Water unavailability, which prevails
due to drought, salinity or freezing, is a major limitation for plant growth
and development (Lesk et al. 2016). The coming decades are likely to
experience more frequent episodes of severe drought due to the worsening global
climate with potentially devastating impact on agriculture (IPCC 2014). This
will pose further challenges to feed a growing world population. Given its
threat to agriculture, plant physiology under drought stress has been
extensively studied. This has significantly improved our understanding of the
responses of plant to water limitation. Plants employ a complex of
interconnected physiological, physical and molecular mechanisms to respond to
drought stress (Chaves et al. 2003; Farooq et al. 2009; Kaur and
Asthir 2017; Kumar et al. 2018; Deepak et al. 2019; Jangra et
al. 2019). Plant stress research also takes into account an important part
of plant biology—the plant-microbe interaction, but its impact in modulating
plant tolerance to stress.
Our
correct understanding is that plants are not independent entities with respect
to their ecological and physiological function. In nature, plants afford a
unique ecological niche for plethora of microorganisms for example, archaea,
bacteria, fungi, virus, protozoa etc.
A diverse kind of relationship exists between plant and these microbes
including but not limited to mutualism and antagonism. The most well documented
example is the mycorrhizae-plant mutualism, where both entities are helped by
each other. In nature, plants also harbour endophytic fungi and viruses. These
can be mutualists, or pathogens of the host plant depending on the host,
microbe and ecological factors. Available
studies suggest that fungal endophytes are present in all terrestrial plants.
It is reported that, endophytes provide nutritional benefit to plants as well
as confer many other benefits such as protection from biotic and abiotic
stresses (see recent reviews by Rodriguez et al. 2009;
Busby et al. 2016; Lugtenberg et al. 2016; Dastogeer and Wylie 2017; Aamir et al. 2020; Kaur 2020).
Plants
also harbour an uncountable number of viruses that are rarely common in many
other host types. Depending on the type of virus, host and environment, the
interaction between virus and plant could range from mutualistic to pathogenic
(Roossinck 2011). Since the discovery of the first virus in 1898 (Beijerinck
1898), most of the plant viruses documented to date are isolated and studied as
pathogens that incite diseases in crop plants (Zaitlin and Palukaitis 2000).
However, in the natural environment, viruses are present in good number in many
symptomatic or asymptomatic plants, but not all viruses cause disease, and some
virus are beneficial (Roossinck 2010). The world of beneficial viruses is
unknown in most cases, but they have been reported from a wide range of hosts
including plants, bacteria, fungi and other eukaryotic microbes, insects and
humans and other animals. Beneficial effects of some plant viruses are evident,
and they exhibit context dependent mutualism and confer fitness benefit to host
under abiotic stress. For example, improved drought stress tolerance was
recorded in some cultivated and wild crops like beet, tomato, rice, watermelon
and nicotiana when treated with virus (Xu et al. 2008; Dastogeer et
al. 2018). The underlying mechanism for this noteworthy observation is
unknown it was found that virus infection increased the water content, water
retention and the level salicylic acid and some osmoprotectants and
antioxidants making the plant more tolerant to water-limiting condition (Xu et
al. 2008). When the roles of microbial symbionts of plants are studied,
most research has concentrated either on direct, pair-wise interactions of the
plant and an endophyte or three-way interactions including insects. However, a
very interesting linkage of a different kind subsists among plant, endophytes
and viruses. In one case, it has been found that a virus in a Curvularia
fungus remains as an obligate symbiont to form a tripartite interaction that
helps plants to grow in soils with higher temperature in Yellowstone National
Park (Márquez et al. 2007).
In
nature, plants are subjected to a mixture of biotic and environmental stresses
at the same time, therefore it is plausible that the stress signalling mechanisms
could share some common pathways and their consequences may overlap
considerably in favour of plants to survive under complex ecological settings.
Reports suggest that plants ability to respond to water limitation could be
improved by symbiotic fungal endophytes (Hubbard et al. 2014; Ghaffari et al. 2019; Sadeghi et al. 2020) and viruses (Xu et al.
2008), individually or in group. In this review, we aimed to discuss the recent
literature available on endophyte and virus-mediated drought tolerance in
plants. We anticipate this will be helpful for the researcher working in this
field to design and plan their research for further advancement in
understanding plant-microbe interaction and plant stress tolerance.
Impact
of drought
on crop production worldwide
Severe
droughts have caused substantial decline in crop yields through negative
impacts on plant growth, physiology, and reproduction. A metanalysis of the
data from 1980 to 2015 reported a global reduction of yield up to 21 and 40% in
wheat and maize crop, respectively due to drought (Daryanto et al.
2016). By using deterministic approaches previous studies analysed the impact
of drought on crop production in Australia (Madadgar et al. 2017), China
(Yu et al. 2014), Czech (Hlavinka et al. 2009), Moldova (Potopová
et al. 2016), South Africa (Araujo et al. 2016), United States
(Troy et al. 2015; Zipper et al. 2016), and worldwide (Lesk et
al. 2016; Matiu et al. 2017). A global yield loss analysis due to
drought in the year 1983 to 2009 showed that the averages of drought-induced
yield losses per drought event was 8% for wheat, 7% for maize and soy, and 3%
for rice; which correspond to 0.29, 0.24, 0.15, and 0.13 t ha-1,
respectively (Kim et al. 2019). The global loss of cereal has been
reported to 4.9–5.2% for the period of 1964–2007 using the superposed epoch
analysis (Lesk et al. 2016). Under drought conditions wheat crop is the
most vulnerable crop in USA and Canada, maize in India and rice is most
affected in Vietnam and Thailand (Leng and Hall 2019).
The
devastating losses of crop production due to droughts are generally witnessed
in developing countries, and the most vulnerable regions to drought are situated
in Sub-Saharan Africa and some parts of Asia. African countries face drought
every year in some places or other. It was estimated that losses due to drought
in 2014–2017 was on average USD $372 billion (Ngumbi 2019) in the African
continent. In South Africa, an El Nińo drought which began in 2018 and
continued to 2020 has been expected to cause a huge loss in crop yield by 20%
of the major crops such as wheat, apple, grape and pear (Roelf 2018). A minimum
of 23 million hectares in Asia (20% of the total rice area) are prone droughts
of varying degrees which is one of the most critical factors causing reduced
and unstable farm production (Pandey and Bhandari 2009). Pakistan experienced
droughts recurrently every four in 10 years (Anjum et al. 2012). The
drought in 1998–2002 resulted loss of rain-fed crop yields by 60–80%, irrigated
crop yields by 15–20% (FAO/WFP 2002; Sarwar 2008). There have been La Nina
events during the years 2000–2010 which resulted in extreme heat and low
rainfall in Pakistan. It has been predicted that temperatures will increase on
average by 2–3oC by 2045-65, especially in parts of South Asia
including Pakistan (IPCC 2014). In Bangladesh annually about 2.7 million
hectares of crop land affected by droughts (Tanner et al. 2007) and
nearly 83% of the Kharif and Rabi crop lands are exposed to different
magnitudes of droughts as shown by Climate Change Cell of Bangladesh which has
been reported by Alamgir et al. (2019). China experienced the worst
drought in 2010–2011 that impacted eight provinces in the northern part of the
country. Around 20% of the farmland and 35% of the entire wheat crop were
damaged due to that drought in the affected china provinces (Krishnan 2011).
Maize and soybean are most affected by drought in China a yield reduction of
6.4 and 9.2% respectively (Liu and Shi 2019).
As a result of availability or
resources to lessen the effect and adopting the measures, the impact of drought
has a propensity to be less extreme on crop production in developed nations.
However, crop damages could be high enough despite all kinds of intervention. A
recent case in the USA in 2012 when a severe drought affected 80% of cropped
land and decreased yields of corn by 27.5% and of soybean by 10% with massive
financial losses (USDA 2013). The 2010 droughts in Russia caused reduction in
wheat harvest by 32.7% severely diminishing the worldwide wheat supply
(Sternberg 2011). The Mediterranean region is also vulnerable to climate change
and drought cause affects crop production in these regions (IPCC 2014; EEA 2016).
For example, Spain has faced episodes of drought in the recent times, which are
in the most severe form in Europe causing an estimated agricultural loss of EUR
3600 million (González-Hidalgo et al. 2018; Peńa-Gallardo et al.
2019).
It is
projected that climate change in the coming decades will alter average
temperature and rainfall values and will increase the unpredictability of
precipitation events which may lead to even more severe and frequent droughts
with a raise from 1 to 30% in extreme drought prone regions by 2100 (IPCC 2014;
Webber et al. 2018; Tibebe et al. 2019; Lee et al. 2019; Spinoni et al. 2020).
Effects of water stress and plant response mechanisms
Water limitation at any stage of
the growth of crops can be detrimental. But the extent of adverse effects is
dependent on the magnitude of stress and crop growth stage as well as other
environmental factors. Numerous studies have been performed to discern the
impacts of water stress on plants and several reviews are available (Farooq et
al. 2009; Silva et al. 2013; Fathi and Tari 2016; Dastogeer and
Wylie 2017; Hussain et al. 2018) that well explained these effects how
plant responds to stress at the morphological, genetical, biochemical, and
molecular levels (Fig. 1). Plants need a vast quantity of water and nutrient
for their survival and development. Plant draws water and most nutrient from
the soil, so a reduction in soil moisture exerts detrimental effects on plant
healthy growth. Scarcity in soil water leads to changes in the physical
condition, which in turn negatively impact plant physiological and biochemical
processes (Silva et al. 2009; Deepak et al. 2019). Lack of water
also reduces nutrient uptake even in the soil with enough nutrient, due the
decreased mobility and absorbance of individual nutrients. It causes reduced
mineral diffusion from the soil matrix to the roots.
Fig.
1:
Schematic diagram showing how drought causes negative impacts on plant growth
and yield
Morphologically,
some plants are more sensitive to drought than others. The seed germination and
seedling vigour of some plants are affected more severely under scarce water
condition. For example, in a laboratory experiment Glycine max has been
shown to be less affected by simulated drought as compared to Macrotyloma
uniflorum and Vigna mungo (Pantola et al. 2017). Also,
subsequent development of plants is significantly affected by drought. Limited
water may cause a decrease in plant height, leaf size, and root and shoot
biomass of plants (Farooq et al. 2009; Zheng et al. 2016). Water
stress also has negative impacts on crop yield (Table 1) and yield parameters
which were reported for many plants such as cotton, maize, peanut, sugarcane,
sunflower and wheat (Pettigrew 2004; Vasantha et al. 2005; Barnabás et
al. 2008; Furlan et al. 2012). The reductions in plant growth and
yield are associated with drought-induced alterations at the physiological,
metabolic and molecular levels. For example, water scarcity causes a reduction
in the photosynthesis and alters gaseous exchange plants. The effects on
photosynthesis are associated with reduced leaf area and reduced photosynthesis
rate in unit leaf area (Wahid et al. 2005). Other possible mechanisms
could be the direct effect on plant metabolic activities or by restricting the
CO2 access through the leaf (Apel and Hirt 2004), discrepancy in light
harvesting and utilization (Foyer and Noctor 2000), reduced Rubisco activity
(Bota et al. 2004), changes of pigments of photosynthesis (Anjum et
al. 2003) and impairment of photosynthetic apparatus (Fu and Huang 2001).
Table 1: Percent yield losses in some important crops caused by drought stress.
|
Crop name |
Yield losses
(%) |
References |
|
Rice |
53–92 |
Lafitte et
al. (2007) |
|
Wheat |
57 |
Balla et
al. (2011) |
|
Maize |
63-87 |
Kamara
et al. (2003) |
|
Chickpea |
45–69 |
Nayyar et
al. (2006) |
|
Soybean |
46–71 |
Samarah et
al. (2006) |
|
Sunflower
|
60 |
Mazahery-Laghab
et al. (2003) |
|
Lentil |
24-70 |
Shrestha et al. (2006); Allahmoradi et
al. (2013) |
|
Faba bean |
68 |
Ghassemi-Golezani and Hosseinzadeh-Mahootchy 2009 |
|
Mung bean |
26-57 |
Ranawake et al. (2011); Ahmad et al. (2015) |
|
Common bean |
40-60 |
Martínez et al. (2007); Rosales-Serna et al. (2004); Ghanbari et al. (2013) |
Water
unavailability at the vicinity of plant roots causes significant reduction in
relative water content and water potential of the leaf, turgor pressure, as
well as the rate of transpiration (Nayyar and Gupta 2006; Campos et al.
2011) which have negative impacts on plant-water relation. Plants grown under
low soil moisture showed reduced growth of roots and lower amount of nutrient
uptake (Subramanian et al. 2006; Asrar and Elhindi 2011; Suriyagoda et
al. 2014). Plants have decreased absorption of some cations (K+,
Ca2+, and Mg2+) due to the disparity in active transport
and permeability of cell membrane under stress (Hu and Schmidhalter 2005;
Farooq et al. 2009). Also, water stress inhibits some enzymes activities
and thus affects plant nutrient assimilation (Ashraf and Iram 2005). Higher
accumulation of reactive oxygen species (ROS) in plant under stress is common
and is associated with insufficient CO2 fixation and increased
photorespiration (Carvalho 2008; Gill and Tuteja 2010).
Several
studies identified several genes that are associated with plant response to
water deficit stress. For example, Benny et al. (2019) used RNA-seq
analysis of different plant species subjected to drought and identified 27
genes that were differentially expressed due to stress. The down-regulated
genes were related to cell wall and membrane structure formation and fatty acid
biosynthesis whereas the up-regulated were related to osmotic stress,
abscisic-activated signalling pathway and hydrogen peroxide treatment stress. The
important transcription factor (TF) families such as MYB, WRKY, bZIPs are
involved in plant stress responses (Qin et al. 2011). Drought-induced
modulation of ABA level modulates expression certain genes including dehydrin
genes and glycine-rich protein gene. The expression of the gene miR398 was
upregulated in drought stressed peanut while certain other genes downregulated
significantly. Several other genes or transcription factors (TFs) have also
been reported including but not limited to AP2/ERF, bZIP, HD-ZIP, bHLH, MYB,
NF-Y, EAR, NAC, and ZPT2 were differentially expressed under water stress
(Bhargava and Sawant 2013). Over the past decades, various works have been
carried out to reveal the mechanism of plant responses under drought at the
physiological, biochemical, molecular and genomics levels. Plant behaviour
under stress is complicated since it depends on space and time, the integration
of stress effects and responses at all underlying levels of organization. All
these mechanisms could be grouped under, morphological: drought escaping
(changing life cycle), or avoidance (alterations in nutrient and water uptake)
or, abandonment (removing parts of plant e.g. leaf); or physiological:
drought tolerance (maintain better osmotic balance and preserve tissue
turgidity or resistance (metabolic changes) (Chaves et al. 2003; Nadeem et
al. 2019).
Fungal endophyte and plant abiotic
stress tolerance
Endophytes are the organisms that inhabit in the plant without apparently causing any damage to
the host at any time in their life cycle (Schulz
and Boyle 2005). The presence of fungal endophytes traced in the fossil
records proposes that fungal endophyte may have
evolved during the terrestrialization of land plants (Rodriguez and Redman
1997; Krings et al. 2012).
The endophytic fungi have been isolated
from various types of plants including conifers, grasses, marine algae,
lichens, mosses, ferns and pteridophytes (Li et
al. 2007; Melo et al. 2014; Eo and Park 2019; Gao et
al. 2019). Majority of the
fungal endophytes form mutualism with hosts. Some of them can be pathogenic to
plant based on the growth stage and defence of the plant and environmental
factors (Schulz and Boyle 2005).
Certain fungal endophytes provide nutritional
benefits to plants. Many others provide significant
adaptation and fitness benefits to plants (Rodriguez et al. 2009; Dastogeer et al. 2018; Aamir et al. 2020). Researches have shown endophytic fungi in both
below ground and above ground plant tissues can shield their host plant from drought stress (Sherameti et al. 2008; Sun et al. 2010;
Hubbard et al. 2014; Husaini et al. 2012; Sadeghi et al. 2020). For Example, Neotyphodium coenophialum
enhance the drought tolerance in tall fescue (Lolium arundinaceum) and perennial ryegrass and perhaps it is the
most widely documented feature of endophyte mediated abiotic-stress tolerance
plants (Bouton et al. 1993; Malinowski et
al. 1997b). In one of our study
we experimentally shown that several
non-grass endophytes isolated from wild Nicotiana plants when
re-inoculated increased the drought tolerance of N. benthamina both in vitro and
glasshouse condition (Dastogeer et
al. 2017b). Subsequently, we have found these endophytes
mediated plant drought tolerance is associated
with changes in stress-related
metabolites, changes in antioxidants, osmolytes and altered expression in
stress-related genes (Dastogeer et
al. 2017a; Dastogeer et
al. 2018). Kane (2011) reported that Neotyphodium lolii
can provide drought stress tolerance to native perennial ryegrass collections
formerly obtained from Mediterranean regions. In
one study, a consortium of fungal endophytes was assessed for their effect on
the growth, eco-physiological and reproductive success of wheat under heat and
drought stress. The findings indicated that the endophytes improved the ability
of wheat plant to tolerate drought and
heat. Interestingly, seeds produced from
drought-stressed wheat infected by the endophyte in the following generation
had decreased water use efficiency compared to those produced by drought-affected plants with no endophyte
infection. However, regarding vigour endophyte-free stressed parents’
germinated seeds more rapidly than those produced by endophyte colonised plants (Hubbard et al. 2014).
In an effort to explain the mechanism
endophyte mediated drought tolerance in plants, scientists have documented
several observations. Similar to mycorrhizal fungi, non-mycorrhizal
fungal endophytes employ various strategies including modulating, changing or
modifying plant physiology, biochemicals and metabolites (see review by Dastogeer and Wylie 2017). Table 2 lists some
of the available literature that presents
fungal endophyte mediated plant stress tolerance. Endophyte-mediated plant responses to drought may be
associated with (a) increase or decrease in plant growth (b) enhanced
photosynthesis (c) osmotic balance, (d) increased gaseous exchange and
water-use efficiency and (e) enhanced antioxidant activities (f) altered
expression of droguht releted genes. For example, a number of fungal endophytic have been
reported to produce biomolecules and metabolic substances (Rasmussen et al. 2008; Nagabhyru et al. 2013) that help the plant
stand in the water limiting environment. Some physiological alterations such altered water potential,
increased osmotic balance and augmented growth and development in tall fescue as a result of N. coenophialum infection have also been observed (Elmi and West 1995).
However, it is important to
note that that endophyte colonization in plant
does not always benefit plant in abiotic stress condition rather their association could be detrimental
for plants in some cases (Cheplick 2004). In a review, Cheplick (2007) outlined the effect of endophytes on stress tolerance and
mentioned some studies that found a neutral role of endophytes on host drought
tolerance. For instance, inoculation of fine fescue with Neotyphodium
originally isolated from dissimilar host gave variable results in that some
genotype decreased biomass, other were neutral while some showed positive
influence (Zaurov et al. 2001). Also, some strains improved plant aluminium
tolerance; others were showed no or negative tolerance compared to endophyte-free
counterpart indicating genotype specificity of
interactions. By a meta-analysis, Dastogeer
(2018) showed fungal endophytes influenced on plant performance in a
context dependent manner. The degree of endophytic effects is higher in plants
grown in drought than those in normal
watering condition. The fate of interactions is dependent on the identity of
the plant host and fungal symbionts.
Plant virus and abiotic stress tolerance in plant
Viruses are considered to be
the most abundant biological beings on the planet (Suttle 2007). Every
living being can be infected by at least one and
normally several viruses and most
organisms are infected by a diverse and
unknown group of viruses. Plants afford enormous
number of viruses that are not very
common in many other host kingdoms. These viruses use host machinery and
resources for their replication and transmission, so it is embedded in our belief that virus infections must always be
harmful to their host (Xu et al. 2008). Indeed, most of plant viruses documented to date are identified
and studied as pathogens that incite diseases in crop plants (Zaitlin and Palukaitis 2000). The first virus
identified was tobacco mosaic virus (Beijerinck
1898) and there are over 1000
classified plant viral pathogens (Gergerich and Dolja 2006). Viruses are rarely considered outside of their role as
pathogens. In the natural
non-agricultural environment, RNA viruses are present in good number in many of the studied
symptomatic or asymptomatic plants, but
their ecological roles have not been known
to the most part (Xu et al. 2008). Depending on the
nature of virus, host and the environment the interaction between virus and
plant could range from mutualistic to pathogenic (Roossinck 2011).
The
world of beneficial viruses is unknown in most cases, but they have been found in a wide range of hosts including plants, bacteria, fungi and other eukaryotic microbes, insects and humans and other
animals. Beneficial effects of some plant viruses are evident, and they exhibit conditional mutualism and
confer abiotic stress tolerance to plants. When Nicotiana
benthamiana plants were infected with viruses with varying host range such
as, cucumber mosaic
Table
2:
Endophyte mediated plant drought stress tolerance.
|
Endophyte
|
Plant
|
Reference |
Major
effects/Mechanism(s) in brief |
|
Acremonium
strictum |
Atractylodes
lancea |
Yang et al. (2014) |
Decrease
tiller number and length, decrease total fresh weight, shoot and root fresh
weight and increase root/shoot ratio, decrease SOD and POD, increase
malondialdehyde (MDA) and CAT accumulation, increase proline, soluble sugar and
soluble protein under mild stress. |
|
Acremonium
sclerotigenum, S. implicatum |
Triticum
aestivum (Wheat) |
Llorens et al. (2019) |
Reduce
levels of stress damage markers, stress‐adaptation metabolites. |
|
Acrocalymma
vagum, Paraboeremia putaminum, Fusarium acuminatum |
Glycyrrhiza
uralensis |
He et al. (2019) |
Increase
AMF fungi, soil organic matter, available phosphorus (P), leaf number,
soluble protein, SOD activity, total root length, root branch, and
glycyrrhizic acid content. |
|
Acrocalymma
vagum |
Ormosia
hosiei |
Liu and Wei (2019) |
Increase
fresh root weight, root volume, root surface area, root fork, and root tip
number. Inoculated seedlings changed
from herringbone branching to dichotomous branching. Mitochondria and other
organelles in root cells of inoculated seedlings remained largely undamaged
under water stress. ABAand IAA content and IAA/ABA ratio of inoculated
seedlings were significantly higher, whereas the content of GA, GA/ABA,
zeatin riboside (ZR)/ABA, and ZR/IAA in inoculated seedlings were lower. |
|
Alternaria spp. |
Astragalus spp. Oxytropis spp. |
Klypina et al. (2017) |
Endophyte did not influence photosynthetic gas exchange and leaf
pigment concentrations. |
|
Alternaria alternata |
Triticum aestivum (Wheat) |
Qiang et al. (2019) |
Endophyte
secretes indole acetic acid (IAA) by both the tryptophan-dependent and
independent manner. Endophyte alter antioxidant enzyme activities, level of
soluble sugars and proline, increase photosynthesis, C and N accumulation,
plant dry biomass. |
|
Aspergillus fumigatus |
Oryza sativa |
Qin et al. (2019) |
Higher
antioxidant capacity both in vivo and in vitro. (Z)-N-(4-hydroxystyryl)
formamide (NFA), an analogue of coumarin was responsible for antioxidant
activity. |
|
Balansia
henningsiana |
Panicum
rigidulum |
Ren and Clayy (2009) |
Increase tiller number, leaf number, and the
root: shoot ratio and photosynthetic pigment and decrease shoot height and
leaf area. Increase |
|
Beauveria
bassiana |
Quercus
rubra, Zea mays |
Ferus et al. (2019);
Kuzhuppillymyal-Prabhakarankutty et al. (2020) |
Increase
leaf relative water content and stomatal conductance, stimulated root growth.
A strain increase germination percentage. Early flowering. |
|
Chaetomium
globosum |
Triticum aestivum (Wheat) |
Cong et al. (2015) |
Increase
root:
shoot ratio, proline content, protein content, and (MDA) content |
|
Cladosporium
cladosporioides, Unknown
ascomycota |
Nicotiana
benthamiana |
Dastogeer et al. (2017a) |
Changes in sugars, sugar alcohols, amino acids and other
metabolites; increase root dry mass and relative water
content (RWC) |
|
Dastogeer 2018 |
Increases plant biomass, RWC,
soluble sugar, soluble protein, proline content, CAT, POD, and PPO and
decrease production H2O2, EC. Upregulation of drought
associated genes. |
||
|
Cladosporium
oxysporum, Embellisia chlamydospore, Paraphoma spp., |
H.
scoparium, Glycyrrhiza uralensis, Zea mays |
Li et al. (2019) |
For H. scoparium, fungi improved the root
biomass and length based on fungi. Paraphoma
spp. and C. oxysporum had positive effects always. For G. uralensis
and Z. mays, endophyte enhanced the root of plants under MD condition
and was dependent on the plant–fungus species |
|
Epichloe
amarillans |
Agrostis
hyemalis |
Davitt et al. (2011) |
Increase
inflorescence number and seed mass. |
|
E. bromicola |
Leymus
chinensis |
Wu et al. (2016) |
Increase root biomass and WUE (water use
efficiency). |
|
Ren et al. (2014) |
Increase total biomass. |
||
|
E. coenophiala (some reported
as Neotyphodium coenophialum or Acremonium coenophialum) |
Festuca
arundinacea |
Assuero et al. (2006) |
Increase dry mass. |
|
Assuero et al. (2000) |
Decrease
dry weight and tiller number. |
||
|
Elmi and West (1995) |
Increase tiller survival and leaf elongation
rates. |
||
|
Hosseini et al. (2016) |
Increase plant available water (PAW). |
||
|
Hill et al. (1996) |
Increase leaf water potential and turgor
pressure. |
||
|
West et al. (1993) |
Enhance tiller density and survival. |
||
|
White et al. (1992) |
No evidence for endophyte-mediated drought
tolerance |
||
|
E. elymi |
Elymus
virginicus |
Rudgers and Swafford (2009) |
Increase tillers number and root biomass |
|
E. festucae var.
lolii (some reported as N. lolii) |
Lolium
perenne |
Amalric et al. (1999) |
Increase number of suckers, water potential,
stomatal conductance, transpiration rate, net photosynthetic rate, and photorespiratory
electron: transport rate. |
|
Briggs et al. (2013) |
Decrease shoot’s
fresh weight. |
||
|
Cheplick et al. (2000) |
Decrease tiller production. |
||
|
Cheplick (2004) |
Decrease tillers, leaf area and total mass. |
||
|
Gibert et al. (2012) |
Decrease biomass production. |
||
|
He et al. (2017) |
Increase
shoot’s drymass. |
||
|
Kane (2011) |
Increase
tiller number, greater tiller lengths, total dry mass and green shoot mass. |
||
|
Malinowski et al. (2005) |
Increase
tiller survival |
||
|
Ren et al. (2006) |
Increase
plant biomass, soluble sugar, tiller number and chlorophyll. |
||
|
E. festucae |
Festuca eskia |
Gibert and Hazard (2011) |
Increase
seedling survival. |
|
Festuca rubra |
Vazquez-de-Aldana et al.
(2013) |
Changes
in root/shoot ratio |
|
|
Achnatherum robustum
(Bunchgrass) |
Hamilton and Bauerle (2012) |
Increase CAT, APA (Ascorbate Peroxidase Acivity), and GR (Glutathione Reductase) |
|
|
Achnatherum sibiricum |
Han et al. (2011) |
No effect on total biomass and chlorophyll
content, increase photochemical efficiency (Fv/ Fm) and carotenoid content,
reduce malondialdehyde (MDA) and no effect on superoxide dismutase (SOD) and
catalase (CAT) |
|
|
Ren et al. (2011) |
Increase
photosynthetic rate. |
||
|
Elymus dahuricus |
Zhang and Nan (2007) |
Increase tiller number, plant height
chlorophyll content, biomass, SOD, POD, RWC, CAT, APX, Proline and decrease H2O2. |
|
|
Zhang and Nan (2010) |
Increase
biomass, plant height and tiller numbers, SOD, POD, CAT and APX, proline
chlorophyll content and decrease H2O2. |
||
|
Festucae latior
(Meadow
fescue) |
Malinowski et al. (1997a) |
Decrease shoot and root drymass. |
|
|
Hordelymus
europaeus |
Oberhofer et al. (2014) |
Increased plant biomass and tiller production. |
|
|
Lolium
perenne (Ryegrass) |
Hahn et al. (2008) |
Decrease
Osmotic potential, herbage yield and proline content, Increase RWC. |
|
|
He et al. (2017) |
Increase
shoot’s drymass. |
||
|
Hesse et al. (2003) |
Increase vegetative tiller, total dry
mass, shoot
mass, root mass and
root/shoot
ratio in dry cultivar |
||
|
Hesse et al. (2005) |
Decrease vegetative tiller and drymass. |
Table 2: Continued
|
|
|
Hesse et al. (2005) |
Decrease vegetative tiller and drymass. |
|
Oliveira et al. (1997) |
Increase water potential. |
||
|
Lolium multiflorum |
Gundel et al. (2006) |
Increase seed
germination. |
|
|
Epichloë sinica |
Roegneria kamoji |
Bu et al. (2019) |
Enhance seed
germination, Decrease ROS. |
|
Exophiala pisciphila |
Sorghum
bicolor (sorghum) |
Zhang and Nan (2010) |
Increase seed
germination. |
|
Exophiala spp. |
Cucumis
sativus |
Khan et al. (2011) |
Altered levels of
stress-responsive ABA, Increase levels of SA and bioactive Gas, GA3 and GA4. |
|
Fusarium spp. |
Solanum lycopersicum (Tomato) |
Azad and Kaminskyj (2016) |
Increase shoot and root biomass, Fv/Fm. |
|
Neotyphodium (rather than Epichloë) |
Poa alsodes
(Grove
bluegrass) |
Kannadan and Rudgers (2008) |
Increase total biomass, shoot and root
biomass, Root/soot ratio, decrease RWC. |
|
N. occultans |
Lolium multiflorum |
Miranda et al. (2011) |
Increase tillering. |
|
N. starrii |
Festuca arizonica
Vasey |
Morse et al. (2002) |
Increase net photosynthesis, leaf
conductance, leaf are ratio, total biomass, shoo and root biomass, water potential. |
|
N. uncinatum |
Meadow Fescue |
Malinowski et al. (1997b) |
Decrease tiller weight and water potential |
|
Penicillium brevicompactum,
P. chrysogenum, |
Lactuca sativa (Lettuce) |
Molina-Montenegro et al.
(2016) |
Increase total biomass, shoot biomass and
proline content, decrease root biomass and Peroxidation of lipids (TBARS). |
|
P. minioluteum |
Chenopodium quinoa |
González-Teuber
et al. (2018) |
Improve root
formation. |
|
P. resedanum |
Capsicum annuum |
Khan et al. (2013) |
Increase chlorophyll content, shoot length,
POD, CAT, GR, polyphenol, SA and Decrease EC, MDA. |
|
Hordeum vulgare (Barley) |
Ghabooli et al. (2013) |
Increase shoot and biomass. |
|
|
Capsicum annuum |
Khan et al. (2015) |
Increase chlorophyll content, soot mass,
shoot length, and SA and Decrease ABA. |
|
|
Phialophora sp. |
Festucae latior
(Meadow
fescue) |
Malinowski et al. (1997a) |
Increase chlorophyll content, GSH, SA and Decrease
leaf area, CAT, ABA, JA. |
|
Phoma glomerata |
Oryza sativa (Rice) |
Waqas et al. (2012) |
Increase chlorophyll content, GSH and SA
and Decrease leaf area, CAT, ABA and JA. |
|
Phoma spp. |
Helianthus annuus |
Seema et al. (2019) |
Enhance the extent of usage of organic
compounds by the plants available in the soil, Increase ammonium in soil. |
|
Piriformospora indica |
Arabidopsis |
Sherameti et al. (2008) |
Increase chlorophyll content, Fv/Fm and
fresh weight |
|
|
Eleusine coracana (Finger millet) |
Tyagi et al. (2017) |
Increase chlorophyll, RWC and
proline content. |
|
|
Triticum aestivum (Wheat) |
Hosseini et al. (2017) |
Adjusts plant
metabolites and proteome, redistributes resources in the host, maintains
aquaporin water channels, modulates proteins involved in autophagy. |
|
|
Zea mays |
Xu et al. (2017) |
Increase shoot and root growth CAT, superoxide
dismutases proline and upregulate drought-related genes DREB2A, CBL1,
ANAC072, and RD29A. Decrease malondialdehyde (MDA) |
|
|
Hordeum vulgare |
Ghaffari et al. (2019) |
Reprograms
metabolites and proteomes |
|
Sarocladium implicatum |
Brachiaria spp. |
Odokonyero et al. (2016) |
Increase RWC; decrease shoot and root
biomass |
|
Trichoderma hamatum |
Theobroma cacao (cacao) |
Bae et al. (2009) |
Increase total biomass, shoot and root
biomass, decrease ASP, Glu, GABA. |
|
T. atroviride |
Zea mays (Maize) |
Guler et al. (2016) |
Increase total Chlorophyll, carotenoid,
Fv/Fm, RWC, shoot and root fresh weight, shoot and root length, SOD, CAT, APX
and GR activity and decrease H2O2,
MDA, |
|
T. harzianum |
Oryza sativa (Rice) |
Pandey et al. (2016) |
Increase chlorophyll, total dry matter and
SOD and decrease MDA and proline. |
|
Solanum lycopersicum (Tomato) |
Mastouri et al. (2012) |
Increase chlorophyll, seed germination,
shoot and root dry matter. |
|
|
Triticum aestivum (Wheat) |
Donoso et al. (2008) |
Increase biomass
dry weight, |
|
|
Talaromyces omanensis |
Solanum lycopersicum (Tomato) |
Halo et al. (2020) |
Improve reproductive characteristics,
chlorophyll fluorescence, increase phloem and cortex width, reduce pith
autolysis, increase shoot dry weight, root length, the number of flowers,
fruit weight and GA3 level. |
|
Uncultured Cladosporium, P. glabrum,
P. brevicompactum, Lophiostoma corticola, Uncultured
Metarhizium |
Hordeum vulgare (Barley) |
Murphy et al. (2015) |
Increase number of tillers, shoot dry
weight, decrease root dry weight. |
|
Penicillium citrinum, Aurobassium pullunts and Dothideomycetes
spp., individually and in
combination |
Citrus reticulate |
Sadeghi et al. (2020) |
Increase activities of APX, SOD, GR and
levels of ASA and GSH), decrease activities of CAT, monodehydroascorbate
reductase (MDHAR) and dehydroascorbate reductase (DHAR), enhanced ratios of
reduced ascorbate/dehydroascorbic acid (AsA/DHA) and reduced
glutathione/oxidized glutathione (GSH/GSSG). |
|
Unknown ascomycetous fungi |
Triticum aestivum (wheat) |
Hubbard et al. (2014) |
Increase seed germination. |
Table
3: Virus mediated plant drought tolerance
|
Virus |
Plant |
Mechanisms |
References |
|
cucumber mosaic virus (CMV) |
Nicotiana benthamiana |
Increase in several
osmoprotectants and antioxidants |
Xu et al. (2008) |
|
Tobacco mosaic virus |
Nicotiana benthamiana |
Increase in several
osmoprotectants and antioxidants |
Xu et al. (2008) |
|
Tobacco rattle virus (TRV) |
Nicotiana benthamiana |
Increase in several
osmoprotectants and antioxidants |
Xu et al. (2008) |
|
cucumber mosaic virus (CMV) |
beet, cucumber, Chenopodiumam
aranticolor, pepper, squash, Solanum
habrochaites, tomato and watermelon |
Increase in several
osmoprotectants and antioxidants |
Xu et al. (2008) |
|
Yellow tailflower mild mottle virus (YTMMV) |
Nicotiana benthamiana |
increases in plant biomass, RWC, osmolytes, and
antioxidant enzymes. Upregulation of drought-related genes in plants. |
Dastogeer et al. (2018) |
virus (CMV) having very wide host range
(Palukaitis et al. 1992;
Roossinck 2001); or Tobacco mosaic virus (TMV) and Tobacco rattle virus (TRV)
both with intermediate host ranges; or brome mosaic virus (BMV), a virus that
has a very narrow host range (Lane 1981), they survive longer after under water
limiting environments (Xu et al. 2008). Again, rice and tobacco plants
exhibited better tolerance in the drought
when inoculated with BMV and TMV, respectively. Improved drought stress
tolerance was also recorded in few other cultivated and wild crops like beet,
cucumber, Chenopodiumam aranticolor, pepper, squash, Solanum habrochaites (a wild relative of tomato), tomato and
watermelon as a result of inoculation with CMV (Table
3, Xu et al.
2008). Furthermore, beets inoculated with CMV were found tolerated cold treatments, but all uninfected plants died (Xu et
al. 2008). The underlying mechanism for this observation is unknown
for the most part. However, the phenomenon of plant increased drought tolerance
could be explained by the effect of virus on plant morpho-physiological changes.
Many cases virus infection causes plant shorter (Hull
2013) with low water requirement thereby can survive during severe
drought environment. Viral infection can alter tissues water content and cause
the production and movement of metabolic compounds (Hull 2013) helping plant more tolerant to drought. In their study Xu et
al. (2008) found
that CMV augmented the water content and water retention in infected plants
which are indicative of decreased of stomatal opening and reduced transpiration
level in virus affected plants (Lindsey and
Gudauskas 1975; Keller et al. 1989). By metabolite
profiling study Xu and associates (Xu et al. 2008) found high-level salicylic acid and some osmoprotectants
and antioxidants in virus-infected plants causing increased plant adaptation to
stress (Singh and Usha 2003). Moreover, TMV infection radically increased ABA
levels in Nicotiana plants (Whenham
et al. 1986) which is often regarded as
plant adaptation strategy to stress environment, but it is not clear whether
this is a usual response of plant to virus infection.
Plant
viruses can be grouped into two groups
viz. acute or persistent virus based their nature of interaction with host (Roossinck
2010). Majority of the acute viruses cause disease and are well researched because persistent virus does not produce any apparent
symptoms on the host information on this type of viruses is very scanty.
Persistent plant viruses belong to the families Endornaviridae, Chrysoviridae,
Partitiviridae and Totiviridae and contain dsRNA in their genomes
(King et al. 2012). They have also been
reported from some cultivated plants like alfalfa, avocado, beets,
cherry, common bean, fava bean, melon, pepper, rice, and tomato, among others.
No harmful effects have been documented
for persistent viruses except for Vicia faba endornavirus
which has been reported to be related with male sterility. Persistent plant viruses
are very common and have been reported in many important crop species, but information on what role they play in the
host is mostly unknown. The reason might be the absence of an inoculation method
and the problem of producing virus-free lines of the infected plants. Since the
persistent virus cannot move between cells rather they spread during cell
replication; as a result, the classical virus-inoculation methods like
mechanical or graft inoculations are not effective
for their transmission (Valverde and
Navas-Castillo 2013).
Modern
technologies in the recent days and the development of metagenomics reveal the
virus richness in many diverse environments and propose that producing disease
is not the usual lifestyle of viruses and that many are probably benevolent,
and some are clearly beneficial. More and
more research works are needed towards a
revealing the fundamental mechanisms of plant-virus interaction and enhanced
plant tolerance to stress will provide the potential
for agricultural applications and also intuition to the key role of viruses in the adaptation and evolution of their hosts.
This is
particularly important in the recent era
of global climate change when drought is becoming one of the chief limiting
factors for crop production worldwide (Wollenweber et
al. 2005).
Three-Way interaction of
endophyte-virus-plant and plant abiotic stress tolerance
There is an exciting three-way
interaction exists among plant, endophytes and viruses. However, viruses of endophytic fungi have not
been studied very well as
animal or plant viruses,
and therefore our current knowledge of
viruses of endophytes is indeed limited. However, many fungal viruses have been identified since the first mycovirus was discovered by Hollings (1962). Majority of
them possess double-stranded RNA (dsRNA) genomes, but species with ssRNA and
dsDNA genomes also reported. Most mycoviruses belong to families Totiviridae and Partitiviridae and few to the family Hypoviridae (Ghabrial 1998). In nature, however, it’s quite
probable that the occurrence of viruses is very
frequent in endophytes along with in other fungi. Even though a large
number of endophyte viruses possibly thrive in nature, our understanding of
them is just at the beginning stage. From the limited examples currently
available, they are perhaps not very distinct from the mycoviruses present in
other fungi. The review paper of Bao and Roossinck (2013) gives us an excellent
and exhaustive account on the endophyte viruses their putative roles where the argued that viruses
have been
detected from all different kinds of fungal endophytes and their species
richness is probably high in endophytes. In particular, the occurrence of RNA viruses is reasonably
common with fungal endophytes of grasses,
and in several species the prevalence and
abundance of virus are quite high (Herrero et
al. 2009).
Oh and Hillman (1995)
isolated and described a virus from the fungal endophyte Atkinsonella hypoxylon. Later the virus was named as
Atkinsonella hypoxylon virus (AhV) which is the type species of Betapartiti
virus genus under Partitiviridae family (Oh and Hillman 1995). A virus named Curvularia
thermal tolerance virus (CThTV) was detected
in C. protuberata,
an endophyte of panic grass growing in geothermic soils. The virus possesses
two dsRNA segments of about 2.2 and 1.8 kbp. The association of this virus in
endophyte was reported to confer the benefit
to plant growing at high temperatures 65°C (Márquez et
al. 2007).
Although CThTV is the only well-characterised
virus from the genus, viruses are relatively common in Curvularia. In a study two dsRNA elements of 3.4 and 4.5 kbp (Herrero et al. 2009) were described in an isolate of C. inaequalis
from Ammophila arenaria (Marram grass). In another study, Feldman and
associates (2012) surveyed to detect viruses from fungal endophytes from the plants
Tallgrass Prairie National Preserve in Oklahoma and they were able to report 25
sets of viral sequences from 20 fungal strains checked from the ragweed and
dodder pairs. They identified four sets of dsRNA from Curvularia spp. which belong to endornaviruses,
chrysoviruses, and CThTV-like viruses (Feldman et al. 2012). dsRNA elements have also been reported from some very common
plant-associated fungi including Drechslera,
Stemphylium and Alternaria. Seven putative mycoviruses including endorna-, toti-, chryso-, hypo-, and partitivirus were
found in A. alternata strain from tallgrass prairie in
Oklahoma. Again, one putative chrysovirus
dsRNAs in Stemphylium solani and A. alternata, one partitivirus like sequence were also identified in Cladosporium
(Feldman et al. 2012). Study Report claims that the endophytic fungus Fusarium culmorum
enhance the salt stress tolerance of its host plant, coastal dunegrass (Rodriguez et
al. 2008).
Later, more than one virus like sequence has been
found in the salt-adapted F. culmorum, but
the roles remain unknown. Besides, two dsRNA elements of 3 and 4.4 kbp were
reported in other isolates of F. culmorum (Herrero et
al. 2009).
Among different kind of fungal endophytes,
the dark septate endophytes have been least
studied and characterised and our knowledge is very limited about mycoviruses association with them. Certain viral
agents were found in Phialophora spp., some of them have dsRNA segments similar to that
of P. graminicola, however,
serological similarity have not been detected (Buck et
al. 1997). Herrero et al. (2009) reported a 2.6 kbp dsRNA in G. graminis fungal endophytes
collected perennial grass Holcuslanatus.
The interaction among
endophyte, viruses and their host plants are parallel to plant-endophyte
interactions. Most of the viruses that have been
identified from fungi have limited host ranges and cause no apparent
symptoms unlike those infect plant or animal hosts (Ghabrial 1998). Only a small number of mycoviruses have been
reported to affect their hosts, causing hypovirulence, disease (Deng et al. 2007) or being beneficial. The most noticeable benefit
that endophytic virus confers to plant is
that the presence of virus in the endophyte increase the abiotic stress
tolerance in plant. For example, a virus-infected endophyte was reported to
increase heat tolerance to tomato plants (Márquez et
al. 2007).
Bao and
Roossinck (2013) suggested from their
survey that the presence of dsRNAs in fungi could be as high as 100% and there
are even variations among fungal populations of the same species. However,
Average virus incidence in endophyte populations is 10%, and they are
probably not host specific (Feldman et
al. 2012) and
out of which only a handful of endophyte viruses have been detected and their putative roles have been explored in
symbiotic systems. Many factors can be
attributed that may affect the occurrence of virus in endophytes in a
plant host, including the rate of vertical transmission (through spores), horizontal transmission, fungus-virus
interaction, and environmental conditions (Bao and Roossinck 2013). It is also urged that the some viruses could be readily lost in the culture
which is the reason for very low result
in the survey. Although it is very difficult
to trace any beneficial or harmful effect that mycoviruses may confer upon the
host, it is assumed that they have some effects that are very subtle and
challenging to demonstrate experimentally with lower sample number (Diepeningen et al. 2006). Till date, only a very few attributes have been evaluated in most experiment, for example
growth parameter, reproduction ability, pathogenic effects, or heat resistance.
However, viruses could be a vital genetic
element for fungi and plant hosts, especially under inhospitable environments,
where viruses can confer supportive genetic information through epigenesis.
Fig. 2:
Schematic representation of fungi and virus mediated drought tolerance in
plants
The mechanism by which the endophyte virus has developed to
defend the fungus from the deadly costs of heat, salt and water stress is not
understood well. Further research is needed to display how the viral factors
might influence the genetic and phenetic expression profiles of the endophyte
host that benefit stress adaptation in plants (Bao and Roossinck 2013). The knowledge of endophyte
viruses and their potential functions will be useful for sustainable
agriculture particularly in the context of climate changes in the global arena. With
greater knowledge of endophyte viruses, it will be important to ponder on some
pertinent questions inorder to apply an endophyte in the sustainable
agricultural system. For example (1) Are there any roles of virus(es) in
enabling the endophyte to offer habitat-adapted benefits to host? (2) Is
presence or absence of virus in endophyte alter its relationship with plant
host from mutualistic to antagonistic? (3) Is there any threat that these
viruses could be parasitic on plants by evolution? (4) Could there be any
synthesis of unexpected or expected by-products in the plant–endophyte, or
plant-endophyte-virus interactions? (5) How easier and stable it will be to
deliver endophyte and/or its virus in the farming system (Bao and Roossinck 2013)? Current research trend envision that more mutualistic endophyte
viruses will be reported and their
functions will be investigated in the
future.
Mechanisms of endophyte and virus-mediated plant drought tolerance
It is now well-documented that some fungal endophytes provide fitness
benefit to plants under drought conditions. There are
few excellent reviews on the mechanisms of how fungal
endophytes mediate drought tolerance in the plant (Singh et al. 2011;
Dastogeer and Wylie 2017) therefore; the current review will not discuss this
at length. Endophyte employ complex mechanisms that involve various metabolites
and metabolic pathways to improve plant stress tolerance (Fig. 2). Although,
many investigations found the role endophytic fungi to confer water limitation
tolerance in host, the underlying mechanism(s) are poorly understood. Available
literatures suggest that fungal endophytes improve plant drought tolerance
through- (a) increase in plant growth and development (Khan et al. 2012,
2014; Azad and Kaminskyj 2016; Dastogeer et al. 2017a, b; Dastogeer et
al. 2018) (b) improvement of osmotic balance (Sun et al. 2010; Azad
and Kaminskyj 2016) (c) increase in gaseous exchange and water-use efficiency
(Bayat et al. 2009; Nagabhyru et al. 2013; Cong et al.
2015) and (d) improvement in plant defence against oxidative damage to reduce,
alleviate and mitigate the harmful effects of drought in fungal inoculated
plants balance (Sun et al. 2010; Azad and Kaminskyj 2016).
From the limited studies available so far, it is
unclear how virus infection improves plant drought tolerance. But, commonly,
virus infection causes a reduction in plant growth and plant become dwarf (Hull
2013) thus reduces the water requirement and give plant more advantage under
low water condition. Other physiological changes, for example, reduced water
content and changes in metabolites are also associated with plant virus
infection (Hull 2013). The drought tolerance in the plant due to infection of
CMV (cucumber mosaic virus) and YTMMV (Yellowtail flower mild motile virus)
also correlated with the leaf water content of the plant (Xu et al.
2008; Dastogeer et al. 2018). Higher water retention in virus-infected
plants could be linked to the reduction of stomatal opening and reduced
transpiration rate (Hall and Loomis 1972; Lindsey and Gudauskas 1975; Keller et
al. 1989). The virus-infected plant usually shows higher levels sugars such
as glucose, fructose and sucrose, which may act as osmoprotectant under stress
as compared to non-infected plants (Fig. 2). An in-depth analysis of
metabolites profiling will provide a better understanding in this regard.
Certain osmolytes and antioxidant enzymes and salicylic acid showed higher
accumulation in virus-infected plants under drought (Xu et al. 2008;
Dastogeer et al. 2018). Role of salicylic acid in improving plant
tolerance to abiotic stress is known (Singh and Usha 2003). Alteration in
metabolite accumulation under stress is considered as one of the vital survival
mechanisms of the plant. Metabolic compounds play a role in osmotic adjustment,
membranes stability, and protect cellular organelles damage due to stress (Hare
et al. 1998). Higher accumulation of these protective compounds in
virus-infected plants makes the plant make the plants more acclimatized for
further stress. Changes in gene expressions associated with the virus-mediated
plant drought tolerance reflect the physiological changes as described above.
Biotic and abiotic stress share some common mechanisms in the plant (Xiong and
Yang 2003; Chini et al. 2004; Dastogeer et al. 2018).
Future perspective and challenges
Although there has been continuous advancement, there are still many
challenges which need to be addressed to identify and successfully apply
microorganisms. For example, screening a large number of fungal endophytes that
are isolated from various plants for their roles as plant drought-tolerant is
very time consuming and the results obtained are dependent on the screening
methods used. Dastogeer et al. (2017b) suggested a simple and rapid
screening method, however, in this method; there is no description of the use
of mix inoculum which is currently getting more attention by the researcher.
One possible modification of this method of the filter paper trial would be to
use fungal culture filtrate/ mycelial suspension instead of agar block to
inoculate fungi so mix inocula could also be added. Further, the response of
early-stage seedling may not be the response of the adult plant. So, the
experimenter needs to design trial, including the plant at a different time of
life cycle.
A pertinent question regarding the application of
microbes in the field would be how stable these effects across variable biotic
and abiotic conditions are. Also, since most of the studies on plant-endophyte
interactions have been conducted under in vitro system or under glasshouse
trial which although essential to know the effects primarily and to narrow down
the problems targeted. However, these controlled trials do not necessarily
reflect the outcome under field condition, which is highly variable due to the involvement
of many known and unknown factors. So, it is important to carry out field-based
trials in addition to finding new promising microbial isolates. Again,
different inoculation methods give variable results. For example, seed and
foliar inoculation is more effective compared to soil and root inoculation
methods. The reason could be the presence of resident microbial diversity in
the soil is overall more, which may create a competitive environment for the
inoculated strains. Although various trials have been performed using
endophytes (fungi and/or bacteria) as biocontrol of plant diseases, there is a
lack of field-trial information on endophyte mediated plant drought tolerance.
Unless sufficient information is available and the outcomes are known, the
inclusion of the microbial strains in the integrated package for abiotic stress
management is not advisable. Another promising area is the inoculation of
beneficial microbes in the consortium. In some cases, especially in case of
beneficial bacteria, the application of microbial consortia gave better results
compared to individual strains. Efforts have also been made to improve fungi
efficacy through genetic engineering but with low success rate. Current genome
editing technology such as CRISPR technology might be an important tool in
manipulating the genetics of endophytes.
The implementation of endophytes or beneficial viruses
into plant stress management program will require a thorough understanding of
the mechanisms and the ecology of plant-microbe interactions. Although several
studies suggested morphological, physiological and molecular mechanisms, more
in-depth studies are needed, which include different beneficial strains with
different plant species. The level of gene(s) expression in plants as well as
in microbe(s) by using proteomics would be a crucial step to discern the
mechanisms. It would allow differential expression of genes under different
conditions, detection of microbe- and host gene expression simultaneously, and
the identification of new RNA species. Also, the metabolomic approach, in
addition to genomic and transcriptomic approach, would give an improved
knowledge of the plant-microbe interaction under drought stress (Kaul et al.
2016; Levy et al. 2018). It essential to develop models that reveal the
genetic and metabolic potential, as well as the organisms’ ecology and
evolution, the complex plant-microbe interactions in order understand their
respective roles and utilize this efficiently and sustainably in crop
production under stress.
Unravelling the mechanisms of endophyte and virus-mediated enhanced
abiotic stress in the plant provides insight into the significant role of
microbes in the ecology and evolution of the hosts. In the crop field, a delay
in the appearance of stress related symptoms of even for a short time can be
crucial. Hence, a better understanding of the mechanistic aspect has the
potential implications in agriculture, which are of significant concern during
climate change, since the impact of the drought is becoming more severe in crop
cultivation worldwide (Wollenweber et al. 2005).
Conclusion
One
of the approaches to address the drought problem in crop production is the
application of stress-tolerant microbes that may enhance plant growth under
stress condition. Various studies demonstrated beneficial effects of the
endophytic fungi on plant growth and adaptability to drought stress. This
review accumulated the available literature that investigated the fungal
endophyte or viruses help plants tolerate to drought stress. Our current
understanding of fungal mediated stress tolerance is improving, but
virus-mediated stress tolerance is lagging behind, which warrant further
studies. The mechanisms suggested from the current literatures provide an
incomplete picture of more elaborate, complex and intriguing mechanisms
underlying fungus or virus-mediated drought tolerance. The present review shows
that in addition to other microbes, some viruses could also play a vital role
as an ecological engineer to tackle stress related anomalies in nature. Another
important aspect in this area is that majority of the investigations have been
performed either in in vitro or in a greenhouse or growth chamber and
very few under real field conditions. Therefore, to facilitate the widespread
and resilient use of beneficial microbes, research should also give trial under
field conditions and make farmers aware of microbe-mediated plant stress
tolerance. In addition to use of single strain inoculum, application of
inoculum consortium with same species or other species or other groups of
microbes such as fungi-virus, fungi-bacteria or other possible combination is
advocated because in in nature microbes’ lives in association with various
community members.
Author Contributions
KMGD conceived the idea, did
literature reviews and wrote the first draft. All other authors (AC, MSAS and
MAA) revised the manuscript substantially and modified the tables and figure.
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