Chapter 1

Agriculturally Important Fungi:

Plant–Microbe Association
for Mutual Benefits

Fatma Ahmed Abo Nouh, Hebatallah H. Abo Nahas,
and Ahmed M. Abdel-Azeem

Contents
1.1  Introduction  1
1.2  Plant-Symbiotic Nitrogen Fixation Association  3
1.2.1  Nitrogen Fixing in Legumes  4
1.2.2  Nitrogen Fixing in Actinorhizal Plants  5
1.3  Plant–Mycorrhizas Association  5
1.3.1  Examples of Specific Activities of AMF  6
1.4  Plant–Endophyte Association  7
1.4.1  Fungal Endophyte  7
1.4.2  Bacterial Endophyte  8
1.4.3  Examples of Specific Activities of Endophytes  9
1.5  Conclusion and Future Prospects  12
References  12

1.1  Introduction

Plants represent a very dynamic system, reflecting a great capacity for adaptation in
constantly fluctuating surroundings. This ability is particularly advantageous in the
areas that are prone to intensive agriculture or biotic or abiotic vagaries (Bhandari
and Garg 2017). Plants are exposed to huge numbers of microorganisms that are
present in the top soil and are found on leaves and stems (Sivakumar and

F. A. A. Nouh · A. M. Abdel-Azeem (*)

Systematic Mycology Laboratory, Botany Department, Faculty of Science,
University of Suez Canal, Ismailia, Egypt
H. H. Abo Nahas
Zoology Department, Faculty of Science, Suez Canal University, Ismailia, Egypt

© Springer Nature Switzerland AG 2020 1

A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable
Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-45971-0_1
2 F. A. A. Nouh et al.

Thamizhiniyan 2012). Plant–microbe interactions are an extensively studied area

and date back to the nineteenth century. The spectrum of plant–microbe interactions
is highly complex, comprising of phylogenetically diverse microbial species (Hirsch
2004) as plants are constantly interacting with a range of microbes both in the rhi-
zosphere and within the plant itself (Badri et  al. 2009; Evangelisti et  al. 2014).
Plant–microbe interactions play a vital role to ensure sustainability in agriculture
and ecosystem restoration (Badri et al. 2009). Plant–microbe interaction is a mode
of communication between plants and microbes which is initiated by the secretion
of different signaling molecules (Rastegari et al. 2020a, b; Verma et al. 2017). One
of the important questions of communication pathways is how the plant distin-
guishes a microbial mutualist from pathogen. It has been reported that during the
course of evolution, plants have evolved unique and sophisticated defense mecha-
nism that involves innate immune system consisting of two classes of immune
receptors that recognize the presence of nonself molecules both inside and outside
of host cells (Jones and Dangl 2006). Encounter with nonself molecule evokes pow-
erful immune responses which in turn prevents the multiplication of microbial
pathogens. An increasing number of pattern recognition receptors have been identi-
fied on the plant cell surface during the past few decades (Boller and Felix 2009).
Microbial communities affect the plant physiology directly or indirectly, in a
positive or negative manner, by various interactions like mutualism, commensalism,
amensalism, and pathogenic consequences (Yadav et  al. 2017, 2020). In plants,
commensalism or mutualism is one of the most common interactions found
(Campbell 1995). The interactions may be categorized as positive, negative, or neu-
tral which largely depends on the nature of microorganisms associating the host
(Abhilash et al. 2012). Positive interactions stimulate plant growth by conferring
abiotic and/or biotic stress tolerance and help the plants for the revitalization of
nutrient-deficient and contaminated soils. Negative interactions involve host–patho-
gen interactions resulting in many plant diseases and adverse effects and host life
(Akram et al. 2017). Moreover, some microbes reside in the soil surrounding the
plant roots just to obtain their nutrition from root exudates. They do not influence
the plant growth or physiology in a positive or negative way, thus forming neutral
interactions (Akram et al. 2017).
Mutualism is an obligatory or highly specific interaction between two popula-
tions in which both of them benefit from each other. It usually required close physi-
cal connection in which both partners may act as if they are one. When they exist
separately, the physical tolerance and metabolic activities will be different for each
single symbiont (Leung and Poulin 2008). Boucher et al. (1982) identified four key
types of mutualism: dispersal, pollination, nutrition, and protection. Community-­
level effects of nutritional mutualisms, such as mycorrhizal fungi N-fixing bacteria
(Hartnett and Wilson 1999) may depend on the degree to which benefits are private
and whether the mutualism enhances the dominance of a single (or few) species to
the detriment of others. Finally, protection mutualisms may be more likely to have
strong community-level effects than other types of mutualism because they are
inherently indirect interactions that require the involvement of at least three spe-
cies, rather than a simple pair such as endophytes (Rudgers and Clay 2008).
1  Agriculturally Important Fungi: Plant–Microbe Association for Mutual Benefits 3

Mutualism could be classified into different types according to partner’s selection

and function or purposes of the relationship. Mutualism according to the partner’s
selection: (1) obligate mutualism occurs when both microorganisms live together
in close proximity, and both species cannot survive without its mutualistic partner.
(2) Facultative mutualism: it occurs when one of the two partners can survive with-
out its m­ utualistic partner by itself in some conditions. Mutualism according to
interaction purposes: (1) Trophic mutualism: it is also called resource–resource
interactions. It is a type of mutualistic association, which comprises the exchange
of nutrients between two species. (2) Defensive mutualism: it is also called ser-
vice–resource relationships. It appears when one organism provides shelter or pro-
tection from predators or pathogens, while the other provides food. (3) Service–service
mutualism: it appears when one species receives service from its partner in return
for transporting another service to the other organism (Selim and Zayed 2017).
Mutualistic relationship such as those formed with nitrogen-fixing bacteria (van
Rhijn and Vanderleyden 1995; Richardson et al. 2000; O’Hara 2001; Zhang et al.
2012; Selim and Zayed 2017; Suman et  al. 2016), mycorrhizal fungi (Wu et  al.
2013; Zayed et al. 2013; Manaf and Zayed 2015; Sengupta et al. 2017), endophytes
(Hilszczańska 2016; Arora and Ramawat 2017; Jain and Pundir 2017; Lata et al.
2018; Khare et al. 2018; Rana et al. 2019c). Most of the plant–microbe interaction
research in the past has focused on the ancient symbiosis between plants and arbus-
cular mycorrhizae (Parniske 2008), nitrogen fixation by rhizobia within the nodules
of legume roots (Oldroyd et al. 2011) and pathogenesis, and management of plant
diseases by natural antagonistic microorganisms (Heydari et al. 2004; Sang et al.
2013). However, the role of endophytes that reside in plants is yet to be explored to
its fullest potential. Endophytic microorganisms and their role in crop health are
now attracting great interest from researchers (Jain and Pundir 2017; Kour et  al.
2019c; Rana et al. 2019a; Suman et al. 2016; Yadav 2019b).

1.2  Plant-Symbiotic Nitrogen Fixation Association

There are two main symbiotic nitrogen-fixation systems: those involving symbioses
between legumes and Proteobacteria (e.g., Bradyrhizobium spp. and Rhizobium spp.),
and those between actinorhizal plants and actinomycetes (e.g., Frankia spp.). Both
systems can convert gaseous nitrogen to ammonia in a process known as nitrogen
fixation. The reaction is catalyzed by the nitrogenize enzyme complex which com-
prises two enzymes, a dinitrogen reductase and a dinitrogenase (Richardson et  al.
2000). The bacteria Rhizobium and Bradyrhizobium (collectively known as rhizobia)
and the actinomycetes (filamentous bacteria) Frankia form nodules on plant roots and
are major contributors to symbiotic nitrogen fixation. The nitrogen-­fixing bacteria
provide the plants with nitrogenous compounds, while in return the plants provide the
nitrogen-fixing bacteria with carbohydrates. This mutualistic association improves
plant growth and health (Selim and Zayed 2017; Kour et al. 2020; Rana et al. 2020).
4 F. A. A. Nouh et al.

1.2.1  Nitrogen Fixing in Legumes

Rhizobia are motile, rod-shaped, Gram-negative bacteria with polar or subpolar fla-
gella. They live in the soil and, almost exclusively, form nodules on roots of mem-
bers of one of the three families of legumes. Nodule-forming bacteria (rhizobia)
require inorganic nutrients for metabolic processes to enable their survival and
growth as free-living soil saprophytes and for their role as the nitrogen (N)-fixing
partners in legume symbioses (Rana et al. 2019c; Yadav 2018). Nitrogen-fixing pas-
ture and pulse legumes are important for maintaining productivity in many agricul-
tural systems (Graham and Vance 2000). A key benefit from using symbiotic
legumes in agriculture is the fixation of atmospheric N by the rhizobia located in
nodules formed on legume roots. Nitrogen fixation is strongly inhibited in the pres-
ence of oxygen so part of the function of the nodule is to provide an anaerobic
environment in which nitrogen fixation can take place. Anaerobic conditions are
achieved by excluding oxygen from the central tissue of the nodule (O’Hara 1998).
Nodules are globose to elongate outgrowths of plant tissue which vary in length
from a few millimeters to a few centimeters. They do not develop near the root tips,
but are abundant on older parts of the root system. The morphology of nodules is
determined by the host, not the symbiont, which occurs within host cells in the cen-
tral tissue of the nodule. The symbionts occur singly or in small groups within
membrane-bound vacuoles. They are called bacteroids to distinguish them from
bacteria outside the host cell because they are often much larger and may develop
branches so they are Y’ or ’X shaped (O’Hara 2001). Rhizobia are classically
defined as symbiotic bacteria that invade the roots and stems of leguminous plants
to fix nitrogen (van Rhijn and Vanderleyden 1995). It is a synthesis of NH4+ (a plant
usable form of N) using atmospheric N2 (plant non-usable form of N) by rhizobia in
nodules of leguminous plants. The important nitrogen-fixing rhizobia genera in
legumes are about 30 named species of nodule bacteria among the 6 accepted gen-
era of Allorhizobium, Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium,
and Sinorhizobium of the family Rhizobiaceae (Young 1996). The majority of sym-
biotic legumes used for agriculture and forestry are nodulated by species of the
genera Bradyrhizobium, Mesorhizobium, Rhizobium, and Sinorhizobium (O’Hara
2001). In agricultural settings, perhaps 80% of the biologically fixed N comes from
family Rhizobiaceae in association with the leguminous plants. Rhizobium and
Bradyrhizobium establish symbiotic associations with roots in leguminous plants
such as soybean, pea, peanut, and alfalfa, convert N2 into ammonia, and make it
available to the plants as a source of N (Badawi et al. 2011). Among the legumes
(Fabaceae), of which approximately 18,000 species have been described, the occur-
rence of nodulation varies considerably among subfamilies. There are successful
nodulation by the Rhizobium strain TAL 1145 on Acacia farnesiana, Calliandra
calothyrsus, Gliricidia sepium, several species of Leucaena, Mimosa invisa,
M. pudica, and Sesbania grandiflora (Richardson et al. 2000).
1  Agriculturally Important Fungi: Plant–Microbe Association for Mutual Benefits 5

1.2.2  Nitrogen Fixing in Actinorhizal Plants

Besides rhizobia, many Frankia species have also been reported to form nodules in
non-leguminous actinorhizal plants for N2 fixation (Zhang et al. 2012). At least 194
plant species in 24 genera are nodulated by actinomycetes in the genus Frankia
(Frankiaceae). These “actinorhizal” plants are woody, dicotyledonous angiosperms
in the Betulaceae, Casuarinaceae, Coriariaceae, Datiscaceae, Elaeagnaceae,
Myricaceae, Rhamnaceae, and Rosaceae (Benson and Silvester 1993). They are
typically early successional plants on nutrient-poor sites. Many species are widely
used in afforestation (including agroforestry) and agriculture (Richardson et  al.
2000). At least the following actinorhizal species are important invaders of natural
systems: Casuarina equisetifolia, Elaeagnus angustifolia, E. umbellata, E. pun-
gens, and Myrica faya (Richardson et  al. 2000). Frankia strains exhibit various
degrees of host specificity. Actinorhizal are much larger than legume nodules, often
measuring several centimeters across. They are essentially infected lateral roots
which branch profusely and have very restricted apical growth, resulting in long-­
lived, coral-like structures (Benson and Silvester 1993). It is clear that, as with
legumes, there are differences between actinorhizal taxa in their ability to form
associations with local microsymbiont. Alders are nodulated wherever they are
transplanted throughout the world, including places where they have no natural
presence (Clawson et al. 1997; Yadav et al. 2018a, b).

1.3  Plant–Mycorrhizas Association

Mycorrhizae are highly evolved soil fungi involved in tripartite interaction mutu-
alistic associations amid soil and plant. The associations formed by Glomeromycota
fungi in plants usually colonize in arbuscules and often vesicles, thus known as
arbuscular mycorrhiza (AM) and vesicular-arbuscular mycorrhizas (VAM). These
are members of Zygomycetes, Ascomycetes, and Basidiomycetes classes of fungi
kingdom (Morton 1988; Morton and Bebtivenga 1994). The common mycorrhizal
associations are vesicular-arbuscular mycorrhizas (VAM): zygomycetous fungi
produce arbuscules, hyphae, and vesicles within root cortex cells, ectomycorrhizal
(ECM): basidiomycetes and other fungi form a mantle around roots and a Hartig
net between root cells, orchid mycorrhizas: fungi produce coils of hyphae within
roots (or stems) of orchidaceous plants, and ericoid mycorrhizas: fungi have
hyphal coils in outer cells of the narrow “hair roots” of plants in the Ericales
(Prasad 2017).
AM fungi found in rhizosphere and associated with several vascular plants have
tremendous contribution in sustainable agriculture as well as agricultural ecosystems
management (Kour et al. 2019a, b). The beneficial effects of indigenous AM fungi on
the nutrition replenishment for plants depend on both the abundance and type of fungi
present in the soil (Prasad and Gautam 2005; Prasad 2005). AM fungi are the obligate
6 F. A. A. Nouh et al.

biotrophs that have been documented to form symbioses with the roots of more than
80% of terrestrial plant species (except in the plants belonging to families Amaranthaceae,
Brassicaceae, Proteaceae, Commelinaceae, Polygonaceae, Cyperaceae, Juncaceae, and
Chenopodiaceae). They are ubiquitous soilborne fungi, whose origin and divergence
dates back to over 450 million years (Redecker et al. 2000). AM fungi belong to the
phylum Glomeromycota (Bhandari and Garg 2017). In general, it has been estimated
that approximately 20% C of net primary productivity is allocated to AM fungus
(Fellbaum et al. 2014; Bücking and Kafle 2015) which is used to maintain and extend
its hyphal network in the soil and in turn provide a majority of the plant nutrients
(Leake et al. 2004). There are mutualistic association among mycorrhizal fungi and
plant roots, in which plants provide fungus with carbohydrates and offer it protection
(Yadav et al. 2019a, b, c). In turn, the fungus increases the surface area of plant roots
for absorbing water, nitrogenous compounds, phosphorus, and other inorganic nutri-
ents (e.g., phosphate) from the surrounding soil and delivers them to the plant which
improves plant growth and health (Zayed et al. 2013).

1.3.1  Examples of Specific Activities of AMF

AMF increase seed yield than the controlled groups of flax seeds, and it depends on
status of nutrient, management, and type of soil. The other beneficial role of AMF
is to control root pathogens and their hormonal production that has higher potential
to withstand synergistic interaction and water stress (Thompson 1994). Also, mycor-
rhizal fungi shelter plant roots from invasion by soilborne root-infecting pathogens.
Endomycorrhizal symbiosis increases plant performance through improving their
tolerance to different environmental stresses, which may be biotic, e.g., pathogen
attack, or abiotic (e.g., drought, salinity, and heavy metal toxicity) (Garg and
Chandel 2010; Garg and Pandey 2015), or presence of organic pollutants and also
enhancing soil structure through formation of hydro-stable aggregates essential for
good soil structure (Manaf and Zayed 2015). In addition, growing evidence indi-
cates that association with AM fungi can improve overall plant growth and repro-
ducibility by improving root length, leaf area, plant biomass, plant tissue hydration,
and nutrient uptake under water-deficit condition (Bhandari and Garg 2017).
Ruth et al. (2011) estimated that about 20% of root water uptake taken by roots
of mycorrhizal barley plants is caused by the presence of fungal mycelium.
Gholamhoseini et al. (2013) stated that inoculation sunflower plant with G. mosseae
improved availability of P, thus minimizing the impact of stress on seed oil percent-
age and oil yield. Studies have further depicted that AM-mediated alleviation of
drought stress could also be allied with enhancement observed in the activities of
antioxidants such as superoxide dismutase (SOD), catalase (CAT), and peroxidase
(POX) in plants (Wu and Zou 2010; Baslam and Goicoechea 2012). AM inoculation
can also modulate plant water status by accumulating osmolytes such as free amino
acids (FAA), Pro, GB, SS, and organic acids (Garg and Baher 2013; Evelin and
Kapoor 2014) which not only lower down osmotic potential but also permit cells to
1  Agriculturally Important Fungi: Plant–Microbe Association for Mutual Benefits 7

maintain turgor-related processes (Ruiz-Lozano et al. 2012). Mycorrhizal inocula-

tions enhance root hydraulic conductivity (Smith et al. 2010) by altering the mor-
phology of root in a structural, spatial, quantitative, and temporal manner which not
only results in production of greater root system and better root system architecture
(RSA) in mycorrhizal plants (Bhandari and Garg 2017). In addition to K+, Ca2+,
ERM of AM fungi, displays the ability to proliferate and exploit the rhizospheric
area, thus stimulating the uptake of other mineral components including N, P, Mg,
Cu, Fe, and Zn, thereby alleviating salt-induced mineral deficiency (Hajiboland
2013; Garg and Pandey 2015). Several studies have validated that AM fungi play a
vital role in improving growth and productivity of host plants in metal-­contaminated
soils (Garg and Bhandari 2014; Nadeem et al. 2014). In addition, more than 30 spe-
cies of AM fungi have been identified in contaminated soils worldwide and some at
high frequencies, such as Paraglomus occultum, G. clarum, G. intraradices, and
Scutellospora pellucida (Bhandari and Garg 2017).

1.4  Plant–Endophyte Association

The interrelationship that exists between host plant and its endophyte is considered
as “balanced antagonism”—a cohabitation in which host plant gains resistance
against pathogenic organisms and phytophagous insects and its overall growth or
biomass quality improves (Rana et  al. 2019a). In most cases, various bioactive
metabolites have been involved (Chowdhary et  al. 2012; Kumar and Kaushik
2013). Numerous fitness benefitting factors conferred by microbes inhabiting
inside host plants. These benefitting attributes hold a huge promise in sustainable
agriculture and disease management of plants (Kaul et  al. 2012; Kumar and
Kaushik 2013).

1.4.1  Fungal Endophyte

Research on fungal endophytes in various plants has progressed significantly.

Fungal species that were majorly reported as endophytes in agricultural crops
include Piriformospora indica (Varma et  al. 1999), Trichoderma spp. (Romao-­
Dumaresq et al. 2012; Sharma et al. 2019), Epicoccum nigrum (Fávaro et al. 2012),
Penicillium spp., Alternaria, Cladosporium, Fusarium spp. (Paul et  al. 2012),
Fusarium oxysporum (Kim et  al. 2007), Chaetomium globosum, Cladosporium
cladosporioides (Naik et  al. 2009), Aspergillus, Curvularia, Gilmaniella,
Arthrobotrys foliicola (Zakaria et al. 2010), Acremonium zeae, Aspergillus flavus,
A. niger, Alternaria alternata, Colletotrichum graminicola, Fusarium verticillioi-
des, Saccharomyces cerevisiae, Trichoderma koningii (Oldroyd et  al. 2011), and
others. Entomopathogens such as Beauveria bassiana and Paecilomyces spp. were
also reported as endophytes in cotton and tobacco (Ek-Ramos et al. 2013).
8 F. A. A. Nouh et al.

Endophytic fungi living asymptomatically in plant tissues may present in almost

all plants (Saikkonen et al. 1998). One species of an endophyte may be associated
with many plant species, and many species of endophytes may be present in the
same species (Rana et  al. 2019a). Some endophytes remain as latent in the host
plant, while others may interact with other endophytes, pathogenic or non-­
pathogenic (Zabalgogeazcoa 2008). Endophytes are known to provide various
types of protections to their host plant, viz. endurance to grow in hot springs, deter
herbivores by producing toxic alkaloids in grasses, and provide protection from
pests in dicots (Zhang et  al. 2006). Colonization by endophytic fungi promotes
plant growth by protecting against several fungal and bacterial borne diseases,
improving the ecological adaptation abilities of the host by providing tolerance to
counteract against biotic and abiotic stresses (Schulz and Boyle 2005; Rana et al.
2019a, b; Yadav 2019a), production of phytohormone is also considered as a sig-
nificant contribution to enhancement of plant growth (Zhou et al. 2014) and nutri-
ents uptake (Zhang et al. 2013; Jain and Pundir 2017).

1.4.2  Bacterial Endophyte

Bacterial endophytes are widely present in agricultural crops and include

Serratia spp., Bacillus spp., Enterobacter spp., Agrobacterium radiobacter,
Burkholderia gladioli, B. solanacearum (McInroy and Kloepper 1995),
Pseudomonas putida (Aravind et al. 2009), P. fluorescens (Ramesh et al. 2009),
Achromobacter xylosoxidans (Forchetti et al. 2010), P. aeruginosa (Paul et al.
2013), Micrococcus spp., and Flavobacterium spp. (UmaMaheswari et  al.
2013), Acetobacter diazotrophicus, Herbaspirillum seropedicae, H. rubrisubal-
bicans (Varma et al. 2017). Utmost bacterial endophytes interact with plants in
a biotrophic and mutualistic association (Hallmann et al. 1997; Kobayashi and
Palumbo 2000). They are also associated with the exchange of nutrients,
enzymes, functional agents, and signals (Hardoim et al. 2015). Bacterial endo-
phytes colonize above (vegetation) and beneath soil (root) host tissues estab-
lishing long-haul natural associations, without doing substantive harm to the
host (Hallmann et al. 1997; Hardoim et al. 2015).
Endophytic bacteria provide a large array of beneficial effects to their host plant.
It promotes plant growth by producing plant growth-enhancing substances such as
indole acetic acid IAA (Naveed et al. 2015), cytokinins CK (Garcia de Salamone
et al. 2001), gibberellic acid GA (UmaMaheswari et al. 2013), and improving nutri-
ent absorption, including nitrogen fixation (Mirza et  al. 2001). Besides growth
enhancement, endophytic bacteria also benefit the host plant by enhancing adapta-
tion for abiotic or biotic stress via phytohormone signaling. The endophytic bacteria
get advantage of being close to the host and protected from the harsh external envi-
ronment (Sturz et al. 2000). Besides PGP activities, the anti-plant pathogenic activi-
ties of these bacterial endophytes are also well documented (Varma et al. 2017). It
produces a wide spectrum of compounds such as antibiotic, exoenzymes, sidero-
1  Agriculturally Important Fungi: Plant–Microbe Association for Mutual Benefits 9

phores, and other antimicrobial compounds which can suppress the growth of
pathogens and act as a biocontrol agent (Brader et al. 2014; Wang et al. 2014). It has
found to be stimulating an underlying pathogen defense mechanism, called as
induced systemic resistance (ISR) that provides an increased level of protection to a
wide variety of pathogens (Pieterse et al. 2014).

1.4.3  Examples of Specific Activities of Endophytes

Herbivory is a well-manifested mechanism exhibited by endophytes that protect

plant species from herbivores. Several direct and indirect effects of alkaloids pro-
duced by endophytes are witnessed. For example, the endophyte, Neotyphodium
occultans when present in neighboring Lolium multiflorum has reduced the aphid
infestation in Trifolium repens plants. This phenomenon can be described as asso-
ciation protection of non-host plants due to changes in host-volatile compounds
which is an indirect effect (Parisi et al. 2014). Direct effects of alkaloids by endo-
phytes in host plants are a common phenomenon as in Fescue grass (by the endo-
phytes Neotyphodium spp. and Epichloe spp.), wherein the host plant leaves are
protected from herbivores by the production of alkaloid, loline, produced by mutu-
alistic fungal endophytes (Roberts and Lindow 2014). Secondary metabolite like
colletotric acid, isolated from the endophytic fungus Colletotrichum gloeosporioi-
des, dwelling in Artemisia annua (Zou et al. 2000), a Chinese traditional herb, was
shown to have activity against pathogenic plant fungi and human pathogenic bacte-
ria (Lu et al. 2000).
This Chinese traditional herb has already been reported to produce artemisinin
(an antimalarial drug). Pestalotiopsis sp. an endophyte of Rhizophora mucronata, a
mangrove, produced pestalotiopen A, exhibiting activity against Enterococcus fae-
calis (Hemberger et al. 2013). Phomopsis spp. occurring as endophytes on different
host plants produces several chemically diverse bioactive compounds. Phomopsis
longicolla, associated with mint plant Dicerandra frutescens, was found to produce
dicerandrol A, B, and C with antimicrobial activity exhibiting zones of inhibition of
11, 9.5, and 8.0 mm against B. subtilis and 10.8, 9.5, and 7.0 mm against S. aureus.
Similarly, Phomopsis longicolla strain C81, associated with seaweed Bostrychia
radicans, produced dicerandrol C active against S. aureus and S. saprophyticus
(Wagenaar and Clardy 2001).
Endophyte-mediated induction of resistance to plant diseases is also reported. In
sunflower, resistance to stem rot caused by Sclerotium rolfsii is reported with the
endophytes Penicillium citrinum LWL4 and Aspergillus terreus LWL5 (Waqas et al.
2015). The fungal pathogens of corn such as Fusarium verticillioides, Colletotrichum
graminicola, Bipolaris maydis, and Cercospora zeae-maydis are antagonized by the
endophyte Bacillus spp. (Varma et  al. 2017). Similarly, the endophyte harboring
wild and ancient maize is antagonistic to its fungal pathogen, Sclerotinia homoeo-
carpa (Shehata et al. 2016). Other important examples of endophytes having antag-
onistic activity are Bacillus spp., Pseudomonas putida, and Clavibacter
10 F. A. A. Nouh et al.

michiganensis against Fusarium solani and Alternaria alternata in Curcuma longa

(Kumar et al. 2016). In banana, the endophytic species of Bacillus such as B. amy-
loliquefaciens, B. subtilis subsp. subtilis, and B. thuringiensis are antagonistic to
fungal pathogens such as Fusarium oxysporum and Colletotrichum graminicola
(Souja et al. 2014). Colonization of P. indica controlled various plant diseases such
as powdery mildew, eyespot, Rhizoctonia root rot, Fusarium wilt, black root rot,
yellow leaf mosaic, Verticillium wilt, cyst nematode, and leaf blight in barley,
wheat, maize, tomato, and Arabidopsis plants. Reduced severity of Verticillium wilt
by 30% in tomato caused by Verticillium dahlia, and increased leaf biomass by 20%
(Chhipa and Deshmukh 2019) The inoculation of an endophytic E. nigrum strain
from an apple tree in the model plant Catharanthus roseus triggered defense
responses against “Candidatus Phytoplasma mali” and reduced symptom severity
(Fávaro et  al. 2012). E. nigrum has shown biocontrol activity against bacterial
pathogen pseudomonas savastanoi pv. Savastanoi (Psv) causing olive knot and
reduced Psv growth/biomass up to 96% (Berardo et al. 2018). Endophytes Epichloe
in temperate grass produce bioactive compounds in host plant which works as a
deterrent to herbivores and pests (Chhipa and Deshmukh 2019).
Antibiotic-mediated resistance is also commonly noticed in certain cases. The
antibiotics like Taxol by Pestalotiopsis microspora in Taxus wallichiana (Strobel
et al. 1996), ecomycins B and C in Lactuca sativa by Pseudomonas viridiflava EB
273 (Miller et al. 1998), and trichodermin in garlic by Trichoderma brevicompac-
tum (Shentu et al. 2014) are effective against specific plant pathogens. Besides pro-
duction of antibiotics, HCN is another antimicrobial compound that is produced by
certain endophytes in crops. For example, Bacillus produces HCN in avocado and
black grapes (Prasad and Dagar 2014). Similarly, Pseudomonas putida produces
HCN that has antibacterial activity against Escherichia coli and Klebsiella pneu-
moniae, and antifungal activity against Pythium ultimum (Kumar et  al. 2015).
Sobolev et  al. (2013) reported antibiosis by the endophytic bacterium, Bacillus
amyloliquefaciens, in peanut. The isolate of sugarcane has shown biocontrol activ-
ity against fungal pathogen Sclerotinia sclerotiorum in sunflower and Pythium in
the cotton crop, and has antibacterial activity against Phytoplasma in apple and
Monilinia sp. in peach fruit and nectarines (Chhipa and Deshmukh 2019).
Pathogen-related enzymes such as lipase, cellulose, protease, amylase, chitin-
ases, and pectinases are also produced by these endophytes (Varma et  al. 2017).
Trichoderma and Phanerochaete are the most comprehensively studied fungi
responsible for lignocellulolytic degradation (Tiquia et  al. 2002). Other fungi
involved in cellulolytic degradation of composting materials are Penicillium,
Fusarium, Aspergillus, Rhizopus, Chaetomium, Alternaria, and Cladosporium
(Yadav et al. 2019a). In addition, bacteria are involved in cellulose degradation, and
many species including those belonging to Cytophaga, Bacillus, Cellulomonas,
Pseudomonas, Klebsiella, and Azomonas are commonly involved in aerobic decom-
position of substrates (Mishra and Sarma 2018). Fouda et  al. (2015) isolated
Alternaria alternata, and sterile hyphae from Asclepias sinaica. It was observed that
these endophytes had the ability to produce several extracellular enzymes including
amylase, pectinase, cellulase, gelatinase, xylanase, and tyrosinase.
1  Agriculturally Important Fungi: Plant–Microbe Association for Mutual Benefits 11

Plant growth-promoting activities by endophytes are well established as is evi-

dent in Echinacea by Pseudomonas stutzeri (Lata et al. 2006), in rice by Pseudomonas,
Bacillus, Enterobacter, and Micrococcus spp. (Mbai et al. 2013). PGP activities of
endophytes are attributed to the production of iron-chelating agents, siderophores as
in rice by Enterobacter spp. and Burkholderia spp. (Souza et al. 2013), indoleacetic
acid (IAA), and other growth hormones as in cashew by Staphylococcus saprophyti-
cus and Escherichia coli (Lins et  al. 2014). Endophytic Azospirillum spp. are
reported to accumulate the abscisic acid (ABA) in mitigating water stress tolerance
in maize. Plant growth-promoting hormones IAA and gibberellins further enhance
the effect (Cohen et al. 2009). Few of the soilborne pathogens like Fusarium oxys-
porum, Pythium spp., Phytophthora spp., Aphanomyces spp., Sclerotium rolfsii,
Gaeumannomyces graminis, Rhizoctonia solani, Verticillium spp., and Thielaviopsis
basicola are found to be negatively affected by PGPR (Sahu et al. 2017).
Water stress alleviation was reported in maize by abscisic acid (ABA) accumulat-
ing endophytic Azospirillum spp. Furthermore, the effect was also seen in IAA and
gibberellin accumulation. Under stress condition, ABA level increases and regulates
plant growth (Sahu et al. 2017) and Bacillus pumilus are reported to promote growth
under water stress (Varma et  al. 2017). P. indica-infected barley plants showed
higher biomass when compared with non-infected plants at salt stress condition
(Waller et al. 2005). Similarly, the plant growth-promoting rhizobacterial (PGPR),
P. fluorescens, an endophyte in eggplant, is antagonistic to Ralstonia solanacearum
by production of siderophores (Ramesh et al. 2009). Neotyphodium and Epichloë of
Festuca rubra are a plant growth promoting endophyte which increase the plant
growth with high uptake of nutrients (Jain and Pundir 2017; Chhipa and Deshmukh
2019). Penicillium sp. from cucumber roots has been found to synthesize Gibberellic
acid and IAA. Inoculating these strains in cucumber plants under drought stress has
shown a significant increase in plant biomass, growth parameters, and assimilation
of essential nutrients and reduced sodium toxicity (Waqas et al. 2012).
Major activities of endophytes include their role as biofertilizer as evident in
banana by Rahnella spp. and Pseudomonas spp. (Ngamau et al. 2012) and corn by
Azotobacter vinelandii, B. subtilis, and Enterobacter cloacae (Varma et al. 2017). A
number of endophytic diazotrophic bacteria have already been reported to colonize
the interior roots of maize, rice, and grasses (Barraquio et al. 1997) and are believed
to be capable of contributing nitrogen nutrition in sugarcane (Boddey et al. 1995),
rice (Yanni et al. 1997), and wheat (Webster et al. 1998). P. indica, a root endophyte,
has been promoted as plant protector, plant growth regulator, and fertilizer in both
agricultural and nonagricultural crops (Schafer et al. 2007). Anuar et al. (2015) iso-
lated Hendersonia Amphinema and Phlebia fungi from trunk and root tissues of oil
palms and observed that Phlebia could serve as a biofertilizer promoting the oil
palm seedlings eventually. These are used as empty fruit bunches (EFB) powder and
real strong bioorganic fertilizer (RSBF) with Phlebia as formulation. The simula-
tions of plant growth executed by plant growth promoters could be attributed in
terms of tolerance to biotic and abiotic stresses and improved plant nutrition
(Machungo et al. 2009).
12 F. A. A. Nouh et al.

1.5  Conclusion and Future Prospects

Soil harbors great diversity of microorganisms; this diversity is responsible for bio-
logical equilibrium created by the associations and interactions of all individuals
found in the community. Plants are the main responsible for most of these interactions
due to their root exudates. These interactions perform significant roles on plant growth
and health and the ecological fitness and resistance of plants to different biotic and
abiotic stresses in soils. Plant–microbe interaction in positive relationship is very ben-
eficial to each other. Mutual relationship in plant microbe associations are mycorrhi-
zas, symbiotic nitrogen-fixing bacteria, and more recently and most interesting
microorganisms endophytes.

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