International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]

https://dx.doi.org/10.22161/ijaers.6.5.17 ISSN: 2349-6495(P) | 2456-1908(O)

A systematic Review and meta-analysis to

Identify and Mitigate the Relationship with the
Plasma Membrane of Plant Water Stress and
Resistance to Pathogens
Daniel Alejandro Kunza, Gustavo Corteza, Jéssica Castro de Carvalho a,
Carlos Eduardo Ribeiro a, Neuton Carlos Palmeiras Galvão a, Elckson
Junior Aquino a, Susana Cristine Siebeneichlera, Magno De Oliveirab,
Paula Santos Alvesb, Wolney Jácomo c, Richard Dias Posselb, Isabela
Maria Agustini da Silveira Bastos a, Aloísio Freitas Chagas Juniord and
Augustus Caeser Franke Portellab
aLaboratory of plant ecophysiology, Federal University of Tocantins, Chácara 69-72 - Rua Badejos, Lote 7, s/n - Jardim
Cervilha, Gurupi, 77404970, Tocantins, Brazil.
b Postgraduate Program in Biotechnology - UFT, PPGBiotec, University Campus of Gurupi - Federal University of
Tocantins - UFT.
cDistance Education - (UFT / EAD)., Public Administration Course, (UFT / EAD). Federal University of Tocantins – UFT.
d Microbiology and Phytopathology Laboratories, Federal University of Tocantins-Campus of Gurupi- UFT.

Abstract— The plasma membrane has very important fields (Sevik and Cetin, 2015; Cetin, 2015; Yigit et al.,
functions, it is composed of a phospholipid bilayer having 2016; Cetin et al., 2018a; Cetin et al., 2018b; Cetin et al.,
a non-uniform and fluid structure that controls input and 2016; Cetin, 2015a).
output of nutrients into the cell and is a way of water Climatic factors are affected by temperature,
transport, whose excess or deficiency affects the plant wind, rain, and drought recent studies with drought stress
development cycle. Depending on the degree of water using remote sensing show monitoring of drought stress.
stress, it can also affect the plant resistance against the It is envisaged that both current land uses and potential
incidence of pathogens that cause great economic losses. future use will be affected by the negative consequences
Fungi and viruses mostly take advantage o f this of possible sea-level rise. The morphological structure of
deficiency, eliminating the plant defense response low elevations suggests that the effects of elevation can
producing molecules for this purpose; however, the plants easily proceed to the interior (Sevik and Cetin, 2015;
employ proteins produced by resistance genes. Cetin, 2015; Yigit et al., 2016; Cetin et al., 2018a; Cetin
Keywords— Water stress, pathogens, plasma membrane et al., 2018b; Cetin et al., 2016; Cetin, 2015a).
resistance. According to Taiz et al. (2017) and Epstein and
Bloom (2006), plant physiology is the study of synthesis
I. INTRODUCTION procedures for plant biological material – e.g. vegetation
Recently researchers found that water stress is growth and the functional process, and its interaction with
important and the effect of the level of stress. It is the environment in which operates . The plant cell plasma
important for irrigation and soils. Also, conducting membrane is an important structure of the cell, being
similar studies on different species and the different composed of a phospholipid bilayer in which proteins are
origins of the species determined to be resistant to inserted or just attached. The most abundant lipids present
drought in wider fields carries great importance in terms in the plasma membrane are the phospholipids, followed
of identifying the species most resistant to drought and in by sterols, which provides mechanical balance on the cell
this way preparing healthy landscaping planning in arid membrane, making it an obstacle to the transport of large

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International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]
https://dx.doi.org/10.22161/ijaers.6.5.17 ISSN: 2349-6495(P) | 2456-1908(O)

portion of hydrophilic molecules and ions (Appezzato-da- physiological stresses can be caused either by excess or
Glória and Carmello-Guerreiro, 2006; Zhou et al., 2018). shortage of water(Rosolem, 2014).
Visually observed in the plasma membrane of Plants placed in mangrove areas, wetlands or
the plant cell that it does not have a uniform structure, but areas near rivers and lakes are subject to stress by excess
rather a heterogeneous mosaic of small territories, where water, which, depending on the intensity, can be lethal
some of them have drowned in specific protein and lipid because it impairs gas exchange between the roots and
constituents, appearing to be stricter and ordered the soil, causing other stress, oxidative (Lopez, 2013).
others suffering strong interactions between different Drought is probably the most important factor in the
molecules, especially the lipids that constitute the agricultural branch, limiting crop yields worldwide, an
membrane (Gerbeau-Pissot et al., 2014; Simon-Plas et al., example is corn: in tropical regions provides 95% of
2011; Taiz et al., 2017). human consumption of cultivars are grown in areas
The plasma membrane has important functions . subject to drought, which consequently generates a
The selective permeability is responsible for selecting the subversion from 10% to 50% of production, 80% in their
entry and exit of substances of the cell, allowing the cultivation areas.
maintenance of its physiological conditions (Appezzato- It should be noted that during the drought, one of
da-Glória and Carmello-Guerreiro, 2006). In this sense, the adaptations of this plant machinery, is the
we can mention aquaporin’s proteins (AQPs) that act on accumulation of solutes in the active cell. This event is
the plasma membrane by increasing its permeability, known as osmotic adjustment, a harmony in the
allowing the transport of water and small molecules conservation of turgor, plant growth and photosynthesis
through the membrane, thereby playing an important role production in low water availability values on the
in water regulation of the cell and the water use sheet(Pimentel, 1999). Due to its complexity, drought
efficiently(Epstein and Bloom, 2006; Lu et al., 2018). tolerance is probably the most difficult feature for genetic
improvement through conventional breeding plants. The
Water stress challenge is even greater for the development of cultivars
The plasma membrane is a phospholipid bilayer, tolerant to drought for the Brazilian environment where
in which various phospholipids are distributed the occurrence and severity of drought may vary each
asymmetrically between the two sheets layers of the year (Petcu et al., 2013; Rosolem, 2014).
membrane forming a primary division of the interior of
the cell (protoplast), and the external space (apop last) The effects of water stress
having a key role in the entry and exit of cell nutrients When the plant is in an environment with
(Epstein and Bloom, 2006; Wang et al., 2018)., One of the sufficient water availability, its cells are in the isotonic
main constraints to plant is water, whose deficit in the state (Figure 1), while with concentrations of solutes in
soil can induce water stress, causing morphological and the internal and external balance. However, when a low
physiological changes, with falls in productivity (Dutra, water availability, the cell before in isotonic state,
2012). The water is the main constituent of plant tissues, performs a process called plasmolysis (Figure 2), in
corresponding in some cases with 95% of the total weight which, due to lack of water causes the extracellular
of the green mass. In this sense, it is very important for medium has a higher solute concentration than the
the healthy development of a plant that its tissues receive intracellular and due to this change in the concentration of
permanently an optimal water amount. The high water extracellular solutes that the water was inside the
content is directly related to the conservation of swelling vacuoles of the cell migrates to the external environment,
of the tissues necessary for photosynthesis, flowering, resulting in the contraction of the vacuoles, giving an
fruiting and condition of origin of products. During the aspect contraction of the cell (Shigematsu et al., 2005).
development of the plant, it performs transpiration,
guttation (or sweating) and exudation, processes that
cause the loss of 98% of the absorbed water(Pes and
Arenhardt, 2015).
The concept of water stress is controversial for a
long time. Inside the agronomic context, water stress is
the availability of water for the plant that generates a
reduction in the economic return of cultivation. in the
physiological context, the problem occurs when a specific
process is affected or not. The agronomic and

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International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]
https://dx.doi.org/10.22161/ijaers.6.5.17 ISSN: 2349-6495(P) | 2456-1908(O)

Losses arising by water stress in agricultural

production depend on the intensity and the duration of
water stress to the crops. If the stress is severe for a long
period of time, the damage can be devastating to crops. If
stress is moderate, with a lower water deficit, the damage
may be reversible or cause less impact on production.
Losses in yield, relate much to the genetic
material and adapted cultured specimen loss or lack of
water (Ryan, 1990). When the plant is under water stress
is the production of proteases, which are proteins related
to the digestion of other proteins (Tremacoldi, 2009); at
the same time is also stimulated the synthesis of protease
Fig.1: Plant tissue, cells in isotonic conditions, using inhibitors to control its proteolytic activity, in the event of
methylene blue colored; microscopy, x400. Source: an uncontrolled way breaks the cell membranes of the
Authors, 2018. plant damage most cellular proteins and a final causes
premature senescence of the plant. Studies on the plant
response to drought in molecular levels show that the
protease inhibitors are also compromised multivalent
proteins in plant defense s against pathogens and
herbivores. Inhibitors also affect the development of
insects indirectly by increasing the production of
digestive proteases to compensate for lower levels of
amino acids available, and these amino acids would be
shifted to the synthesis of more proteases to the detriment
of other essential proteins (Faustino, 2015).
Pathogenic agents
According to Lopez (2013) and Righi (2012),
economic loss as a result of infections in plant material
caused by pathogenic agents is well documented. Fungi
are the main, cause of diseases in plants in the world. A
survey conducted by the Imperial College London and the
University of Oxford (Fisher, 2012), demonstrates that
Fig.2: Plant tissue, plasmolyzed cells using soy crops, rice, corn, wheat, and potato have a
colored methylene blue; microscopy, x400. Source: considerable loss due to successful infection of fungicide,
Authors, 2018. an exorbitant loss that could feed a population of 600
million to 4 billion people. These data reinforce the
According to the authors Fanti and Perez (2004), importance of phytopathological research. Viruses come
the plant when subjected to a high degree of water stress in agronomic half with his percentage of losses in human
or salinity, can cause the non-viability of the germ of the cultures affecting the economies of many countries in the
seed process. In this sense, the reduction of water and world. It is difficult to obtain data from the loss of crops
osmotic potential affects the process of seed development. by viral pathogens (Cavalcante et al., 2013).
The absence of water may also cause the vulnerability of Diseases caused by viruses have less
plants to diseases and pests and can cause the closure of conspicuous than other types of diseases caused by other
stomata, thus reducing the development, resulting in the pathogens. The phytopathological study of plants and
accumulation of solutes and antioxidants, reducing the viruses is important because the viruses have the ability to
development leaf area and stem. Water stress causes the infect a wide variety of existing plant specimens.
synthesis of abscisic acid in the roots, where it is causing Economic losses caused by viral infections has already
root and development and formation of secondary roots been presented since the beginning of the 90s, where in
and is transported by various parts of the plant may have Southeast Asia rice cultivars represented annual losses
other responses, for example, the reduced growth of estimated at one trillion dollars. In the seventeenth
leaves and their abscission or advanced to the century, a viral infection caused frightening losses in the
reproductive cycle. (Fanti and Perez, 2004; Scalon, 2011). production of tulip flowers (Lopez, 2013; Righi, 2012).

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International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]
https://dx.doi.org/10.22161/ijaers.6.5.17 ISSN: 2349-6495(P) | 2456-1908(O)

The infection in plants by pathogens occurs and the major route of contagion by pathogens. This
when the pathogen tried to cross the cuticle, hydrophobic indicates that the closure of the stomata is a functional
layer to the complex aggregate outermost cell walls of the output of pathogens and immune effector. Stomata
epidermis aerial organs. This body serves as a barrier, respond to abiotic and biotic signals, and the pathogens
preventing water loss and infection by pathogens; the cell perform the use of abiotic environmental biological
wall, which serves as a physical and chemical barrier conditions with a high humidity creating active virulence
against the invasion and spread of pests and herbivores; factors causing the closure of the activities of the stomata,
Additionally, released cell wall oligosaccharides act as as a method of its infectious process (Gudesblat et al.,
important signaling molecules, inducing defens e 2009).
responses against pathogens, symbionts and various other
physical and chemical barriers such as the toxic
secondary metabolites produced by plants themselves
(Taiz et al., 2017).
Vegetables have no immune system as animals,
defend cells adapting to the environment that is being
submitted (Rizzardi, 2003). Generally, plants respond to
infection using an innate system of two branches. The
first one is constitutive, also called performed; the second
is induced, also called post-training. The first group refers
to structures synthesized by plants, regardless of the
consequences caused by pathogens, containing various
actions and functions in plant resistance in particular. It
may be noted that in this group there is the presence of
cuticles, stomatal and its numerous forms, conducting
vessels of sap, silica pilosities layers and this group reacts
molecules and common to many classes of microbes, Fig.3: Plant tissue. A1: stomata; A2: stoma; x400
including pathogens. The second group includes the microscopy. Source: Authors, 2018.
mechanisms of resistance whose expression occurs in
response to pathogen infection factors, directly or through Viruses can seep into plant cells by foliar lesions ,
its effects on host targets. that could be the formation of physical impact or insects. They can also be spread by
halos, buds, lignification or cellular barriers or layers of vegetative propagation or by contaminated seeds. Since
cork, abscission layers, Tylose, and gel deposition fungi secrete hydrolytic enzymes such as cutinases,
hesperidin, histological and these barriers (Jones and pectinases, hemicellulases, among others to degrade the
Dangl, 2006). cell wall and into the plant cells (Lopez, 2013; Gerbeau-
According to Stangarlin (2011), pathogens Pissot et al., 2014; Simon-Plas et al., 2011; Taiz et al.,
produce molecules which eliminate the defense response, 2017.).
however, employ vegetable protein produced by the These results suggest that the perception of the
resistance genes, this intense activity of plant defense and plasma membrane signal can direct the cellular response,
recognized as resistance gene-by-gene. The secondary depending on how the membrane reacts and changes its
metabolites with antimicrobial action that have a low inner structure. However, still, need to be explored by
molecular weight are known as phytoalexins, they are which mechanisms these structural changes in the
synthesized by plants in response to physical stress, membrane are translated into defensive reactions
chemical or biological. They are able to reduce or guard (Gerbeau-Pissot et al., 2014; Simon-Plas et al., 2011; Taiz
activities of pathogens, conditioned genotype of the host et al., 2017; Wang et al., 2018).
or pathogen. The operation mode of phytoalexins on fungi In general, it is assumed that resistance to stress
covers the cytoplasmic disintegration, disorder of cellular is cost expensive, mainly due to the need for allocation of
substances, protrusion of the plasma membrane, and metabolites for defense end hindering or interrupting
enzymatic reduction of fungal origin (Gerbeau-Pissot et other physiological processes of the plant, having a
al., 2014; Simon-Plas et al., 2011; Stangarlin, 2011). negative impact on its development (Bacete et al., 2018).
The main pathogens invasion routes are the
stomata (Figure 3), and recent research has proven II. MATERIAL AND METHODS
regulatory action is closing and opening of this structure The methodology was based on Oliveira, (2018).

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International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]
https://dx.doi.org/10.22161/ijaers.6.5.17 ISSN: 2349-6495(P) | 2456-1908(O)

To identify articles on the subject was held The grouped articles were excluded in order:
search in the databases PubMed, ScienceDirect, Sciullo, repeated irrelevant review, other publishing formats
Google Scholar, Dialnet, WorldWideScience.org, (notice, short communications, perspectives, letters), and
Tandfonline, Dialnet, Microsoft Academic. The following other languages. In addition, manual searches were made
filters have been added to search on ScienceDirect: only in reference lists of review articles found with the
journals; title, abstract; key-words: “Water stress” predetermined keywords.
“pathogens” “plasma membrane resistance”. After removal of the articles repeated between
After consultation, the application databases and the different searches, the exclusion criteria were applied,
search strategy between different studies repeated as shown in Figure 4. Of the 111 remaining articles were
searches were identified. Inclusion criteria for articles retrieved 35 original research articles related to the
were original research articles and conceptualize the plasma membrane and plant water stress and resistance to
research related to the plasma membrane of the plant cell, pathogens. Through manual search were recovered 2
giving greater emphasis on their role in resistance to more items.
incoming interrelated in pathogens during water stress, in
different fields of research, including research completed
in Portuguese, English, and French.

Fig.4: Flowchart of identification and selection of items. Source: Authors, 2018.

III. RESULTS AND DISCUSSIONS There was also little information about the viral
This work focuses on the issue of the operation origin of pathogens in plants, a fact that further limited
of the plasma membrane of plant cells, giving greater the theme of development. In this research, it was found
emphasis on their role in resistance to drought stress and that the papers have a relationship study of 14.71% of
the entry of pathogens. Based on the research conducted, fungal diseases as statistical relationships demonstrate in
few papers that analyzed pathologies of bacterial origin, Table 1, summarize the work of several authors. It was
which indicates the need to carry out further searches of evident the need to develop more studies on the origin of
bacterial pathogens in vegetable medium demonstrating a pathologies both bacteria with other diseases, as there are
total of 5.88% of study bacteria (Figure 1). Both through many studies on fungi in the Brazilian and international
the internet, as for books surveyed for this review, it agriculture. Future prospects seek the inclusion of a
became clear the lack of information on diseases caused greater number of researches on various plant diseases.
by both bacteria and other neglected diseases.

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International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]
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Table.1: Correlation of articles and pathologies found during the research and its percentages.
PATHOLOGIES REFERENCES TOTAL %
LOPEZ., 2013
TAIZ ET AL. ,2017
VIRUS BOTÂNICA NO INVERNO 2012 5 14,71
GALDEANO, KLEINGESINDS,2013
MOLLIER,2014
JORDI LUQUE, 1997
UTA FUCHS, 2006
MÁRIO LÚCIO, 2003
CAVALVANTE FLÁVIA, 2013
FUNGI ADNE ABBUD, 2013 9 26,47
LAURA BACETE, 2017
BENJAMIN PETRE, 2014
FANTI SILMARA, 2004
STANGARLIN, 2010
LAURA BACETE, 2017
FERRO, M.I.T.,2006

BACTERIUM 2 5,88

RIZZARDI MAURO, 2003

RESENDE MÁRIO,2003
FERRO, M.I.T.,2006
FEW DISEASES STUDIED NAT REV MOL CELL BIOL. 2008 4 11,76

Total 20 58,82

This is the fact that fungi are the causative of drought, which related to challenges of phenotyping and
larger diseases in world agriculture, viruses are also a characterization of these, materials tolerant pathogens
major cause of it. There is a need to conduct further study during stress water. In the scientific community towards
on the pathology of the Bacteriological source and its the real cause of diseases during drought pres ents a major
consequences for plant use in global agronomy. debate with several disagreements among researchers.
During our research for this review, the authors The authors mentioned that we have access to
reported in their serious problems jobs, there is no way the use of technologies that can mitigate these factors,
around them completely, since these are unpredictable those that have provided solutions to various problems. In
because the consequences will vary on the event period, relation to water stress, it is possible to increase some
the degree of intensity and the reaction presented by strategies to meet the momentary need to pass the plants,
plants. In many cases the damage caused by water stress such as the rational use of water dams will result in less
and/or pathogens irreversible. wear of the plant, bringing benefits to the vegetation
It is clear to point out that there are changes in around them. Thus, it is noteworthy that the importance of
the defense mechanisms of plants when they undergo studies of environmental rationing, conscious and agro-
water stress, this can result in infectious agents actions, ecological, the rational use of water resources directed to
but these are not invulnerable, there will be the moment agricultural production and in its different productive
that will hit the limit (total system loss of defense) and sectors.
thus suffered major damage, such as the weakening of We should point out that the motivating text
your metabolism or even death. also caveat some possible ways to partially protect plants
Currently, transgenic approaches have been from invading pathogens, such as the use of chemicals
presented as a solution in research to create an that can stimulate the synthesis of protease inhibitors to
opportunity to light the production of various crops in control their proteolytic activity, such action would help
drought conditions or water deficit. Although it has a strengthen the immune system of the plant and thus
comprehensive range study of tolerance to drought, there generate many benefits to agriculture.
are challenges associated with the phenotype and
identification of materials tolerant to diseases during the

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International Journal of Advanced Engineering Research and Science (IJAERS) [Vol-6, Issue-5, May- 2019]
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CONFLICT OF INTERESTS [13] Gerbeau-Pissot P, Der CD, Thomas, Anca IA,
The authors have not declared any conflict of interests. Grosjean K, Roche Y, Perrier-cartucho JM,
Mongrand S-Plas, Simon F (2014). Modification of
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