut. 159, 2675–2683.
Weyens, N., Beckers, B., Schellingen, K., Ceulemans, R., van der Lelie, D., Newman, L., Zhang, Y., Liu, J., Zhou, Y., Gong, T., Wang, J., Ge, Y., 2013. Enhanced phytoremediation of
Taghavi, S., Carleer, R., Vangronsveld, J., 2015. The potential of the Ni-resistant TCE- mixed heavy metal (mercury)–organic pollutants (trichloroethylene) with trans-
degrading pseudomonas putida W619-TCE to reduce phytotoxicity and improve genic alfalfa co-expressing glutathione S-transferase and human P450 2E1.
phytoremediation efficiency of poplar cuttings on a Ni-TCE co-contamination. Int. J. Hazard. Mater. 260, 1100–1107.
J. Phytoremediation 17, 40–48. Zhang, H., Tang, J., Wang, L., Liu, J., Gurav, R.G., Sun, K., 2016. A novel bioremediation strat-
Whitfield Åslund, M.L., Lunney, A.I., Rutter, A., Zeeb, B.A., 2010. Effects of amendments on egy for petroleum hydrocarbon pollutants using salt tolerant Corynebacterium
the uptake and distribution of DDT in Cucurbita pepo ssp pepo plants. Environ. Pollut. variabile HRJ4 and biochar. J. Environ. Sci. 47, 7–13.
158, 508–513. Zorrig, W., Shahzad, Z., Abdelly, C., Berthomieu, P., 2012. Calcium enhances cadmium tol-
Winter, R.B., Yen, K.M., Ensley, B.D., 1989. Efficient degradation of trichloroethylene by a erance and decreases cadmium accumulation in lettuce (Lactuca sativa). Afr.
recombinant Escherichia coli. Nat. Biotechnol. 7 (3), 282–285. J. Biotechnol. 11.
Wiszniewska, A., Hanus-Fajerska, E., Muszyńska, E., Ciarkowska, K., 2016. Natural organic Zwillich, T., 2000. A tentative comeback for bioremediation. Science 289, 2266–2267.
amendments for improved phytoremediation of polluted soils: a review of recent
progress. Pedosphere 26 (1), 1–12.
Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: a review of
sources, chemistry, risks and best available strategies for remediation. ISRN Ecol.
2011, 1–20.

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Science of the Total Environment 628–629 (2018) 1582–1599

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Microbe and plant assisted-remediation of organic xenobiotics and its

• This review offers details on enhanced

Recombinant strategy Results References

Organic pollutants e.g.

Fig. 1. Biochemical/biotechnological treatment of organic pollutants in rhizosphere.

Endophytic bacteria Plant association Pollutant type Case studies

Rhizospheric bacteria Plant association Soil contaminant Case studies

Nicotiana tabaccum CYP105A1 Cytochrome Streptomyces Resistance to sulfonylurea (O'Keefe et al.,

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