Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: A review

Pedosphere 30(1): 40–61, 2020 doi:10.1016/S1002-0160(19)60839-8 ISSN 1002-0160/CN 32-1315/P c 2020 Soil Science Society of China ⃝ Published by Elsevier B.V. and Science Press

Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: A review Madhurankhi GOSWAMI and Suresh DEKA∗ Environmental Biotechnology Laboratory, Resource Management and Environment Section, Life Sciences Division, Institute of Advanced Study in Science and Technology (IASST), Guwahati Assam 781035 (India) (Received April 27, 2019; revised July 15, 2019)

ABSTRACT With the continuous increase in human population, there is widespread usage of chemical fertilizers that are responsible for introducing abiotic stresses in agricultural crop lands. Abiotic stresses are major constraints for crop yield and global food security and therefore require an immediate response. The implementation of plant growth-promoting rhizobacteria (PGPR) into the agricultural production system can be a profitable alternative because of its efficiency in plant growth regulation and abiotic stress management. These bacteria have the potential to promote plant growth and to aid in the management of plant diseases and abiotic stresses in the soil through production of bacterial phytohormones and associated metabolites as well as through significant root morphological changes. These changes result in improved plant-water relations and nutritional status in plants and stimulate plants’ defensive mechanisms to overcome unfavorable environmental conditions. Here, we describe the significance of plant-microbe interactions, highlighting the role of PGPR, bacterial phytohormones, and bacterial metabolites in relieving abiotic environmental stress in soil. Further research is necessary to gather in-depth knowledge on PGPR-associated mechanisms and plant-microbe interactions in order to pave a way for field-scale application of beneficial rhizobacteria, with the aim of building a healthy and sustainable agricultural system. Therefore, this review aims to emphasize the role of PGPR in growth promotion and management of abiotic soil stress with the goal of developing an eco-friendly and cost-effective strategy for future agricultural sustainability. Key Words: phytohormones, plant-microbe interaction, root colonization, root morphological change, secondary metabolites, stress alleviation, stress tolerance Citation: Goswami M, Deka S. 2020. Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: A review. Pedosphere. 30(1): 40–61.

INTRODUCTION Today, according to the most recent estimate by the United Nations (UN), there are 7.3 billion people in the world, and this number is expected to reach 9.7 billion by 2050. The rapid worldwide increase in human population is accompanied by an increase in the level of environmental damage as a consequence of rapid industrialization and urbanization (Mahanty et al., 2017). To meet the growing demand for food worldwide, the unconditional usage of chemical fertilizers in agricultural production is necessary regardless of the damage to soil health and ecology. As a consequence, the introduction of deleterious abiotic environmental stresses in soil resulted in a considerable decrease in crop quality and quantity (Shrivastava and Kumar, 2015). Meanwhile, natural abiotic stresses prevent crop plants from achieving their full genetic potential (Tuteja and Sopory, 2008). ∗ Corresponding

author. E-mail: [email protected].

Abiotic stresses are adverse environmental conditions that hamper microbial functional diversity and soil physicochemical properties, resulting in considerable yield loss. These stresses include drought, high salinity, heavy metal toxicity, and high and low temperature, among others. A standout amongst dominant and regular abiotic stresses is soil salinization or salinity stress. Soil salinization refers to an increase in the concentration of salts in the soil. Saline soils are defined as soils in which the electrical conductivity (EC) of the saturation extract (ECe ) in the root zone exceeds 4 dS m−1 (ca. 40 mmol L−1 NaCl) at 25 ◦ C and has an exchangeable sodium percentage of 15%. Throughout the years, a considerable share of arable lands (20% of all cultivated lands and 33% of all irrigated lands) has been affected by the increase in soil salinity (Jamil et al., 2011). It is estimated that soil salinity has influenced ca. 3.6 billion hectares of agricultural dryland out of the world’s 5.2 billion hectares of arable land.

PLANT GROWTH-PROMOTING RHIZOBACTERIA

Existing literature sources describe about the severe impacts of soil salinity on plant health and productivity and the loss in crop yield due to soil salinization. It has been evaluated that soil salinization caused a total loss of US$27.3 billion, which directly affected the world economy (Meena et al., 2017). It has been estimated that abiotic stresses influence ca. ten hectares of land per minute, three of which are lost as a consequence of soil salinization around the world. In India, soil salinity has taken over seven million hectares of cultivable land (Flowers and Yeo, 1995). Similar to high salinity, drought is a condition of extreme stress that affects the hydrological cycle and has a prominent negative impact on the environment as well as on the society and economy. Drought is defined as a condition or a period in which the critical precipitation level is not reached. Globally, the percentage of drought-affected arable land has increased more than twice in the period from the 1970s to the early 2000s, and the unaffected land areas are expected to reduce to half by 2050, presenting a great threat to worldwide crop yield (Kasim et al., 2013). Prolonged drought conditions would result in a situation of reduced available water in soil, with atmospheric conditions causing continuous loss of water by transpiration or evaporation (Jaleel et al., 2009). Extremely dry conditions can have a significant influence on the physiology of the soil ecosystem (Geng et al., 2016). Drought has far-reaching negative effects on the global food production, causing an estimated decrease of 5% in harvest yield in the primary food-producing nations and an annual loss of 17% in harvest yield in the tropics, arid, and semi-arid regions (Edmeades et al., 1992). Throughout the last few years, a lot of interest was directed towards sustainable agriculture with the emphasis on the implementation of soil inoculation with beneficial rhizosphere microorganisms known to promote plant growth under various abiotic stresses (Kumar and Verma, 2018). Application of rhizospherecolonizing microorganisms can help promote environmental stability and develop sustainable agriculture over the years. This group of root-associated microbes is termed as plant growth-promoting rhizobacteria (PGPR). They belong to various genera (Bacillus, Pseudomonas, Enterobacter, Burkholderia, Klebsiella, Variovorax, Azospirillum, Azotobacter, and Serratia) and are believed to promote plant growth under both normal and stress conditions. Reportedly, there are a few PGPR strains that are sensitive to abiotic stresses, while there are a large number of PGPR strains that can endure abiotic stress while maintaining plant fitness and soil health (Vimal et al., 2017). These stress-

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tolerant rhizosphere-colonizing microbes display various mechanisms for alleviating harsh soil conditions thereby increasing plant growth. Specifically, the associated plant microbes encourage plant growth directly by enabling easy nutrient acquisition as well as indirectly by synthesizing certain inhibitory substances or antibiotics for disease suppression in plants (Mahanty et al., 2017). Still, there is not much information on rhizobacteria-mediated stress tolerance in plants despite of it having a great potential for increasing agricultural productivity and sustainability. In this review article, we wanted to explore the success of PGPR in alleviation of abiotic stresses in soil as well as to emphasize the PGPR associated mechanisms for upgrading agricultural sustainability, productivity, and profitability. The PGPR are a group of bacteria that colonize the rhizosphere of various leguminous and non-leguminous plants with a wide array of biologically and ecologically significant functions. The root rhizosphere is the most dynamic and nutrient-laden ecological niche as a consequence of accumulation of various root exudates influencing the surrounding soil microbial flora (Hiltner, 1904). Root colonization by the rhizospheric bacteria is principally a consequence of 5%–21% of total organic carbon being fixed in the rhizosphere region (Barber and Martin, 1976; Oliveira, 1995), plant photosynthetic products comprising 5%–30% of the root exudates (Glick, 2014), and the presence of a series of low molecular weight compounds such as ions, free oxygen and carbon, mucilage, and different primary and secondary plant metabolites (Uren, 2000; Bertin et al., 2003). Additionally, they use chemotaxis to colonize plant roots that help them to get involved in several important biological processes (Kloepper, 1992; Hardoim et al., 2008; Dimkpa et al., 2009) (Fig. 1). Even under stress conditions, PGPR play a fundamental role in plant growth and development by both indirect and direct mechanisms. They actively participate in inducing plant growth through mobilization of soil nutrients, control of hormonal and nutritional balance in plants, and secretion of plant growth regulators and signal molecules. They also induce resistance in plants against a wide range of phytopathogens that are responsible for various plant diseases (Dakora et al., 2015; Spence and Bais, 2015; Tanaka et al., 2015). This particular group of rhizobacteria also produces certain metabolites such as biosurfactants that can target pathogens, altering their cell membrane permeability, causing cell lysis and production of siderophores that can restrict the growth of pathogens by restricting iron accessibility (Zloch et al., 2016). They are known for

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M. GOSWAMI AND S. DEKA

Fig. 1 Schematic diagram depicting plant growth-promoting rhizobacteria (PGPR) colonizing plant roots and altering their morphological and physiological traits. IST = induced systemic tolerance.

the production of different plant growth promoters, exopolysaccharides, rhizobitoxine (Vardharajula et al., 2011), and certain signal molecules such as lumichrome (Dakora et al., 2015) and lipochitooligosaccharides (Tanaka et al., 2015). Rhizobitoxine can promote plant growth and development under stress conditions by restricting ethylene production in plants. Similarly, the two signal molecules, lumichrome and lipochitooligosaccharides, can help the plants in sensing environmental stress. Moreover, they act as growth regulators in microbes and plants, affecting plant biomass production, shoot and root growth, lateral root branching, cell cycle, embryogenesis, and serving as protectants in plant defense. In particular, these signal molecules initiate plant symbiotic interactions with rhizospheric microorganisms, thus protecting the plants from the negative impacts of biotic and abiotic stress (Tanaka et al., 2015). In addition to the aforementioned ones, thuricin 17 (Th17), a type of bacteriocin produced by different Bacillus species, also functions as a potent bacterial signaling compound promoting plant growth in both leguminous and non-leguminous plants. Among all, this

is the most widely studied bacteriocin molecule because of its substantial involvement in the promotion of plant growth. Thuricin 17 aids in the germination of seedlings even under stress conditions (Subramanian and Smith, 2015). Amongst the phytohormones, indole-3-acetic acid (IAA) is the most important signal molecule in plant-microbe interactions, including phytostimulation and phytopathogenesis (Duca et al., 2014). These groups of bacteria are potential candidates for ameliorating abiotic stresses because of their inherent metabolic and genetic capabilities (Gopalakrishnan et al., 2015). They are known to contain certain plant growth-promoting enzymes, such as 1-aminocyclopropane-1-carboxylate (ACC) deaminase, and to produce extracellular lytic enzymes like chitinases, glucanases, cellulases, and proteases that cause cell lysis and degradation of fungal cell walls (Mabood et al., 2014). Furthermore, some of the PGPR strains have sigma factors that help plants to overcome the negative impacts of stress through certain alterations in gene expression. In general, the mechanisms exhibited by PGPR help maintain the normal growth rate of

PLANT GROWTH-PROMOTING RHIZOBACTERIA

plants under stress conditions by mitigating the negative impacts of stress on plant development. ABIOTIC STRESSES: IMPACTS OF DROUGHT AND SALINITY STRESSES Abiotic stresses are adverse environmental conditions that influence soil microbial diversity and physicochemical properties, causing substantial yield loss (Miloˇsevi´c et al., 2012). The main cause of the sudden increase in abiotic stresses is constant human activities, either intensive agricultural practices aimed at boosting agricultural productivity or degradation of arable lands because of industrialization (Miloˇsevi´c et al., 2012; Minhas et al., 2017). These abiotic stresses generally have severe negative impacts on plant growth and development (Fig. 2) (Meena et al., 2017). Drought stress: a curse for agricultural production Drought is a period of unusual decrease in moisture content in the soil as a consequence of a prolonged period of low rainfall. It is one of the most

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common and most devastating abiotic stresses that caught the attention of environmentalists and agricultural scientists. Globally, it is one of the major causes of restricted plant growth and productivity. The majority of arable lands around the world are influenced by drought stress. The share of drought-affected arable land has increased more than twice during the period from 1970s to the early 2000s, and the share of unaffected land is expected to reduce to half by 2050, posing serious threats to worldwide crop productivity (Ashraf and Wu, 1994; Vinocur and Altman, 2005; Kasim et al., 2013). Drought has far-reaching consequences on human society, especially on national economies (Kumar and Verma, 2018). With the constant change in atmospheric conditions, it has been predicted that the severity, recurrence, and duration of drought in many crop-producing nations will increase, which would pose a serious threat to global food security. Consequently, there is a need to find ways of enabling plants to adjust to environmental drought stress while maintaining normal plant growth in order to be able to satisfy the global food requirement.

Fig. 2 Schematic diagram depicting the effects of diverse abiotic stresses on plants and the roles of plant growth-promoting rhizobacteria (PGPR) in alleviating stress in soil.

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Plant responses to drought stress: adaptive mechanisms Drought stress affects growth parameters and stress-responsive genes in plants. Plants modify their morphological and physiological traits to adjust to harsh environmental conditions (Hameed et al., 2010). Plant roots are crucial for sensing and responding to various external environmental stimuli because of their direct contact with soil water and accessible nutrients. The root system receives stress signals from the soil and integrates both biotic and abiotic cues to adjust and alter its genetic program for post-embryonic root development (S´anchez-Calder´ on et al., 2013). Plant roots alter their morphology depending on variations in soil surface moisture, i.e., water deficit conditions lead to deeper root penetration while higher water content in the soil decreases root infiltration (Zhang et al., 2017). Accordingly, alterations in root morphology help the plants survive drought conditions. The presence of a large number of short and slender lateral roots in addition to smaller roots results in larger root surface area for better absorption of moisture and nutrients from soil during drought conditions (Wang et al., 2016). A root system with an extensive root surface area is crucial for increasing plant tolerance to drought stress. Similarly, the presence of specialized tissues, such as rhizodermis, and the reduction in the number of cortical layers in roots are considered as adaptive benefits for plants to survive drought stress. Moreover, hormonal crosstalk and activation of enzymes related to plant root morphology have been implicated as potential stress-responsive signals for modifying root architecture. Additionally, the R2R3-type myeloblastosis (MYB) transcriptional activator and plant microRNA miR393 are also known to play a significant role in root-mediated adaptation to drought stress through attenuation of auxin signaling (Seo and Park, 2009; Chen et al., 2012). In conclusion, these adaptations are positively correlated with root growth and have a direct impact on crop yield under drought conditions. The mechanisms involved in drought tolerance in plants include different biochemical, physiological, and molecular processes. These processes are regulated by hormonal interactions in plant tissues (Khan et al., 2018). Plant growth regulators, such as gibberellic acid (GA), cytokinin (CK), auxin, abscisic acid (ABA), jasmonic acid (JA), and ethylene allow plants to modify their responses and adapt to drought stress (Basu et al., 2016). Drought stress causes fluctuations in gene expression patterns in plants, and alters the expression of dehydrin/late embryogenesis abundant (LEA)

M. GOSWAMI AND S. DEKA

genes and molecular chaperones responsible for protecting the cell from protein denaturation (Hussain et al., 2018). Moreover, studies have reported that drought stress induces the expression of a variant of histone H1, which is responsible for the expression of drought stress-responsive genes for stomatal closure (Scippa et al., 2004). Under drought conditions, ABA acts as an essential signaling mediator for regulating various plant developmental processes and adaptive responses. Osmotic stress in plants induces ABA synthesis that begins in plastids and ends in the cytoplasm with xanthoxin conversion to ABA (Seo and Koshiba, 2002). In addition, ABA improves drought tolerance through proper regulation of stress-responsive genes. There are several ABA signaling genes, such as OsNAP, OsNAC5, and DSM2, which have been proven to improve grain yield under drought conditions. Furthermore, these ABA-induced non-stomatal adaptations in plants can be used to improve the quality and quantity of crop yield. Recently, some studies reported that overexpression of ABA-induced GhCBF3 gene resulted in drought resistance in plants through proper maintenance of water level, chlorophyll, and proline content (Ma et al., 2016). Drought-induced increase in ABA levels regulates the expression of glycine-rich dehydrin genes (DHN1/RAB DHN2) as well as the expression of a conserved element of RAB28 gene (Hussain et al., 2018). Under drought stress, CKs are responsible for delaying leaf senescence and death, which are adaptive traits necessary for increasing crop yield, as well as for increasing stress tolerance in plants by seed priming. An increase in the level of endogenous CK as a consequence of the expression of isopentenyltransferase (IPT) helps plants adapt to drought stress by delaying drought-induced senescence, thereby promoting crop yield (Peleg and Blumwald, 2011; Peleg et al., 2011). Recently it has been reported that higher levels of auxin increased drought tolerance in plants, and this was connected with reduced levels of reactive oxygen species (ROS) and delayed leaf senescence. Moreover, some studies revealed that overexpression of one of the YUCCA genes (YUCCA6) is crucial in maintaining the balance of auxin levels in several crop plants (Ke et al., 2015). Both increased and decreased levels of auxin can increase drought tolerance in plants. Increased levels of auxin promote the upregulation of drought stress LEA genes, leading to an increase in drought tolerance (Xie et al., 2003; Zhang et al., 2009). Some studies proposed that higher expression of OsIAA6, YUC6, DEEPER ROOTING 1 (DRO1) genes related to auxin biosynthesis induces drought tolerance in crop cultivars, thereby promoting crop yield under drought

PLANT GROWTH-PROMOTING RHIZOBACTERIA

stress conditions (Uga et al., 2013; Jung et al., 2015; Ke et al., 2015). Moreover, auxin is considered an important factor in defense responses in plants as it is involved in regulating the expression of different genes and in mediating hormonal crosstalk in both abiotic and biotic stress responses (Fahad et al., 2015). Gibberellic acid also plays an important role in drought stress. A sharp decrease in endogenous GA (as a consequence of the overexpression of AtGAMT1 gene) results in increased plant drought tolerance. The AtGAMT1 gene encodes an enzyme that catalyzes the methylation of active GA, resulting in the production of inactive GA methyl esters, thus lowering endogenous GA levels and increasing drought tolerance in plants (Ullah et al., 2018). Similarly, JA is believed to play a crucial role in combating various abiotic stresses. Some studies reported that exogenous application of JA improved plant performance in dry environments (Bandurska et al., 2003) and regulated stomatal dynamics (Riemann et al., 2015). In drought stress conditions, the presence of JA and its derivatives results in the degradation of jasmonate ZIM-domain (JAZ) proteins involved in activation of myelocytomatosis (MYC) transcription factor (TF) MYC2, and this leads to the up-regulation of drought stress tolerance genes in plants (Chini et al., 2007). Drought stress tolerance induced by PGPR Prolonged drought conditions stimulate rhizosphere-colonizing bacteria to secrete various phytohormones, osmolytes, extracellular polymeric substances, and antioxidants for inducing root morphological changes and increasing stress tolerance (Yang et al., 2009). Table I illustrates the role of PGPR in alleviating drought stress and enhancing plant growth and development. Bacterial ABA has a crucial role in drought stress alleviation. A few researches reported the efficiency of PGPR in stimulating the production of endogenous ABA, reducing the effects of adverse environmental abiotic stress in soil (Forni et al., 2017). Inoculation of PGPR Phyllobacterium brassicacearum strain STM196 into the rhizosphere of Arabidopsis plants enhanced their osmotic stress tolerance by elevating ABA levels, thereby decreasing leaf transpiration (Bresson et al., 2013). Moreover, higher levels of endogenous ABA stimulate root hydraulic conductivity (Aroca et al., 2006) and up-regulation of aquaporin membrane proteins (Zhou et al., 2012) which increases drought tolerance in plants. Cohen et al. (2015) studied the effects of ABA-producing Azospirillum brasilense Sp 245 on Arabidopsis thaliana Col-0 and aba2-1 mutant

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plants in drought and wet conditions. They observed that priming of the two mutant plants with Sp 245 increased endogenous ABA levels with an increase in plant biomass, lateral roots, photosynthetic and photoprotective pigments, and an altered root architecture along with an increase in seed yield, survival rate, proline level, relative leaf water content, and stomatal conductance. Moreover, ABA is likewise involved in root growth and other necessary plant adaptations apart from increased chlorophyll content and water potential in plants under drought stress (Zhang et al., 2004; Giuliani et al., 2005). The signal molecule IAA is responsible for different plant growth and developmental processes, such as cell division, elongation, and differentiation (Asgher et al., 2015). Some studies demonstrated the variations in auxin synthesis, transport, metabolism, and its activity on exposing the plants to different abiotic stresses (Ljung, 2013). Continuous exposure of plants to stress conditions resulted in a significant decrease in endogenous IAA levels. Application of auxin-producing rhizosphere bacteria can induce significant variations in endogenous IAA synthesis. Creus et al. (2004) reported that bacterial inoculation into the plant rhizosphere improved crop yield under drought stress. They observed that pre-inoculation of Azospirillum brasilense Sp245 to wheat enhanced crop yield and mineral quality with improved water potential, relative and absolute water content, cell wall elasticity, and apoplastic water fraction, indicating an increase in drought tolerance. Similarly, Dimkpa et al. (2009) reported the efficiency of bacterial IAA in increasing stress tolerance in plants. Some of the Azospirillum species were reported to bring about root morphological changes in order to increase stress tolerance in plants. Pereyra et al. (2012) observed a significant increase in osmotic stress tolerance in wheat seedlings inoculated with Azospirillum as a consequence of specific morphological changes in coleoptile xylem architecture. They attributed this enhanced tolerance to upregulation of indole-3-pyruvate decarboxylase gene, resulting in increased IAA synthesis in Azospirillum cells. In water-deficient conditions, Azospirillum-plant associations play a significant role in plants stress tolerance and survival. This type of synergistic plant-microbe association results in a decrease of leaf water potential that can be attributed to IAA production by the existing Azospirillum cells, resulting in enhanced water and nutrient uptake (Arzanesh et al., 2011). Apart from Azospirillum sp., Bacillus sp. is also involved in increasing drought tolerance in plants. he plant growth-promoting rhizobacterium B. thuringiensis was reported to increase drought resista-

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TABLE I Plant growth-promoting rhizobacteria (PGPR)-induced changes in plant morphological, physiological, and molecular traits under environmental stresses PGPR

Plant

Changes in plant morphological, physiological, or molecular traits

Reference

Azospirillum brasilense Sp245 Pseudomonas putida H-2-3 Phyllobacterium brassicacearum STM196

Wheat (Triticum aestivum) Soybean (Glycine max L.) Oilseed rape (Arabidopsis thaliana)

Increased relative and absolute water content, water potential, and apoplastic water fraction Increased production of gibberellins

Creus et al., 2004

Bresson et al., 2013

Achromobacter piechaudii ARV8

Tomato (Lycopersicum esculentum cv. F144) and pepper (Capsicum annuum L. cv. Maor) Oilseed rape

Improved osmotic tolerance as a result of increased abscisic acid (ABA) content which decreases leaf transpiration Increased fresh and dry weights of tomato and pepper plants with significantly decreased ethylene production Expression of drought responsive gene (ERD15) and ABA responsive gene in Arabidopsis plants Significantly increased relative water content

Timmusk and Wagner, 1999 Grover et al., 2014

Decreased plant ethylene concentration due to sequestration and cleavage of plant produced 1-aminocyclopropane-1-carboxylate (ACC) deaminase Increased plant growth and nitrogen content, and stimulated nodulation process Stimulated seed germination and seedling growth

Lim and Kim, 2013

Paenibacillus polymyxa Bacillus sp. KB129 Bacillus licheniformis K11

Sorghum (Sorghum bicolor var. CSV-15) Pepper

Paenibacillus polymyxa and Rhizobium tropici Arthrobacter siccitolerans 4J27, Pseudomonas fluorescens DR11, Enterobacter hormaechei DR16, and Pseudomonas migulae DR35 Pseudomonas putida GAP-P45

Common bean (Phaseolus vulgaris L.) Foxtail millet (Setaria italica)

Pseudomonas entomophila BV-P13, Pseudomonas stutzeri GRFHAP-P14, Pseudomonas putida GAP-P45, Pseudomonas syringae GRFHYTP52, and Peudomonas monteilli WAPP53 Bacillus amyloliquefaciens HYD-B17, Bacillus licheniformis HYTAPB18, Bacillus thuringiensis HYDGRFB19, Paenibacillus favisporus BKB30, and Bacillus subtilis RMPB44 Pseudomonas aeruginosa GGRJ21

Maize (Zea mays)

Sunflower (Helianthus sp.)

Maize

Mung bean (Vigna radiate (L.) R. Wilczek)

Kang et al., 2014b

Mayak et al., 2004b

Figueiredo et al., 2008 Niu et al., 2017

Increased survival, plant biomass, and root adhering soil/root tissue ratio of sunflower seedlings as well as significantly increased stable soil aggregates Increased plant biomass, leaf water potential, relative water content, root adhering soil/root tissue ratio, aggregate stability, mean weight diameter, as well as proline, sugars, and free amino acid levels and reduced transpiration rate

Sandhya et al., 2009

Increased plant biomass, relative water content, leaf water potential, root adhering soil/root tissue ratio, aggregate stability, as well as proline, sugars, and free amino acid levels, decreased leaf water and electrolyte loss, and increased activity of antioxidant enzymes (ascorbate peroxidase, catalase, and glutathione peroxidase) Increased root length, shoot length, dry weight, and relative water content along with stronger upregulation of three drought stress-responsive genes, i.e., dehydration-responsive element binding protein (DREB2A), catalase (CAT1), and dehydrin (DHN)

Vardharajula et al., 2011

nce in French lavender (Lavandula dentata) plants growing in drought-affected areas by increasing IAA production, thereby enhancing plant metabolic activities and significantly improving the nutritional and physiological status of the plant (Armada et al., 2014). Simi-

Sandhya et al., 2010

Sarma and Saikia, 2014

larly, Raheem et al. (2018) conducted pot trials to evaluate the role of rhizobacteria in enhancing the growth of wheat under different water regimes. They reported that at the highest level of water stress, i.e., at 10% field capacity (FC), there was a significant im-

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provement in shoot length of wheat plants inoculated with B. amyloliquefaciens S-134. Moreover, they reported that the inoculation of B. muralis D-5 and Enterobacter aerogenes S-10 increased grain yield of wheat plants by 34% with a two-fold increase in spike length and seed weight. Tahir et al. (2019) reported that PGPR strains BN-5 and MD-23 secreting ACC deaminase, IAA, and exopolysaccharide (EPS) increased the yield and quality of maize under both well-watered and drought conditions. They observed that the inoculation of PGPR strains reduced the water loss in excised leaves and increased relative leaf water and chlorophyll contents as well as grain yield in plants under both well-watered and drought conditions compared to uninoculated control plants. Similar to IAA, bacterial ACC deaminase plays a significant role in drought stress alleviation and drought tolerance in plants. Plant metabolic activities are regulated by ethylene, and ethylene biosynthesis is regulated by both biotic and abiotic environmental conditions. Under stress conditions, the plant hormone ethylene endogenously regulates plant homeostasis resulting in restricted root and shoot growth. Plants are homeostatic in nature and plant homeostasis gets disturbed under stressed conditions. Plant homeostasis can be maintained through proper regulation of bacterial ACC deaminase that results in suitable degradation of plant produced ACC and balance of the total ACC content in plants, thereby enhancing plant growth (Awasthi et al., 2015; Glick et al., 2007a, b). Literature sources revealed that inoculation of plants with ACC-producing bacteria not only enhanced seed yield, seed number, and seed nitrogen accumulation, but also efficiently restored root nodulation in the host plant. Increase in root nodulation can be achieved by successful inoculation of efficient nitrogen-fixing bacteria in the root rhizosphere, thereby preventing drought-induced decrease in nodulation and in turn restoring seed nitrogen content. Priming of tomato and pepper seedlings with ACC deaminasecontaining Achromobacter piechaudii ARV8 (Mayak et al., 2004b) enhanced both dry and fresh weight of the plants. Similarly, priming of pea plants with Variovorax paradoxus 5C-2 (Belimov et al., 2009) enhanced plant growth, crop yield, and water use efficiency in plants. Recently, Belimov et al. (2015) studied the efficiency of certain auxin-producing and ACC deaminase-containing rhizosphere-colonizing bacteria (Achromobacter xylosoxidans Cm4, Pseudomonas oryzihabitans Ep4, and Variovorax paradoxus C2) in improving growth and yield of well-watered and waterdeficient potato plants by decreasing amino acid con-

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centration in the rhizosphere. They observed that rhizobacterial inoculation increased root biomass and tuber yield up to 50% and 40%, respectively, in a pot experiment, as well as tuber yield up to 27% in a field experiment. Thus, it is widely acknowledged that the implementation of PGPR into drought-stressed soil provides an economic mean for sustainable crop health apart from crop yield. Chandra et al. (2019a) observed that inoculation of ACC deaminase-containing Variovorax paradoxus RAA3 and a consortium of Pseudomonas spp. (DPC12, DPB13, DPB15, and DPB16) significantly increased the growth of wheat plants in water-stressed rain-fed conditions. Post-inoculation with these strains increased wheat growth and foliar nutrient concentrations under water-stressed conditions and caused significant positive changes in antioxidant properties compared to control plants. Furthermore, Chandra et al. (2019b) extended their study and focused on three ACC deaminase-containing bacterial strains, Pseudomonas palleroniana DPB16, Pseudomonas sp. UW4, and Variovorax paradoxus RAA3, in order to evaluate their efficiency in improving growth, nutrient content, and yield of wheat varieties HD2967 (drought sensitive) and PBW660 (drought tolerant) under drought and rainfed conditions. They observed increased wheat yield as well as significant positive changes in biochemical and antioxidant properties in wheat plants after bacterial inoculation compared to the uninoculated plants under both conditions. Gibberellins or GA are a group of plant growth hormones involved in several developmental and physiological processes in plants. They act as signaling factors for host plants under both normal and stressed conditions (Bottini et al., 2004). There are reports of Pseudomonas strain producing gibberellins under drought stress conditions, thereby enhancing cell division and cell elongation in the affected plants (Shao et al., 2008). Creus et al. (2004) reported the efficiency of Azospirillum lipoferum in increasing drought stress tolerance in wheat plants. Similarly, Kang et al. (2014b) studied the efficiency of GA-producing Pseudomonas putida H-2-3 on the growth and physiological processes of soybean plants growing under drought stress conditions. They observed that the inoculation of H-2-3 protected the plants from drought stress by modulating antioxidant levels via decreasing superoxide dismutase (SOD), flavonoids, and radical scavenging activity. Recently, Park et al. (2017) studied the efficiency of Bacillus aryabhattai SRB02 in the production of gibberellin and other related phytohormones by inoculating soybean roots under drought stress conditions in South Korea. They observed a significant

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improvement in plant growth and development after the inoculation of SRB02 into the rhizosphere. Similarly, Ghosh et al. (2019) reported that after inoculating Arabidopsis thaliana seedlings with GA-, auxin-, and CK-producing Pseudomonas aeruginosa PM389, Pseudomonas aeruginosa ZNP1, Bacillus endophyticus J13, and Bacillus tequilensis J12 strains individually, they observed that all four strains were able to alleviate the adverse effects of drought stress on plants, as evidenced by their enhanced fresh weight, dry weight, and water content compared to the uninoculated plants. Under drought stress conditions, CKs are known to play a vital role in delaying premature leaf senescence and death. An increase in endogenous CK level benefits the plants by enhancing drought tolerance as well as increasing crop yield in plants (Peleg and Blumwald, 2011). There are several research findings that revealed the efficiency of CKs in increasing plant drought tolerance. Arkhipova et al. (2007) observed a significant increase in both shoot/leaf CK content and biomass of 12-d-old lettuce seedlings growing under water deficit conditions after inoculation with a CK-producing Bacillus sp. strain. They concluded that inoculation of CK-producing bacterial isolate enhanced root biomass and root sink strength in drought-affected plants. Similarly, a delay in drought-induced senescence was observed in alfalfa plants primed with CK-producing bacterium Sinorhizobium meliloti (Xu et al., 2012). It was found that CK synthesis could be increased up to five times the normal CK production level via cell transformation through the expression of Agrobacterium IPT gene. For instance, Grover et al. (2011) observed that inoculation of CK-producing bacterial strain Azotobacter chrococcum to drought-affected plant rhizosphere resulted in the accumulation of ABA, which is responsible for the degradation of ROS produced as a result of water-deficient conditions, thereby relieving drought stress. Liu et al. (2013) observed that inoculation of CK-producing Bacillus subtilis can alleviate drought stress by interfering with the suppression of shoot growth, showing the potential of this isolate to function as a drought stress alleviator in arid environments. Recently, Jorge et al. (2019) revealed that inoculation of drought-tolerant CK-producing bacterial Methylobacterium oryzae isolate to lentils (Lens culinaris cv. CDC Maxim) significantly increased growth, physiological parameters, water management, CK levels, and drought tolerance in drought-affected lentils. Similarly, JAs are involved in increasing drought tolerance in plants, and it has been reported that exogenous application of JAs increases the production of different antioxidants that ultimately assist in drought

M. GOSWAMI AND S. DEKA

alleviation. The defensive activity of JAs is related to their ability to behave as antioxidants. Moreover, JAs enhance the activities of enzymes, including cationic peroxidase, pathogenesis-related proteins, and antioxidant enzymes in crop plants (Forni et al., 2017). De Domenico et al. (2012) studied the pattern of expression of jasmonate signaling pathway gene MYC2 in Desi chickpea grown under drought stress conditions. One of their reports established the role of jasmonates in early drought stress signaling and their association with the tolerance mechanism of the drought-tolerant chickpea variety. Similar results were reported by Tiwari et al. (2016) in ameliorating drought stress in chickpea cv. BG-362 (Desi) and cv. BG-1003 (Kabuli) after the inoculation of Pseudomonas putida MTCC5279 (RA) strain in vitro and under greenhouse conditions. Some of the PGPR, besides producing phytohormones, also produce osmolytes in order to combat severe water-deficient conditions. These osmolytes work synergistically with plant-produced osmolytes and promote plant growth. Proline has been recognized as a multifunctional signatory molecule which in high concentration helps increase stress tolerance in plants by acting as an osmolyte, a metal chelator, and an antioxidant defense molecule (Dar et al. 2016). Thus, a positive correlation was drawn between proline build-up and drought tolerance in plants. Subsequently, Sandhya et al. (2010) and Ansary et al. (2012) reported that priming of maize plants with Pseudomonas putida GAP-P45 or Pseudomonas fluorescens increased proline levels in plants, thereby improving plant biomass, relative water content, and leaf water potential of maize plants in arid environments. Likewise, trehalose is a well-known osmoprotectant that provides osmoprotection to plants by stabilizing dehydrated enzymes and plant membranes (Yang et al., 2010). Studies have reported that high levels of trehalose have a positive impact on survival and yield of plants nodulated by rhizobial strains after severe and long periods of drought. Su´arez et al. (2008) observed that priming of Phaseolus vulgaris plants with Rhizobium etli increased drought tolerance in drought-affected plants. Along with other stress-responsive genes, it stimulated the trehalose-6-phosphate synthase gene responsible for trehalose biosynthesis in plants, thereby increasing plant drought tolerance. Similarly, Rodr´ıguez-Salazar et al. (2009) observed that priming of maize plants with a transformed Azospirillum brasilense using a plasmid carrying a trehalose biosynthesis fusion gene (otsA and otsB) resulted in an increased drought stress survival rate to 85% in comparison to 55% survival

PLANT GROWTH-PROMOTING RHIZOBACTERIA

rate in plants inoculated with wild-type strain. Likewise, polyamines such as cadaverine, spermidine (Spd), spermine (Spm), and putrescine (Put) are some of the significant metabolites involved in increasing osmotic tolerance in drought-affected plants in addition to having a key role in cell-differentiation, root elongation, and transcriptional regulation (Kaushal, 2019). Recently, it has been reported that inoculation of Arabidopsis plants with Spd-producing Bacillus megaterium BOFC15 resulted in elevated levels of cellular polyamines under drought stress conditions. Increase in levels of cellular polyamines helped the plants survive drought stress by modifying the host root system with longer primary roots and increased lateral roots as compared to the length of roots of the uninoculated plants (Zhou et al., 2016). Antioxidant enzymes such as catalase (CAT), peroxidases (POX), ascorbate peroxidase (APX), glutathione peroxidase (GPX), and SOD play a crucial role in drought stress alleviation. They help in the elimination or formation of ROS produced as a result of oxidative stress in plants (Simova-Stoilova et al., 2008). Priming of lettuce (Lactuca sativa) with PGPR Pseudomonas mendocina increased CAT activity in plants, thereby protecting the plants from oxidative damage caused by drought stress (Kohler, 2008). Similarly, Heidari and Golpayegani (2012) reported that inoculation of basil plants with Pseudomonas spp. increased CAT activity in plants. They further studied the effect of microbial consortium on the activity of antioxidant enzymes in drought-affected plants. They observed that priming of basil plants with a microbial consortium increased the activity of multiple antioxidant enzymes, including GPX and APX, thereby increasing stress tolerance in plants. On the other hand, Vardharajula et al. (2011) observed that priming of maize plants with Bacillus spp. reduced the antioxidant enzymes activity (including APX and GPX) in plants. As a result, plants displayed physiological responses that could alleviate the negative effects imposed by drought stress. A similar pattern of antioxidant enzyme activity was observed by Naseem and Bano (2014) in maize plants inoculated with EPSproducing bacteria. Similarly, Armada et al. (2014) observed that inoculation of autochthonous PGPR Bacillus thuringiensis to French lavender and sage (Salvia officinalis) promoted growth and drought tolerance via reduction in stomatal conductance as well as the activity of glutathione reductase (GR) and APX. Application of EPS-producing PGPR strains plays a vital role in increasing stress tolerance of plants growing in water-deficient areas. These PGPR strains not

49

only protect the bacterial inoculants from water stress but also play a crucial role in the regulation of plant nutrient content and translocation of soil water across the roots through microbial biofilm formation (Grover et al., 2011). Moreover, EPS increases the number of soil micro-aggregates that improve plant growth by increasing aggregate stability and root-adhering soil/root tissue (RAS/RT) ratio. Increase in soil aggregation increases water and nutrient uptake from the soil under drought stress conditions, ensuring better plant growth and survival (Vardharajula et al., 2011). Some reports described the efficiency of EPS-producing bacteria in increasing stress tolerance in plants after inoculation. Increased EPS production was observed after the inoculation of a PGPR strain Bacillus amyloliquefaciens in plants under water-deficient conditions compared to non-stressed plants, thereby enhancing resistance in plants (Kaushal and Wani, 2016). Similarly, Hussain et al. (2014) reported that inoculation of catalaseand EPS-producing Rhizobium leguminosarum (LR30), Mesorhizobium ciceri (CR-30 and CR-39), and Rhizobium phaseoli (MR-2) to wheat plants increased the growth, biomass, and drought tolerance of wheat seedlings. Molecular studies revealed that plants inoculated with microbes show different patterns of gene expression in comparison to non-colonized plants. Microbialinduced systemic tolerance (MIST) to drought was observed in Arabidopsis plants primed with Paenibacillus polymyxa due to expression of drought stressresponsive early response to dehydration 15 (ERD15) gene and ABA-responsive gene RAB18 (Timmusk and Wagner, 1999). Wang et al. (2012) observed that MIST to drought tolerance was induced in cucumber plants primed by Bacillus cereus AR156, Bacillus subtilis SM21, and Serratia spp. XY21 via increasing the transcriptional levels of cytosolic ascorbate peroxidase (cAPX) as well as ribulose-1,5-bisphosphate carboxylase oxygenase small and large subunit (RBCS and RBCL, respectively), thereby conferring induced systemic tolerance (IST) in plants under drought stress. Similarly, upregulation of drought stress-responsive genes dehydration responsive element binding (DREB2A) and dehydrin (DHN) was observed in Vigna plants primed with Pseudomonas aeruginosa GGRJ21 (Sarma and Saikia, 2014). In some cases, PGPR priming resulted in repressed expression of stress-responsive LEA and dehydrins involved in the protection of plant macromolecules under stress conditions. Similarly, PGPR priming causes a significant decrease in the expression of genes encoding ROS-scavenging enzymes (CAT, APX, and glutathione transferase (GST)) and ethy-

50

lene biosynthesis genes, such as ACS and ACO, thereby inducing systemic tolerance in drought-stressed plants. Lim and Kim (2013) observed that priming of pepper plants with PGPR strain Bacillus licheniformis B11 resulted in significant increase in plant growth under drought stress conditions. Several reports observed stimulated expression of various drought stress tolerance genes (such as Cadhn, VA, sHSP, and CaPR10) in various plants, e.g., pepper plants showed a 1.5-fold increase in drought tolerance after the inoculation of Bacillus licheniformis B11 (Lim and Kim, 2013). Similarly, co-inoculation of Bacillus amyloliquefaciens 5113 and Azospirillum brasilense NO40 to wheat plants increased their tolerance to drought stress by up-regulation of different stress tolerance genes, such as APX1, SAMS1, and HSP17.8 as well as by increasing the enzymatic activity of specific enzymes involved in plant ascorbate-glutathione redox cycle (Kasim et al., 2013). Thus, gene expression studies play a significant role in understanding the responsive nature of an organism under different environmental conditions and can be characterized by different molecular approaches like 2-D polyacrylamide gel electrophoresis (2D-PAGE), differential display polymerase chain reaction (DD-PCR), real-time polymerase chain reaction (RT-PCR), microarray analysis, Illumina sequencing, etc. (Schlauch et al., 2010). Salinity stress: a major constraint in agricultural production Salinity stress is one of the major constraints to world agricultural production. The immense decrease in global food production in salt-stressed areas is a consequence of changes in soil physicochemical properties which ultimately result in permanent land degradation. Moreover, continuous stress conditions bring about significant changes in plant physiological and morphological traits, resulting in nutrient cytotoxicity and osmotic imbalances (Saharan and Nehra, 2011). It affects almost every aspect of plant growth including germination, vegetative growth, and reproductive development as well as photosynthesis. Under salinity stress, photosynthesis rate is reduced as a consequence of reduction in water potential, which results in a significant decrease in the supply of carbohydrates required for the process of cell growth. The process of photosynthesis is also inhibited when high concentrations of Na+ and Cl− accumulate in chloroplasts, resulting in decreased chlorophyll content in plants. Apart from the abovementioned factors, reduced rate of photosynthesis can also be a consequence of decreases in photosystem II (PSII) activity, electron transport, pho-

M. GOSWAMI AND S. DEKA

tophosphorylation activity, photosynthetic enzymes, chlorophyll, and carotenoid contents (Parihar et al., 2015). Additionally, salt stress disturbs photorespiration, thereby bringing about changes in normal cell homeostasis. Disturbed ion homeostasis affects physiological and metabolic processes in plants (Munns, 2002). Plant responses to salt stress: adaptive mechanisms The plant root architecture determines root performance. A branched root system enables the plants to easily acquire water and nutrients from soil, thereby increasing the substitution rate of plant water loss (Passioura, 1988). A proliferated root system is therefore essential for deep penetration into the soil layers and easier acquisition of water and nutrients (Franco et al., 2011). Under salt stress, plants modify their root architecture to adapt to the surrounding environment. Salt stress induces the reduction of root cortex in order to shorten the distance between epidermis and stele so that there is easy uptake of essential minerals from the soil while preventing the unwanted ones (Hose et al., 2001; Taiz and Zeiger, 2002). It often promotes the suberization of hypodermis and endodermis in the woody tree roots, resulting in the formation of Casparian strip (a specially modified carbohydrate cell wall present in the apoplastic space of a plant cell) closer to the root apex. In halophytes, the Casparian strip along with the endodermis and exodermis form a tight hydrophobic barrier which regulates the apoplastic pathway and maintains the flow of solutes through the selectively permeable plasma membrane into the cytoplasm. Additionally, halophytes have a dense cytoplasm in the meristematic zone of root tips that acts as a barrier against the unwanted influx of solutes into the plant cell during salt stress (Chen et al., 2011). Moreover, they have a thickened primary root that acts as a sink for Na+ ion sequestration in order to prevent Na+ accumulation in the lateral roots and young leaves, thereby protecting the plants from salt stress (Galvan-Ampuda and Testerink, 2011). However, it is quite complex to describe a universal scenario of root responses to an external stimulus, as it varies from species to species as well as between different root developmental stages. In conclusion, the pronounced capacity of the roots to adapt to various external stress conditions is a result of their significant root plasticity (Riedelsberger and Blatt, 2017; Suralta et al., 2018). Plants can regulate and coordinate their growth and stress tolerance by changing the levels of hormone production, distribution, and signal transduction, which consequently promote survival or pro-

PLANT GROWTH-PROMOTING RHIZOBACTERIA

tection from environmental stress (Colebrook et al., 2014). A well-known stress hormone, ABA enables plant growth and survival under conditions of drought and salinity stress (Basu and Rabara, 2017). Salinity causes osmotic stress and water deficiency in plants, which results in a sudden increase in endogenous ABA content. An elevated level of ABA in plants induces stomatal closure and accumulation of various osmoprotectants and proteins for osmotic adjustment. Moreover, the accumulation of ABA under salt stress helps mitigate the toxic effect of salinity on photosynthesis, growth, and other physiological functions. Additionally, it prompts the accumulation of K+ , Ca2+ , and compatible solutes such as proline and sugars in root cells, thereby counteracting the uptake of Na+ and Cl− which ultimately protects the plants from ruthless impacts of salt stress (Atia et al., 2018). Under salt stress, GA enhances seed germination and improves salt tolerance in plants by reducing stomatal resistance of leaves and accelerating transpiration and water usage efficiency (Yang et al., 2014). The stress hormone ethylene can positively or negatively influence stress tolerance in plants. Acetyl-CoA synthetase (ACS) is important for ethylene biosynthesis, and the up-regulation of ACS genes is essential for ACC biosynthesis. Regulation of these genes occurs at both transcriptional and post-transcriptional level. Subsequently, it was reported by Atia et al. (2018) that high salinity induced the expression of stress-responsive ACS genes and the synthesis of ethylene, increasing salt tolerance in plants. Likewise, CKs are involved in responses to various environmental stresses, including salinity stress. They have been reported to increase salt stress tolerance in plants via seed priming, and they are mainly produced in plant roots and are transported via xylem vessels to the shoot system where they regulate growth and developmental processes in plants. Under salt stress, the endogenous CK level in plants decreases significantly as a consequence of a sharp decrease in CK biosynthesis. This alters the gene expression pattern in plants, thereby eliciting appropriate responses to stress conditions (Ryu and Cho, 2015). Recent reports revealed that genetic engineering of CKs has been able to successfully control CK content in plants, thereby increasing crop yield and improving plant adaptaˇ zkov´ tion to salt stress (Ziˇ a et al., 2015; Prerostova et al., 2017). Salicylic acid (SA) plays a significant role in plant responses to abiotic environmental stresses (Miura and Tada, 2014). Exogenous application of SA alleviates salinity-induced inhibition in plant growth and increases photosynthetic activity and leaf Na+ , Cl− ,

51

and H2 O2 concentrations, thereby improving plant tolerance to salt stress (Khan et al., 2010; Nazar et al., 2011). Some reports have suggested that pre-treatment of different agriculturally important crops with SA increases ABA accumulation in plants, thereby improving plant tolerance to salt stress (Miura and Tada, 2014). Salt sensory pathways can be linked to various stress tolerance responses. The TF family genes that include bZIP, WRKY, APETALA2/ethylene response factor (AP2/ERF), MYB, bHLH, and NAC are expressed differently in response to salt stress (Srivastava, 2017). Moreover, certain genes have the ability of autophagy that enables plants to scavenge oxidized proteins and regulate ROS levels under salinity stress. Some of these ATG genes (such as AtATG8) involved in autophagocytosis were reported to respond to salt stress in order to increase stress tolerance in plants (Forni et al., 2017). Studies have shown that the overexpression of LEA-like stress proteins encoded by COR genes in plants showed higher salt tolerance in comparison to wild plants (Xu et al., 1996). Under salt stress, stress-induced overexpression of CBF3 under the control of RD29A promoter resulted in an enhanced expression of COR genes that are responsible for increasing osmotic stress tolerance in plants (Kasuga et al., 1999). Thus, we can conclude that LEA-like stress proteins are responsible for providing protection to plants under salt stress. Moreover, salt stress also induces the expression of stress-responsive genes such as NHX1, SOS1, BZ8, SAPK2, and SNRK2, known to play a crucial role in enhancing stress tolerance in plants. For example, NHX1 and SOS1 genes were reported to participate in Na+ /H+ exchange by reducing cellular Na+ concentration under salt stress. Similarly, the SAPK2 gene is responsible for regulating salt stress acclimatization, ion homeostasis, growth, and development of plants (Chakraborty et al., 2015). Salt stress tolerance induced by PGPR Salinization is the most destructive environmental threat influencing a billion hectares of land on a worldwide scale (Egamberdieva and Lugtenberg, 2014). Continuous osmotic stress influences the reproductive processes in plants and causes slow emergence of new leaves and decrease in flowering and fruiting rate (Santner and Estelle, 2009). Plant health in salinized soils can be improved with the use of microbial inoculants (Lugtenberg et al., 2013). These microbial inoculants produce IAA, gibberellins, and other phytohormones that increase root length, root surface area, and the

52

number of root tips in plants (Egamberdieva and Kucharova, 2009), which ultimately helps in regulating plant nutrient contents and balancing ion influx in plants under salt stress (Grover et al., 2011). Table II lists the roles of PGPR in salinity stress alleviation via alteration in morphological, physiological, and molecular traits of the host plant. Production of auxin is a common trait of PGPR and is believed to be a strong alleviator of salt stress in plants. Auxin is also an important plant growth regulator responsible for several cellular functions, including vascular tissue differentiation, lateral and adventitious root initiation, stem and root elongation, and orientation of root and shoot growth in response to light and gravity (Glick, 1995). In combination with plants’ endogenous IAA pool, PGPR stimulates plant cell growth and proliferation. Auxinproducing PGPR strains surviving under saline stress were found to maintain root and leaf growth rates in plants. This is because of the additional auxin produced by PGPR which is being transferred to the surrounding rhizosphere (Albacete et al., 2008). Similarly, Egamberdieva (2009) reported that priming of wheat plants with IAA-producing Pseudomonas strains (P. extremorientalis TSAU20, P. aurantiaca TSAU22, and P. extremorientalis TSAU6) resulted in a significant increase in root and shoot growth of wheat seedlings by 40% and 52%, respectively (100 mmol L−1 of NaCl concentration) compared with the control plants. Sadeghi et al. (2012) reported that priming of wheat plants with IAA-producing Streptomyces isolate enhanced the growth of wheat plants under salt stress. They observed that auxin level significantly increased after addition of salt to the culture medium and that it can be used as a potent bio-fertilizer under saline conditions. The reports put forth by Yao et al. (2010) signified the efficiency of PGPR strains in balancing the level of phytohormones released by plants in order to enhance their stress tolerance. They reported that inoculation of PGPR strain Pseudomonas putida Rs-198 resulted in increased production of endogenous IAA, promoting the growth of cotton seedlings growing under salt stress. Apart from the aforementioned Pseudomonas spp., some of the Bacillus strains can also enhance plant growth under stressed conditions. Bacillus amyloliquefaciens SQR9 was reported to enhance salt tolerance in maize seedlings growing in salinized soil. The bacterial inoculation resulted in increased chlorophyll, glutathione, and total sugar contents as well as peroxidase and catalase activity and the K+ /Na+ ratio (Chen et al., 2016). It was recently reported that priming of IAA-producing Pseudomonas knackmussii

M. GOSWAMI AND S. DEKA

MLR6 to Arabidopsis thaliana increased plant growth and reduced oxidative damages caused by salt stress compared to control plants (Rabhi et al., 2018). Studies observed a promising nature of PGPR in reducing the increased levels of plant ACC by taking up ACC directly from plant roots and converting it to α-ketobutyrate and ammonia. This causes a decrease in ethylene content in plants, which could otherwise cause severe damage to plants (Botella et al., 2000; Bianco and Defez, 2009; Pliego et al., 2011). It was reported that bacterial ACC deaminase plays a crucial role in enhancing the growth of several crop plants grown under salt stress (Mayak et al., 2004a; Siddikee et al., 2010; Bal et al., 2013). Saravanakumar and Samiyappan (2007) reported that priming of groundnut seedlings with ACC-containing PGPR strain Pseudomonas fluorescens TDK1 promoted plant growth and stress tolerance in salt-affected plants in comparison with groundnut seedlings primed with ACClacking Pseudomonas strains. Similarly, Shahzad et al. (2010) observed that application of ACC-containing rhizobacteria in salt-stressed crops led to an increase in the number of lateral roots, lateral root length, and dry root weight (Shaharoona et al., 2006). Egamberdieva et al. (2013) reported that inoculation of Pseudomonas trivialis 3Re27 to goat’s rue plants (Galega officinalis) increased salt tolerance in salt-affected plants by promoting root and shoot growth. Priming of pepper plants with Bacillus sp. WU5 promoted the growth of pepper seedlings in terms of increased fresh weight, dry weight, shoot length, and root length in comparison to the uninoculated plants under saline conditions (Wang et al., 2018). Cheng et al. (2007) monitored the growth of canola plants inoculated with either wild-type Pseudomonas putida UW4 or a mutant of this strain lacking ACC deaminase. They observed that the addition of wild-type strains significantly increased the growth of canola plants in comparison to the mutant strains. Similarly, Ali et al. (2014) observed that plants pre-treated with ACC deaminasecontaining wild-type PGPR endophytes (Pseudomonas fluorescens YsS6 and Pseudomonas migulae 8R6) were healthier and grew much bigger compared to those pretreated with ACC deaminase-deficient mutant strains. Another plant stress hormone, ABA acts as an endogenous signaling molecule that increases resistance in plants for surviving adverse environmental conditions, particularly salinity and drought. Plants exposed to salt stress initiates a proportional increase in endogenous ABA level, thereby helping plants to acclimatize to high salt concentrations in roots, xylem sap, and shoots (Ryu and Cho, 2015) and to a concomitant

PLANT GROWTH-PROMOTING RHIZOBACTERIA

53

TABLE II Roles of growth-promoting rhizobacteria (PGPR) in alleviation of salinity stress and enhancement of stress tolerance in plants PGPR

Plant

Changes in plant morphological, physiological, or molecular traits

Reference

Pseudomonas aeruginosa T15, Pseudomonas fluorescens NT1, and Pseudomonas stutzeri C4 Azospirillum brasilense

Tomato (Lycopersicum esculentum)

Increased root and shoot length with decreased endogenous ethylene levels

Tank and Saraf, 2010

Maize (Zea mays)

Increased Na concentration and decreased K+ /Na+ ratio and calcium concentration Enhanced 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity and nutrient uptake by the plant Enhanced induced systemic tolerance (IST) in plants with production of ACC deaminase Increased growth and germination by increase in absorption of Mg2+ , Ca2+ , and K+ Improved growth, photosynthesis rate, mineral content and antioxidant enzyme system of the plant Enhanced root branching and increased secretion of flavonoids and lipochitooligosaccharides Increased root length and dry weight by 47% and 50%, respectively

Hamdia et al., 2004 Kohler et al., 2009 Mayak et al., 2004a Yao et al., 2010 Golpayegani and Tilebeni, 2011 Dardanelli et al., 2008 Egamberdieva, 2011

Cotton

Increased dry weight of roots and shoots

Egamberdieva and Jabborova, 2013

Radish (Raphanus sativus) Cotton Citrus (Citrus macrophylla)

Increased fresh and dry weight of both shoot and root as well as chlorophyll content Increased plant height and dry weight Decreased transpiration rate and stomatal conductance in plants with significant drop in the levels of abscisic acid (ABA) and salicylic acid (SA) and increased plant growth Increased plant height, fresh and dry weight, and total chlorophyll content as well as an increase in total sugar and proline contents

Yildirim et al., 2008 Yue et al., 2007 Vives-Peris et al., 2018

Eggplant (Solanum melongena L.)

Alleviated salt stress effects in eggplants by increasing the K+ /Na+ ratio and K+ -Na+ selectivity in the eggplants and promoting plant growth and productivity

Abd El-Azeem et al., 2012

Faba bean (Vicia faba L.)

Enhanced plant height (10.66%), shoot fresh weight (9.52%), and plant leaf area (61.86%) as well as proline content

Metwali et al., 2015

Pseudomonas mendocina Palleroni Achromobacter piechaudii ARV8 Pseudomonas putida Rs 198 Pseudomonas sp. and Bacillus lentus Azospirillum brasilense Pseudomonas chlororaphis TSAU13 and Pseudomonas extremorientalis TSAU20 Pseudomonas alcaligenes PsA15, Pseudomonas chlororaphis TSAU13, Pseudomonas extremorientalis TSAU20, and Bacillus amyloliquefaciens BcA12 Staphylococcus kloosii and Kocuria erythromyxa Klebsiella oxytoca Pseudomonas putida KT2440 and Novosphingobium sp. HR1a Microbacterium oleivorans KNUC7074, Brevibacterium iodinum KNUC7183, and Rhizobium massiliae KNUC7586 Xanthobacter autotrophicus BM13, Enterobacter aerogenes BM10, and Bacillus brevis FK2 Pseudomonas putida, Pseudomonas fluorescens, and Bacillus subtilis

Lettuce (Lactuca sativa) Pepper (Capsicum annuum L.) and tomato Cotton (Gossypium hirsutum) Basil (Ocimum basilicum) Bean (Phaseolus vulgaris) Bean

Pepper

decrease in transpiration rates (Albacete et al., 2008). While there are several reports describing the production of ABA by PGPR, there is minimal information documenting the influence of exogenously produced bacterial ABA on plants in comparison to plant produced ABA under drought conditions. Naz et al. (2009) reported that application of ABA-producing PGPR to salt-affected soybean seedlings under in vitro conditions resulted in a significant improvement

Hahm et al., 2017

in growth and nutritional status of inoculated plants. Similarly, Cohen et al. (2015) observed that inoculation of ABA-producing Azospirillum brasilense to Arabidopsis seedlings promoted plant growth through modifications in host root architecture and stimulation of photosynthetic pigments. On the other hand, Kang et al. (2014a) observed that priming of cucumber plants with ABA-producing microbial consortium of Burkholderia cepacia SE4, Promicromonospora sp.

54

SE188, and Acinetobacter calcoaceticus SE370 decreased ABA levels in plants, thereby defending them from severe damage caused by salt stress. Similarly, priming of ABA-producing Bacillus amyloliquefaciens H-2-5 to soybean plants suppressed the salt-induced stress effects by reducing ABA levels (Kim et al., 2017). Gibberellins or GA are important plant growth regulating hormones. They play a crucial role in seed dormancy as well as in the formation of floral organs and lateral shoot growth (Olszewski et al., 2002). Gibberellin-treated crop plants showed increased water uptake and reduced stomatal resistance when grown under salt stress conditions (Maggio et al., 2010). It was reported that under saline conditions, exogenous application of GA increased germination and growth rate of plants (Ahmad, 2010; Manjili et al., 2012). Additionally, GA exhibits crosstalks with other hormones that mediate tolerance mechanisms in plants growing under stressed conditions (Wolbang et al., 2004). It was reported that exogenous application of gibberellins to salt-stressed plants led to significant increase in fruit yield, leaf area, nitrogen, phosphorus, and potassium uptake along with significant increase in plant osmotic components (Khan et al., 2004). Similarly, Kang et al. (2014b) observed that priming of soybean plants with gibberellin-producing rhizobacterium Pseudomonas putida H-2-3 increased the growth of soybean plants under salt and drought stress conditions. They also observed a significant increase in shoot length, fresh weight, and total chlorophyll content of soybean plants via up-regulation of stress hormones such as GA and antioxidants in the plants. In addition to phytohormone production, rhizosphere bacteria also produce osmolytes for helping the plants adapt to extremely saline conditions. Upadhyay et al. (2012) studied the effectiveness of PGPR inoculation on wheat rhizosphere and observed that co-inoculation of Bacillus subtilis and Arthrobacter sp. enhanced the growth of wheat plants, causing a significant increase in dry biomass, soluble sugars, and proline content. The role of osmoprotectants in alleviating salt stress was further studied by Jha et al. (2011). They observed that co-inoculation of Pseudomonas pseudoalcaligenes in combination with a rhizosphere bacterium Bacillus pumilus showed significant stress tolerance potential in plants via production of osmoprotectants and antioxidants at initial stages of plant growth. Individual inoculation of Pseudomonas pseudoalcaligenes resulted in an increased level of quaternary compounds (glycine-betaine) and shoot biomass at lower salinity levels, whereas at higher salinity levels, co-inoculation of two PGPR strains,

M. GOSWAMI AND S. DEKA

Pseudomonas pseudoalcaligenes and Bacillus pumilus, showed prominent stress-alleviating results. Similarly, priming of chickpea plants with Bacillus subtilis (BERA 71) significantly enhanced plant growth via modulation in the antioxidant system, thereby eliminating salt-induced oxidative damage in plants (Abd-Allah et al., 2018). Similarly, antioxidants play a notable role in relieving salt stress in plants (Jha and Subramanian, 2016). Upadhyay et al. (2012) reported that inoculating salt-affected wheat plants with Bacillus subtilis SU47 and Arthrobacter sp. SU18 increased the overall growth of the plants. They observed that inoculation of PGPR strains decreased antioxidant enzyme activity in wheat leaves, most notably the activity of CAT, thus alleviating the negative effects imposed by salt stress. In conclusion, they suggested that co-inoculation with Bacillus subtilis and Arthrobacter sp. could alleviate the adverse effects of soil salinity on wheat growth. In a similar context, the role played by bacterial EPS in stress alleviation is noteworthy. In general, salinity stress causes an imbalance in ion influx in plants growing in salt-affected areas, but the application of EPS-producing PGPR strains results in a significant decrease in Na+ and increase in K+ content, thereby alleviating salt stress experienced by the plants. These strains bind Na+ ions and decrease the levels of Na+ ion uptake by plants (Nadeem et al., 2010; Kang et al., 2014a). However, several studies reported the efficiency and potential of Pseudomonas sp. for alleviating salinity stress in plants growing in salt-affected areas. These bacteria protect their host plants against negative impacts of salt stress by decreasing Na+ ion uptake. Yao et al. (2010) reported that inoculation of Pseudomonas putida Rs-198 selectively increased Ca2+ , K+ , and Mg2+ uptake and decreased Na+ uptake by plants, thereby protecting the plants against negative impacts of salt stress. Molecular studies revealed the upregulation of several stress-responsive genes in plants viz. RBCS, ribulose-1,5-bisphosphate carboxylase oxygenase subunits (RBCL), H + -PPase (encoding H+ -pumping pyrophosphatase), HKT1, NHX1, NHX2, and NHX3 in conditions of salinity stress. As observed by Chen et al. (2016), some of the stress-responsive genes are upregulated, while others are downregulated to allow the plants to survive the harsh environmental conditions. They focused on 9-cis-epoxycarotenoid dioxygenase (NCED) expression in maize plants as it is the key enzyme in the biosynthesis of ABA in plants. Both upregulation and downregulation of NCED gene were reported to have a direct impact on ABA synthesis

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(Sun et al., 2012) and thus play a crucial role in stress alleviation as well as in increasing stress tolerance in plants. Although in many cases the overexpression of NCED increased stress tolerance in plants, in case of the research done by Chen et al. (2016), the inoculation of Bacillus amyloliquefaciens SQR9 strain to maize plants increased salinity tolerance in maize plants via down-regulation of NCED gene expression. Tolerance induced in the maize plants was also a result of stable maintenance of Na+ homeostasis. Priming of Arabidopsis thaliana with Burkholderia phytofirmans PsJN resulted in high tolerance of inoculated plants to salt stress in comparison with the control plants. This was a result of changes in the expression pattern of genes associated with ion homeostasis (KT1, HKT1, NHX2, and SOS1) induced by Burkholderia phytofirmans PsJN (Pinedo et al., 2015). Similarly, a halophyte grass Puccinellia tenuiflora primed with Bacillus subtilis GB03 showed less Na+ accumulation while upregulating the expression of PtHKT1 and PtSOS1 genes to increase stress tolerance under high salt concentration (Niu et al., 2016).

ditions has not been explored in detail. Moreover, the explanation of the underlying mechanism in the alleviation of abiotic stress by PGPR needs to be better elucidated and a lot more needs to be unveiled about PGPR-mediated stress tolerance in plants.

CONCLUSIONS AND FUTURE PERSPECTIVES

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The rhizosphere colonizing PGPR strains are capable of enhancing stress tolerance in plants under different abiotic stresses. Change in root morphology is one of the important physiological mechanisms that can improve water and nutrient uptake in plants in harsh edaphic conditions. This results in enhanced plant growth as a consequence of increased synthesis of osmolytes or osmoprotectants along with manipulations in levels of phytohormones via production of bacterial-associated growth hormones. The research that has been recognized so far offers a broad picture of the abiotic stresses and their effects on plant growth. Moreover, the defensive strategies adopted by the plants in order to acclimatize to the stressed conditions have been discussed and published extensively. Still, the beneficial and ameliorative effects of PGPR involving the highly complex and intriguing mechanisms associated with stress alleviation remained speculative. In-depth knowledge of the PGPR-associated mechanisms is highly essential for contributing to the development of PGPR-mediated ameliorative strategies for abiotic stress. Certain root architecture changes induced by PGPR are important for increasing stress tolerance in plants and thus require detailed research. In addition to this, the manipulative effect of PGPR on phytohormone production in plants grown under stressed con-

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ACKNOWLEDGEMENTS The authors are very grateful to the Director of the Institute of Advanced Study in Science and Technology (IASST), Guwahati, India, for providing the necessary facilities as well as to the Department of Science and Technology (DST) for providing financial assistance as a Senior Research Fellow. The authors would like to acknowledge Dr. Pranjit Bora, Assistant Professor, Department of English, Dibrugarh University, for his professional help in editing the manuscript to improve writing quality. Moreover, the authors would like to thank Dr. Kaustuvmani Patowary, Research Associate, Division of Life Sciences, Institute of Advanced Study in Science and Technology, for his help in organizing the manuscript.

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