Microbe-Mediated Mitigation of Abiotic Stresses

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This entry is adapted from the peer-reviewed paper 10.3390/agronomy12092069

Abiotic stresses are the most significant factors reducing agricultural productivity. Plants face extreme environmental conditions that may affect their biological mechanisms, thereby influencing their growth and development. Microorganisms possess substantial metabolites that aid in helping plants mitigate abiotic stresses. Plants’ interaction with microbes constitutes a diversified ecosystem, as sometimes both the partners share a mutualistic relationship. Endophytes, plant-growth-promoting rhizobacteria (PGPRs), and arbuscular mycorrhizal fungi (AMFs) are examples of microorganisms that play an essential role in alleviating abiotic stresses and, hence, improving plant growth. The plant–microbe interaction leads to the modulation of complex mechanisms in the plant cellular system.

arbuscular mycorrhizal fungi (AMFs) abiotic stresses endophytes microbiomes mutualistic relationship plant cellular system plant-growth-promoting rhizobacteria (PGPRs) plant–microbe interaction biochar

1. Introduction

In the current century, the availability of sufficient food is a major problem due to the growing population and fewer food-production resources ^[1]. Decreased area of arable farmlands is one of the major reasons for the food shortage. Various human activities; degradation of soil; deforestation; and multiple environmental factors, such as flooding, salinity, extreme temperature, and heavy metal stress, are the main reasons for decreased fertile lands ^[2]. Somehow, plants have adapted various traits according to their surrounding environment, while some plants increased the production of osmolytes and scavenging of ROS ^[3]. In the last few decades, some modern plant biotechnology techniques have been used extensively to modify plants with desired adaptations such as resistance to phytopathogens, tolerance against stressful conditions, and enhanced nutritional values. These techniques include conventional breeding and genetic engineering, which are used to transfer desirable traits from one plant to another ^[4].

It is estimated that by the year 2050, crop productivity should be increased from 60 to 100% to meet the anticipated global population (9.7 billion). The current agricultural practices and climate-change situation do not favor the achievement of this target ^[5]. Particularly, the use of infertile land is a major challenge. The increase of crop productivity by using infertile lands is challenging. To enhance crop yield, some farmers apply chemical fertilizers which are not suitable for soil health or for the food chain. Another disadvantage of using chemical fertilizers is that they are more expensive and damage plant health, as well ^[6].

Soil salinity incurs a decrease in the plants’ growth and yield. Usually, the soil salinity is increased by using saline water and different manures ^[7]. The lower productivity in agricultural lands also affects agribusinesses. According to the FAO, more than 20% of the lands are affected by salinity ^[8]. Soil salinity causes sodium aggregation, which promotes chlorosis and changes in ion stability, which ultimately results in yield loss, as well as a reduction in the nitrogen content in plants. The salinity in the roots’ area may decrease the weight of plant parts ^[9]. The rhizosphere is the root zone of a plant where rhizobacteria reside. These rhizobacteria are vital for the maintenance of soil health ^[10]. The inoculation of plants with 3–5% rhizobacteria enhances plant growth. Thus, they are named plant-growth-promoting rhizobacteria. These rhizobacteria include a diversity of microbes that have the potential to increase plant growth and yield ^[11].

Although some microorganisms are considered harmful to plants due to their disease-causing properties ^[12], most soil microorganisms help plants to survive stressful conditions. These microorganisms are now being used in agriculture to produce food crops. Several microorganisms play a significant role in the fixation of atmospheric nitrogen; organic wastes; pesticide detoxification; mitigation of plant disease; and production of bioactive compounds, such as vitamins, hormones, and enzymes ^[13].

Plant-growth-promoting rhizobacteria (PGPRs) and plant-growth-promoting fungi (PGPFs) are examples of some microorganisms that help to mitigate abiotic stress ^[14]. Beneficial microorganisms mitigate abiotic stress by adapting various strategies such as phytohormone production, lowering ethylene oxide levels, upregulation of dehydration response, and the induction of genes encoding antioxidant genes. Bacteria that reside in the plant’s root usually secrete phytohormones that mitigate the salinity and decrease seedling growth ^[15]. It has been observed that plant-growth-promoting bacteria such as Pseudomonas sp. and Bacillus promote plant growth under stressed conditions by the secretion of indole acetic acid and siderophores. The lowered ethylene level helps plant roots grow, ultimately leading to a healthy plant ^[16].

Some studies revealed that the enhanced growth of plants under abiotic stress by microorganisms is due to the activation of primary metabolisms, leading to increased plant growth, improved photosynthesis, better uptake of nutrients, and higher antioxidant enzymes activity. Moreover, some secondary metabolites also help in tolerating abiotic stress, such as flavonoids, phytoalexins, phenyl-propranoids, and carotenoids ^[17]. Both fungal and bacterial species help to enhance the production of secondary metabolites under abiotic stress ^[18].

The use of PGPRs from manures is also a promising approach to decrease the negative effects of abiotic stress. PGPRs aid in the growth of the plant and the removal of heavy metals and to overcome the negative effects of pesticides. Thus, they lead to the bioremediation of polluted soils ^[19].

It is assumed that crop productivity can be enhanced by using various modern strategies, including the use of beneficial microorganisms. These microorganisms have the potential to increase crop productivity through the stimulation of phytohormones, nitrogen fixation, and resistance against abiotic and biotic stress. By the detailed study and research on these microorganisms, one can make suitable microbial formulation or consortia that can help a plant to increase its productivity at a low cost ^[20].

2. Microbiome and Stresses

Plant metabolism is highly affected by biotic, as well as abiotic, stresses. These stresses also have a significant effect on the composition of root exudates. Field-grown plants are highly exposed to environmental stresses. Biotic stress factors are extremely harmful to plant growth and development. These factors include pathogenic fungi, bacteria, viruses, nematodes, and insects, while abiotic stress factors include temperature, drought, waterlogging, salinity, toxic organic compounds, and metal salts. These abiotic stresses also have negative effects on plant growth. There is a high chance that plants may encounter various environmental stresses at the same time. Contrarily, much rhizospheric microbiota protect plants from massive environmental stresses. The selection of plant-growth-promoting bacteria (PGPBs) depends on the range of environmental stresses. It has been observed that PGPBs play a significant role in the growth and development of plants. Under biotic and abiotic stresses, the synthesis of phytohormones such as ethylene can vary under moderate environmental stresses. In response to ethylene production, plant defensive genes are expressed to protect plants from environmental stresses. A high concentration of ethylene in plants may lead to plant senescence, chlorosis, and abscission ^[21]. Biotic stresses often alter the composition of microbial communities associated with the stress plants. It has been reported that, in the diseased cotton plant of Verticillium, the number of beneficial bacteria and arbuscular mycorrhizal fungi decreased, while plant pathogenic fungi increased. The relationship between the soil microbiome and the strawberry plant’s resistance against Verticillium dahlia and Macrophomina phaseolina has been observed. In another experiment, an alteration in the root exudate was observed due to the aphid infestation in the pepper plant. This phenomenon leads to the decreased resistance of pepper plants to aphids due to plant-recruiting rhizobacteria ^[22]. In another study, it has been observed that compost has a significant effect on tomato plant growth and can also aid in fighting the diseases caused by Fusarium oxysporium and Verticillium dahlia. The added compost also helped to decrease the disease intensity caused by these pathogens. Thus, it was concluded that fungal pathogens may alter the composition of plant microbiomes, and added compost may overcome the negative effects ^[23].

Many abiotic factors, such as drought and salinity, inhibit the crop yield and have negative effects on the crop microbiome. In yet another study, a significant difference was observed between dry-wheat land and irrigated crops. Later, it was noted that the density of the rhizosphere microbiome increases in irrigated crops ^[24]. Thus, it can be concluded that, for the maintenance of a healthy rhizosphere microbiome, an adequate amount of water is necessary. An improvement in a drought-ridden cotton plant through a beneficial microbiome has also been observed. It was observed that the development of the sorghum root microbiome has been delayed due to drought stress. The drought stress leads to the abundance of bacteria within the microbiome. Climate change, including extreme temperatures, may affect the phyllosphere and rhizosphere microbiome of many plants. The soil microbiome is also affected by the low nitrogen and carbon levels. Devastating changes in soil pH and C:N ratios can alter the composition of the microbiome ^[25].

3. Plant Microbiome

To understand the defense mechanism in plants, one needs to study the plant–pathogen interaction. Many microbial communities and microbes have beneficial effects on their host plant. These microbes benefit the plants by improving nutrient acquisition and growth; providing resistance against pathogens; and y enhancing resistance against abiotic stresses, such as heat, drought, soil salinity, and many others. Somehow, beneficial microbes are often specific to a species cultivar. It was observed that few plant signals that trigger plant immune response can distinguish between pathogenic and beneficial microbes. However, it is still unclear which factors help a plant distinguish between beneficial and pathogenic microbes ^[26]. Naturally, a plant’s habitat is a conducive environment for several microbes, including bacteria, oomycetes, fungi, archaea, and even pathogenic microbes. Plant microbiota composition is shaped by the complex multilateral interaction among microbes. Microbes exhibit commensal, pathogenic, and mutualistic relations with their host plants. The microbiome profiling of plants and looking at root-associated soils revealed the dynamic and diverse range of microbiomes. Many environmental factors (soil type, daylight, and season) and host factors (species and developmental stage) may affect the shape of bacterial communities. Soil and air act as physical barriers for plant-associated microbiomes ^[27]. The phyllosphere is the aerial part of the plant and is a suitable habitat for microbes. The phyllospheric microbiome greatly affects the performance of the plant. These microbes also help to remove contaminants from plants. They also help to maintain plant health and suppress the growth of plant pathogens. The microbiota of plant parts that are far from the soil or in other aerial parts of plants are highly affected by the long-distance transport process. Highly beneficial and functionally significant microbes are found belowground. At the early stages of growth, microbial communities above the ground are highly influenced by the soil. Microbial communities are found abundantly in soil, with lower amounts in the rhizosphere portion and a more decreased proportion in the endophytic compartment. Four bacterial phyla were found to dominate around the rhizosphere and endosphere of plants: Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria ^[28]. Members of bacterial communities have a strong influence on each other, as they can have antagonistic, mutualistic, and competitive interactions. Mostly, microbes interact by engaging in nutritional competition, exchange, and interdependence relations. The endosphere compartment of the plant has lower microbial diversity than rhizosphere. The microbial community of the root endosphere is more abundant than in the leaves. However, it is also known that entophytic microbes also play a significant role in plant development ^[29]. The effect of the root bacterial microbiome on maize, barley, and Arabidopsis thaliana in soil has been studied ^[30]. Peiffer et al. ^[31] observed that approximately 5–7% of the microbiome genotypes differ from the host genotype. These differences were mostly related to the quantitative nature, at a large scale, when maize rhizosphere microbiomes were studied. The microbiome was sampled during the growing season and then replicated after 5 years, showing that the root-associated microbiota was not changed. Only 143 operational taxonomic units (OTUs) were identified that correlated to the plant genotype ^[32]. About 200 naturally occurring Arabidopsis thaliana accessions have been screened in a single member of the rhizosphere community. Those accessions that were selected have been planted in natural soils; two of them could inhibit the growth of Pseudomonadaceae. Thus, it can be concluded that even a single cultivar is enough to affect the structure of microbial communities. The rhizosphere is a significant zone between the plant’s root and soil microbiomes. The rhizosphere provides a suitable environment for both plant and microbial growth. The assemblage of microbiomes in the rhizosphere mostly depends on plant-derived metabolites ^[33].

4. Microbe-Mediated Mitigation of Abiotic Stresses

For the survival of a plant in an environment with abiotic stress, one of the key adaptations is microbial interaction with the plant. Microbe-mediated induction of abiotic stress response is termed Induced Systemic Tolerance (IST). The microbiome helps plants mitigate abiotic stress by using their metabolic and genetic capabilities ^[34]. It was observed that the most significant rhizospheric occupants that aid in the mitigation of various abiotic stresses in plants belong to the genera Pseudomonas ^[35], Azotobacter ^[36], Azospirillium ^[37], Rhizobium, Pantoea, Bacillus, Enterobacter ^[35], Bradyrhizobium ^[38], Methylobacterium ^[39], Burkholderia ^[40], and Trichoderma ^[40] and the group cyanobacteria ^[41]. To overcome crop productivity limitations, one of the viable methods is the selection, screening, and application of stress-tolerant microorganisms. Trichoderma species have been thoroughly investigated in this regard. In one of the studies, Trichoderma harzianum was used for the alleviation of stress in rice by upregulating aquaporin, dehydrin, and malonialdehyde ^[42]. T. harzianum was also employed for the enhanced production of oil from NaCl-affected Indian mustard (Brassica juncea). This, as shown in the results, also improved the nutrient uptake, enhanced the accumulation of antioxidants, and lowered the Na⁺ uptake ^[43]. Brotman et al. ^[44] demonstrated that mutant Trichoderma can mitigate salinity stress by the production of ACC-deaminase. In barley and oats, the production of IAA and ACC-deaminase seemed to be enhanced by the use of Pseudomonas sp. and Acinetobacter sp. ^[45]. Simmons et al. ^[46] used Streptomyces sp. for the alleviation of salt stress and growth enhancement in the Micro-Tom tomato plant. Meanwhile, in maize and wheat, drought stress was ameliorated by using the strain Burkholderia phytofirmans PsJN ^[47]. Alteration in the levels of phytohormones, defense-related protein, enzymes, antioxidants, and epoxypolysaccharides is identified as Rhizobacteria-induced drought endurance and resilience (RIDER). These alterations make plants more resistant toward abiotic stresses ^[48].

The soil microenvironment of the root region contains many microbes, as it harbors a diversity of nutrients, minerals, and metabolites. Substances secreted by a plant root significantly affect microbial colonization within the rhizosphere. Microorganisms move toward the root exudates by chemotactic movement. This movement acts as a dragging force for the colonization of microbial communities around the roots. PGPRs function as biofertilizers, phytostimulators, and biocontrol agents while harnessing the benefits of the rhizosphere/microenvironment. PGPRs depend upon their capabilities, interaction mode, and surrounding conditions. Plant growth is stimulated by bacteria through direct, as well as indirect, actions ^[49]. Synthesis of bacterial compounds through the direct method is beneficial for the uptake of essential nutrients and micronutrients from the soil. These bacteria also help produce plant-growth regulators such as IAA, deaminase, and ACC, which help improve plant growth. These growth-promoting compounds enhance the growth and prevent stress ethylene from becoming overly inhibitory to plant growth ^[50]^[51]. Moreover, the microbes help sequestrate iron and zinc, phosphorous and potassium solubilize, atmospheric nitrogen fixation, and plant hormone synthesis. However, on the other hand, the indirect mechanism shows antagonistic activity toward plant pathogenic organisms and the production of antifungal compounds ^[52]. Bacterial metabolites act as extracellular signals to induce systemic resistance. This initiates a series of internal processes. The activation of plant defense mechanisms is triggered by the translocated signal received by distant plant cells. Another significant microbiome that acts as a plant-growth promoter is fungi, particularly mycorrhiza, either mycorrhizal fungi or vesicular-arbuscular mycorrhizal (VAM) fungi. These fungi form endosymbiotic associations with plants. Their hyphae form complex networking; thus, nutrient uptake by roots increases.

Salt tolerance in barley and drought tolerance in Chinese cabbage were found to be induced by the root fungal endophyte identified as Piriformospora indica ^[53]. Microbes help plants maintain their growth and development, even under abiotic stress, and they also aid in the production of nutrients, hormones, and organic phytostimulant compounds. These actions of microbiomes make them strong and viable to fight against abiotic stress for plants. Various studies were carried out that elaborate on the role of microbiomes in the mitigation of abiotic stress for crop plants. Some soil-inhabiting microbes, such as Achromobacter, Azospirillum, Variovorax, Bacillus, Enterobacter, Azotobacter, Aeromonas, Klebsiella, and Pseudomonas, help to enhance plant growth even under undesirable environmental conditions ^[48]. Such soil bacteria that help plants to grow under abiotic stress have been classified as plant-growth promoters (PGP). Indole acetic acid (IAA) synthesized in plant shoots acts as plant-growth-regulating molecules. Auxins and IAA perform as a growth-stimulating effect, resulting in root-growth initiation, while a higher concentration of auxin negatively affects plant root growth ^[35]. Table 1 presents a list of microbes and tolerance strategies used to control abiotic stress in plants. It was observed from recent studies that PGPRs not only help in the alleviation of abiotic stresses but also increase the plant crop yield of several crops, including rice, maize, barley, and soybean ^[54].

Table 1. Various tolerance strategies used to control abiotic stress in plants.

Plants	Abiotic Stress	Microbial Inoculation	Tolerance Method	References
Arabidopsis thaliana	Salt	Bacillus subtilis GB03	Tissue-specific regulation of sodium transporter HKT1.	^[55]
Glycine max	Salt	Pseudomonas simiae	4-nitroguaiacol and quinolone promote soybean-seed germination.	^[56]
Oryza sativa	Salt	Root-associated growth-promoting rhizobacteria	Expression of salt-stress-related RAB18 plant gene.	^[57]
Oryza sativa, Triticum aestivum, Zea mays, Gossypium hirsutum	Salt	Cyanobacteria and cyanobacterial extracts	Phytohormones as elicitor molecule.	^[58]
Zea mays	Osmotic stress	Bacillus megaterium	High hydraulic conductance and increased root expression and ZmPIP isoforms.	^[59]
Vitis vinifera, Capsicum annuum	Salt	Burkholderia, Arthrobacter Bacillus	Increased accumulation of proline.	^[60]
Capsicum annuum	Salinity	Azospirillum brasilense and Pantoea dispersa (Co-inoculation)	High stomatal conductance and Photosynthesis.	^[61]
Arabidopsis	Salinity	Bacillus subtilis	Decreased root transcriptional expression of a high-affinity K⁺ transporter (AtHKT1) decreasing root Na⁺ import.	^[55]
Phaseolus vulgaris	Salinity	Azospirillum brasilense strain Cd	Stimulation of persistent exudation of flavonoids.	^[62]
Zea mays	Drought	Burkholderia phytofirmans Enterobacter sp. FD17	Increased photosynthesis, root and shoot biomass under drought conditions.	^[63]
Arabidopsis thaliana	Drought	Pseudomonas chlororaphis O6	Production of 2R,3R butanediol- a volatile compound.	^[64]
Triticum aestivum	Heat	Bacillus amyloliquefaciens, Azospirillum brasilence	Reduced regeneration of reactive oxygen species, pre-activation of heat shock transcription factors, and changes in metabolome.	^[65]
Brassica juncea	Arsenic toxicity	Staphylococcus arlettae	Increased dehydrogenase, phosphatase, and available phosphorus in soil.	^[66]
Triticum aestivum	Zn toxicity	Pseudomonas aeruginosa	Improved biomass, N and P uptake, and soluble protein.	^[67]
Phragmites australis	Hg toxicity	Photobacterium spp.	IAA and mercury reductase activity.	^[68]
Miscanthus sinensis	Cd, AS, Cu, Pb and Zn toxicity	Pseudomonas koreensis AGB-1	ACC deaminase and IAA production.	^[69]

4.1. Mechanisms of PGPRs

The changes in the rhizosphere microbial community may cause plant-growth promotion by PGPRs ^[70]. PGPRs use both direct and indirect modes of action for plant growth. Some PGPRs are strains of Bacillus, Rhizobium, Acinetobacter, Alcaligenes, Azotobacter, Arthrobacter, Enterobacter, Pseudomonas, Serratia, and Burkholderia. In the direct mode of action, PGPRs include atmospheric nitrogen fixation, the production of phytohormones and enzymes in plants. Meanwhile, siderophores’ production, antibiotics’ production, and enzymes’ release (e.g., chitinase) are among the mechanisms of the indirect mode of action ^[71].

4.2. Direct Mechanisms

In direct mechanisms, PGPRs help to promote plant growth in the absence of the pathogen. Rhizospheric microbial activity also affects the rooting and nutrient-availability pattern. Some direct mechanisms of PGPRs for plant growth are discussed hereunder.

Nitrogen fixation—The plant growth and productivity depend on the availability of vital nutrients such as nitrogen (N₂). Nitrogen-fixing microorganisms play an important role in biological nitrogen fixation under mild temperatures ^[72]. Nitrogen-fixing organisms are classified into symbiotic and non-symbiotic N₂-fixing bacteria. Symbiotic N₂-fixing bacteria include leguminous and non-leguminous plants such as rhizobia and Frankia. Meanwhile, non-N₂-fixing bacteria refer to cyanobacteria such as Nostoc, Azotobacter, and Azocarus ^[73]. The symbiosis connection may lead to the production of nodules ^[74]. The nitrogen-fixation mechanism is carried out by an enzyme nitrogenase complex. For nitrogen fixation and the regulation of the enzyme, genetic control is present in such bacteria and nitrogenase genes are required. Meanwhile, for the synthesis and regulation of enzymes, regulatory genes are required; nitrogenase genes are also required. Moreover, regulatory genes are required to synthesize and regulate the enzymes. Structural genes are involved in activating Fe protein, iron–molybdenum cofactor biosynthesis, and electron donation ^[75].

Phosphate Solubilization—Under stress conditions, plants usually face a shortage of nutrients such as phosphorous. It is mostly present in the soil in both forms, i.e., organic and inorganic ^[76]. The shortage of phosphorous in plants occurs due to the presence of insoluble P in plants, but plants can only absorb it as monobasic and diabasic ions ^[73]. Phosphate-solubilizing bacteria can work as a source of phosphorous in the form of biofertilizers. Some phosphate-solubilizing bacteria are Azotobacter, Microbacterium, Bacillus, Burkholderia, Enterobacter, Flavbacterium, Erwinia, Rhizobium, and Serratia ^[77]. As plants cannot absorb inorganic P, Rhizobacteria have the potential to solubilize it, thus enhancing plant growth and yield. However, another cause of P solubilization could be due to the synthesis of organic acids by rhizospheric microorganisms ^[78]. In plants such as the potato, tomato, wheat, and radish, phosphorous was solubilized by microbial species such as Azotobacter chroococcum, Enterobacter agglomerans, P. putida, Bradyrhizobium japonicum, Cladosporium herbarum, and Rhizobium leguminosarum ^[79].

Siderophore production—Iron is present abundantly in nature, but it is still unavailable for plants. Mostly, iron is found in the form of Fe³⁺. PGPRs help to solubilize it by the secretion of siderophores, which are low-molecular-weight iron-binding proteins that help in the chelation of ferric iron (Fe³⁺). The bacterial cell membrane dissolves siderophores and Fe³⁺ in a 1:1 complex. This Fe³⁺ is reduced to Fe²⁺ and then released from siderophores to the cell. PGPRs enhance plant growth by releasing siderophores, which also help mitigate various plant diseases. Microbial siderophores act as a metal-chelating agent, which helps to control the iron availability in the rhizosphere ^[80].

Phytohormone production—It is well-known that microbes help in the synthesis of phytohormone auxin, also known as indole-3-acetic acid (IAA). Many microorganisms that are isolated from multiple crops have the ability to synthesize IAA as a secondary metabolite ^[81]. IAA plays a significant role in the interaction of rhizobacteria and plants ^[82]. The synthesis of IAA affects plat cell division and helps to stimulate seed and tuber germination and the formation of adventitious roots. The secretion of bacterial IAA provides higher access for plants to nutrients by increasing their root surface area and length ^[83]. Mostly, Rhizobium species produce IAA, which upregulates cell division and the formation of vascular bundles. Several environmental stress factors, such as an acidic pH, osmotic stress, and carbon limitation, cause the modification of IAA synthesis in bacteria ^[84].

References

Cooper, R.N.; Houghton, J.T.; McCarthy, J.J.; Metz, B. Climate Change 2001: The Scientific Basis. Foreign Aff. 2002, 81, 208.
IPCC. Climate Change 2014 Synthesis Report Summary Chapter for Policymakers; IPCC: Paris, France, 2014; p. 31.
Compant, S.; van der Heijden, M.G.; Sessitsch, A. Climate change effects on beneficial plant–microorganism interactions. Fed. Eur. Microbiol. Soc. 2010, 73, 197–214.
Wadgymar, S.M.; Daws, S.C.; Anderson, J.T. Integrating viability and fecundity selection to illuminate the adaptive nature of genetic clines. Evol. Lett. 2017, 1, 26–39.
Rashid, M.I.; Mujawar, L.H.; Shahzad, T.; Almeelbi, T.; Ismail, I.M.; Oves, M. Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol. Res. 2016, 183, 26–41.
Leifheit, E.; Verbruggen, E.; Rillig, M. Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation. Soil Biol. Biochem. 2015, 81, 323–328.
Compant, S.; Samad, A.; Faist, H.; Sessitsch, A. A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. J. Adv. Res. 2019, 19, 29–37.
Wagner, M.R.; Lundberg, D.S.; Coleman-Derr, D.; Tringe, S.G.; Dangl, J.L.; Mitchell-Olds, T. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild arabidopsis relative. Ecol. Lett. 2014, 17, 717–726.
Gehring, C.A.; Sthultz, C.M.; Flores-Rentería, L.; Whipple, A.V.; Whitham, T.G. Tree genetics defines fungal partner communities that may confer drought tolerance. Proc. Natl. Acad. Sci. USA 2017, 114, 11169–11174.
Calvo, O.C.; Franzaring, J.; Schmid, I.; Müller, M.; Brohon, N.; Fangmeier, A. Atmospheric CO2 enrichment and drought stress modify root exudation of barley. Glob. Chang. Biol. 2017, 23, 1292–1304.
Saleem, M.; Law, A.D.; Sahib, M.R.; Pervaiz, Z.H.; Zhang, Q. Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 2018, 6, 47–51.
Liu, H.; Brettell, L.E.; Qiu, Z.; Singh, B.K. Microbiome-mediated stress resistance in plants. Trends Plant Sci. 2020, 25, 733–743.
Sagar, A.; Rathore, P.; Ramteke, P.W.; Ramakrishna, W.; Reddy, M.S.; Pecoraro, L. Plant growth promoting rhizobacteria, arbuscular mycorrhizal fungi and their synergistic interactions to counteract the negative effects of saline soil on agriculture: Key macromolecules and mechanisms. Microorganisms 2021, 9, 1491.
Evelin, H.; Devi, T.S.; Gupta, S.; Kapoor, R. Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: Current understanding and new challenges. Front. Plant Sci. 2019, 10, 470.
Porcel, R.; Aroca, R.; Azcon, R.; Ruiz-Lozano, J.M. Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 2016, 26, 673–684.
Al-Arjani, A.-B.F.; Hashem, A.; Abd Allah, E.F. Arbuscular mycorrhizal fungi modulates dynamics tolerance expression to mitigate drought stress in Ephedra foliata boiss. Saudi J. Biol. Sci. 2020, 27, 380–394.
Chen, J.; Zhang, H.; Zhang, X.; Tang, M. Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front. Plant Sci. 2017, 2017, 1739.
Li, Z.; Wu, N.; Meng, S.; Wu, F.; Liu, T. Arbuscular mycorrhizal fungi (AMF) enhance the tolerance of Euonymus maackii rupr. At a moderate level of salinity. PLoS ONE 2020, 15, e0231497.
Hartman, K.; Tringe, S.G. Interactions between plants and soil shaping the root microbiome under abiotic stress. Biochem. J. 2019, 476, 2705–2724.
Vandenkoornhuyse, P.; Quaiser, A.; Duhamel, M.; Le Van, A.; Dufresne, A. The importance of the microbiome of the plant holobiont. New Phytol. 2015, 206, 1196–1206.
Pandey, V.; Ansari, M.W.; Tula, S.; Yadav, S.; Sahoo, R.K.; Shukla, N.; Bains, G.; Badal, S.; Chandra, S.; Gaur, A. Dose-dependent response of trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 2016, 243, 1251–1264.
Ahmad, F.; Ahmad, I.; Khan, M.S. Indole acetic acid production by the indigenous isolates of azotobacter and fluorescent pseudomonas in the presence and absence of tryptophan. Turk. J. Biol. 2005, 29, 29–34.
Brotman, Y.; Landau, U.; Cuadros-Inostroza, Á.; Takayuki, T.; Fernie, A.R.; Chet, I.; Viterbo, A.; Willmitzer, L. Trichoderma-plant root colonization: Escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog. 2013, 9, e1003221.
Chang, P.; Gerhardt, K.E.; Huang, X.-D.; Yu, X.-M.; Glick, B.R.; Gerwing, P.D.; Greenberg, B.M. Plant growth-promoting bacteria facilitate the growth of barley and oats in salt-impacted soil: Implications for phytoremediation of saline soils. Int. J. Phytoremediat. 2014, 16, 1133–1147.
Simmons, C.; Reddy, A.; Simmons, B.; Singer, S.; VanderGheynst, J. Effect of inoculum source on the enrichment of microbial communities on two lignocellulosic bioenergy crops under thermophilic and high-solids conditions. J. Appl. Microbiol. 2014, 117, 1025–1034.
Naveed, M.; Hussain, M.B. Zahir a. Zahir, birgit mitter & angela sessitsch. Plant Growth Regul. 2014, 73, 121–131.
Kaushal, M.; Wani, S.P. Plant-growth-promoting rhizobacteria: Drought stress alleviators to ameliorate crop production in drylands. Ann. Microbiol. 2016, 66, 35–42.
Hayat, R.; Ali, S.; Amara, U.; Khalid, R.; Ahmed, I. Soil beneficial bacteria and their role in plant growth promotion: A review. Ann. Microbiol. 2010, 60, 579–598.
Baltruschat, H.; Fodor, J.; Harrach, B.D.; Niemczyk, E.; Barna, B.; Gullner, G.; Janeczko, A.; Kogel, K.H.; Schäfer, P.; Schwarczinger, I. Salt tolerance of barley induced by the root endophyte piriformospora indica is associated with a strong increase in antioxidants. New Phytol. 2008, 180, 501–510.
Suarez, C.; Cardinale, M.; Ratering, S.; Steffens, D.; Jung, S.; Montoya, A.M.Z.; Geissler-Plaum, R.; Schnell, S. Plant growth-promoting effects of hartmannibacter diazotrophicus on summer barley (Hordeum vulgare L.) under salt stress. Appl. Soil Ecol. 2015, 95, 23–30.
Vinayarani, G.; Prakash, H. Growth promoting rhizospheric and endophytic bacteria from Curcuma longa L. as biocontrol agents against rhizome rot and leaf blight diseases. Plant Pathol. J. 2018, 34, 218.
Vandana, U.K.; Rajkumari, J.; Singha, L.P.; Satish, L.; Alavilli, H.; Sudheer, P.D.; Chauhan, S.; Ratnala, R.; Satturu, V.; Mazumder, P.B. The endophytic microbiome as a hotspot of synergistic interactions, with prospects of plant growth promotion. Biology 2021, 10, 101.
Begum, N.; Qin, C.; Ahanger, M.A.; Raza, S.; Khan, M.I.; Ashraf, M.; Ahmed, N.; Zhang, L. Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Front. Plant Sci. 2019, 10, 1068.
Zhang, H.; Kim, M.-S.; Sun, Y.; Dowd, S.E.; Shi, H.; Paré, P.W. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter hkt1. Mol. Plant-Microbe Interact. 2008, 21, 737–744.
Vaishnav, A.; Kumari, S.; Jain, S.; Varma, A.; Tuteja, N.; Choudhary, D.K. Pgpr-mediated expression of salt tolerance gene in soybean through volatiles under sodium nitroprusside. J. Basic Microbiol. 2016, 56, 1274–1288.
Jha, Y.; Sablok, G.; Subbarao, N.; Sudhakar, R.; Fazil, M.T.; Subramanian, R.; Squartini, A.; Kumar, S. Bacterial-induced expression of rab18 protein in orzya sativa salinity stress and insights into molecular interaction with gtp ligand. J. Mol. Recognit. 2014, 27, 521–527.
Singh, S. A review on possible elicitor molecules of cyanobacteria: Their role in improving plant growth and providing tolerance against biotic or abiotic stress. J. Appl. Microbiol. 2014, 117, 1221–1244.
Marulanda, A.; Azcón, R.; Chaumont, F.; Ruiz-Lozano, J.M.; Aroca, R. Regulation of plasma membrane aquaporins by inoculation with a bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 2010, 232, 533–543.
Ait Barka, E.; Nowak, J.; Clément, C. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, burkholderia phytofirmans strain psjn. Appl. Environ. Microbiol. 2006, 72, 7246–7252.
Del Amor, F.M.; Cuadra-Crespo, P. Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct. Plant Biol. 2011, 39, 82–90.
Dardanelli, M.S.; de Cordoba, F.J.F.; Espuny, M.R.; Carvajal, M.A.R.; Díaz, M.E.S.; Serrano, A.M.G.; Okon, Y.; Megías, M. Effect of azospirillum brasilense coinoculated with rhizobium on phaseolus vulgaris flavonoids and nod factor production under salt stress. Soil Biol. Biochem. 2008, 40, 2713–2721.
Naveed, M.; Mitter, B.; Reichenauer, T.G.; Wieczorek, K.; Sessitsch, A. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans psjn and Enterobacter sp. FD17. Environ. Exp. Bot. 2014, 97, 30–39.
Cho, S.M.; Kang, B.R.; Han, S.H.; Anderson, A.J.; Park, J.-Y.; Lee, Y.-H.; Cho, B.H.; Yang, K.-Y.; Ryu, C.-M.; Kim, Y.C. 2r, 3r-butanediol, a bacterial volatile produced by pseudomonas chlororaphis o6, is involved in induction of systemic tolerance to drought in arabidopsis thaliana. Mol. Plant-Microbe Interact. 2008, 21, 1067–1075.
Ahmad, P.; Hashem, A.; el-daim-Allah, E.F.; Alqarawi, A.; John, R.; Egamberdieva, D.; Gucel, S. Role of trichoderma harzianum in mitigating NaCl stress in indian mustard (Brassica juncea L.) through antioxidative defense system. Front. Plant Sci. 2015, 6, 868.
Lu, X.; Jin, C.; Yang, J.; Liu, Q.; Wu, S.; Li, D.; Guan, Y.; Cai, Y. Prenatal and lactational lead exposure enhanced oxidative stress and altered apoptosis status in offspring rats’ hippocampus. Biol. Trace Elem. Res. 2013, 151, 75–84.
Kloepper, J.W.; Schroth, M.N. Relationship of in vitro antibiosis of plant growth promoting rhizobacteria to plant growth and the displacement of root microflora. Phytopathology 1981, 71, 1020–1024.
Islam, F.; Yasmeen, T.; Ali, Q.; Ali, S.; Arif, M.S.; Hussain, S.; Rizvi, H. Influence of pseudomonas aeruginosa as pgpr on oxidative stress tolerance in wheat under zn stress. Ecotoxicol. Environ. Saf. 2014, 104, 285–293.
Raymond, J.; Siefert, J.L.; Staples, C.R.; Blankenship, R.E. The natural history of nitrogen fixation. Mol. Biol. Evol. 2004, 21, 541–554.
Bhattacharyya, P.N.; Jha, D.K. Plant growth-promoting rhizobacteria (pgpr): Emergence in agriculture. World J. Microbiol. Biotechnol. 2012, 28, 1327–1350.
Giordano, W.; Hirsch, A.M. The expression of maexp1, a melilotus alba expansin gene, is upregulated during the sweetclover-sinorhizobium meliloti interaction. Mol. Plant-Microbe Interact. 2004, 17, 613–622.
Bruto, M.; Prigent-Combaret, C.; Muller, D.; Moënne-Loccoz, Y. Analysis of genes contributing to plant-beneficial functions in plant growth-promoting rhizobacteria and related proteobacteria. Sci. Rep. 2014, 4, 6261.
Xu, Z.Z.; Zhou, G.S. Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass leymus chinensis. Planta 2006, 224, 1080–1090.
Khan, M.S.; Zaidi, A.; Wani, P.A.; Oves, M. Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ. Chem. Lett. 2009, 7, 1–19.
Zaidi, A.; Khan, M.; Ahemad, M.; Oves, M. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung. 2009, 56, 263–284.
Guo, J.K.; Ding, Y.Z.; Feng, R.W.; Wang, R.G.; Xu, Y.M.; Chen, C.; Wei, X.L.; Chen, W.M. Burkholderia metalliresistens sp. Nov. a multiple metal-resistant and phosphate-solubilising species isolated from heavy metal-polluted soil in southeast china. Antonie Van Leeuwenhoek 2015, 107, 1591–1598.
Yadav, J.; Verma, J.P.; Jaiswal, D.K.; Kumar, A. Evaluation of pgpr and different concentration of phosphorus level on plant growth, yield and nutrient content of rice (Oryza sativa). Ecol. Eng. 2014, 62, 123–128.
Ghosh, U.D.; Saha, C.; Maiti, M.; Lahiri, S.; Ghosh, S.; Seal, A.; MitraGhosh, M. Root associated iron oxidizing bacteria increase phosphate nutrition and influence root to shoot partitioning of iron in tolerant plant typha angustifolia. Plant Soil 2014, 381, 279–295.
El-Tarabily, K.A.; ElBaghdady, K.Z.; AlKhajeh, A.S.; Ayyash, M.M.; Aljneibi, R.S.; El-Keblawy, A.; AbuQamar, S.F. Polyamine-producing actinobacteria enhance biomass production and seed yield in Salicornia bigelovii. Biol. Fertil. Soils 2020, 56, 499–519.
Neubauer, U.; Furrer, G.; Schulin, R. Heavy metal sorption on soil minerals affected by the siderophore desferrioxamine b: The role of fe (iii)(hydr) oxides and dissolved fe (iii). Eur. J. Soil Sci. 2002, 53, 45–55.
Mathew, B.T.; Torky, Y.; Amin, A.; Mourad, A.H.; Ayyash, M.M.; El-Keblawy, A.; Hilal-Alnaqbi, A.; AbuQamar, S.F.; El-Tarabily, K.A. Halotolerant marine rhizosphere-competent actinobacteria promote Salicornia bigelovii growth and seed production using seawater irrigation. Front. Microbiol. 2020, 11, 552.
Patten, C.L.; Glick, B.R. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 1996, 42, 207–220.
Glick, B.R. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica 2012, 2012, 963401.
Camerini, S.; Senatore, B.; Lonardo, E.; Imperlini, E.; Bianco, C.; Moschetti, G.; Rotino, G.L.; Campion, B.; Defez, R. Introduction of a novel pathway for iaa biosynthesis to rhizobia alters vetch root nodule development. Arch. Microbiol. 2008, 190, 67–77.
Arshad, M.; Saleem, M.; Hussain, S. Perspectives of bacterial acc deaminase in phytoremediation. TRENDS Biotechnol. 2007, 25, 356–362.
Kapoor, R.; Evelin, H.; Mathur, P.; Giri, B. Plant Acclimation to Environmental Stress; Springer: Berlin/Heidelberg, Germany, 2013; pp. 359–401.
Balestrini, R.; Lumini, E. Focus on mycorrhizal symbioses. Appl. Soil Ecol. 2018, 123, 299–304.
Posta, K.; Duc, N.H. Benefits of arbuscular mycorrhizal fungi application to crop production under water scarcity. In Drought Detect Solut; InTechOpen: Rijeka, Croatia, 2020.
Ouledali, S.; Ennajeh, M.; Ferrandino, A.; Khemira, H.; Schubert, A.; Secchi, F. Influence of arbuscular mycorrhizal fungi inoculation on the control of stomata functioning by abscisic acid (aba) in drought-stressed olive plants. S. Afr. J. Bot. 2019, 121, 152–158.
Laxa, M.; Liebthal, M.; Telman, W.; Chibani, K.; Dietz, K.-J. The role of the plant antioxidant system in drought tolerance. Antioxidants 2019, 8, 94.
Bao, X.; Wang, Y.; Olsson, P.A. Arbuscular mycorrhiza under water-carbon-phosphorus exchange between rice and arbuscular mycorrhizal fungi under different flooding regimes. Soil Biol. Biochem. 2019, 129, 169–177.
Wang, Y.; Qiu, Q.; Yang, Z.; Hu, Z.; Tam, N.F.-Y.; Xin, G. Arbuscular mycorrhizal fungi in two mangroves in south china. Plant Soil 2010, 331, 181–191.
Estrada, B.; Aroca, R.; Maathuis, F.J.; Barea, J.M.; Ruiz-Lozano, J.M. Arbuscular mycorrhizal fungi native from a m editerranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ. 2013, 36, 1771–1782.
Al-Karaki, G.N. Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci. Hortic. 2006, 109, 1–7.
Talaat, N.B.; Shawky, B.T. Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ. Exp. Bot. 2014, 98, 20–31.
Vurukonda, S.S.K.P.; Vardharajula, S.; Shrivastava, M.; SkZ, A. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 2016, 184, 13–24.
Miliute, I.; Buzaite, O.; Baniulis, D.; Stanys, V. Bacterial endophytes in agricultural crops and their role in stress tolerance: A review. Zemdirbyste-Agriculture 2015, 102, 465–478.
Mitter, B.; Petric, A.; Shin, M.W.; Chain, P.S.; Hauberg-Lotte, L.; Reinhold-Hurek, B.; Nowak, J.; Sessitsch, A. Comparative genome analysis of burkholderia phytofirmans psjn reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front. Plant Sci. 2013, 4, 120.
Sgroy, V.; Cassán, F.; Masciarelli, O.; Del Papa, M.F.; Lagares, A.; Luna, V. Isolation and characterization of endophytic plant growth-promoting (pgpb) or stress homeostasis-regulating (pshb) bacteria associated to the halophyte prosopis strombulifera. Appl. Microbiol. Biotechnol. 2009, 85, 371–381.
Khan, A.L.; Hussain, J.; Al-Harrasi, A.; Al-Rawahi, A.; Lee, I.-J. Endophytic fungi: Resource for gibberellins and crop abiotic stress resistance. Crit. Rev. Biotechnol. 2015, 35, 62–74.
Singh, L.P.; Gill, S.S.; Tuteja, N. Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal. Behav. 2011, 6, 175–191.
Rodriguez, R.J.; Henson, J.; Van Volkenburgh, E.; Hoy, M.; Wright, L.; Beckwith, F.; Kim, Y.-O.; Redman, R.S. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2008, 2, 404–416.
Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010, 33, 453–467.
Bae, H.; Sicher, R.C.; Kim, M.S.; Kim, S.-H.; Strem, M.D.; Melnick, R.L.; Bailey, B.A. The beneficial endophyte trichoderma hamatum isolate dis 219b promotes growth and delays the onset of the drought response in theobroma cacao. J. Exp. Bot. 2009, 60, 3279–3295.
Mastouri, F.; Björkman, T.; Harman, G.E. Seed treatment with trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 2010, 100, 1213–1221.

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