Rhizospheric Microbial Diversity: An Important Component for Abiotic Stress Management in Crop Plants Toward Sustainable Agriculture

C H A P T E R

9 Rhizospheric Microbial Diversity: An Important Component for Abiotic Stress Management in Crop Plants Toward Sustainable Agriculture Deepika Goyal*, Om Prakash†, and Janmejay Pandey* *Department of Biotechnology, School of Life Sciences, Central University of Rajasthan, Ajmer, India † Microbial Culture Collection, National Centre for Cell Sciences, Pune, India

O U T L I N E 9.1 Introduction

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9.2 Environmental Stress and Their Impact on Agriculture

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9.3 Strategies Implemented by Plants Against Abiotic Stress

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9.4 Technical Interventions for Abiotic Stress Tolerance 9.4.1 Pesticides and Fertilizers 9.4.2 Seed Priming 9.4.3 Transgenic Plants

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9.5 Microorganisms in Plant Stress Management 9.5.1 PGPR in Abiotic Stress Management 9.5.2 Secretion of Phytohormones by PGPRS 9.5.3 Production of Volatile Compounds 9.5.4 Potassium and Phosphate Solubilization 9.5.5 Nitrogen Fixation 9.5.6 Secretion of ACC Deaminase 9.5.7 Secretion of Antibiotics/Inhibitory Substances

New and Future Developments in Microbial Biotechnology and Bioengineering https://doi.org/10.1016/B978-0-444-64191-5.00009-2

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9.6 PGPRs Usage: Status and Recommendations 9.7 Rhizospheric Microbial Community: Significance in Plant Stress Management 9.7.1 Influence of Host Plant on Rhizospheric Microbial Community 9.7.2 Influence of Rhizospheric Microbial Community on Host Plant Growth and Survival 9.7.3 Rhizospheric Microbial Community Engineering for Plant Stress Management

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9.8 Future Directions in Rhizosphere Microbiome Engineering in Sustainable Agriculture 129 9.9 Conclusions

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References

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Further Reading

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© 2019 Elsevier B.V. All rights reserved.

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9.1 INTRODUCTION Plant in general and crop plants in particular are often exposed to a plethora of biotic and abiotic stresses that result in loss of productivity and economic losses all around the world. Such losses are significantly more pronounced in developing and underdeveloped countries wherein agriculture practices with respect to abiotic stress management are rather inadequate. According to the recent report on “Global Food Security Index” published by The Economist Intelligence Unit; “The global food security has improved in past few decade, due to increased agriculture production and resulting reduced food prices, yet with existing socioeconomic and political trends, the continued progress with respect to global food security may not be a foregone conclusion” (https://foodsecurityindex.eiu.com/). Along with the challenges posed by the global warming and water-level depletion, the challenge for ensuring food security has been widely acknowledged as the most important global challenge faced by the human kind in the present times (Brown et al., 2017; Sammugam and Pasupuleti, 2018). In view of this and other similar predictions, it is an important technical challenge for agriculture science community to develop and facilitate programs for adaptation of crop plants with ability to survive and exhibit robust growth under niches marred with harsh environmental conditions and abiotic stresses (e.g., high temperatures, draught, salinity, pathogens, nutrient limitation, and other climatic disasters) and render agronomic capabilities for sustained agriculture (Wagner, 1999; Wang, 2009; Beddington, 2010). The conventional stress management systems used for the protection of plants and crops against biotic and abiotic stresses involve the widespread use of pesticides and fertilizers ( Jayaraj et al., 2016). Each of these group of chemicals provide protection against stress and enhance the survival and growth of plants under stress conditions as they provide protection against attack by potential microbial pathogens and nutrient limitations, respectively. Since most of the pesticides and fertilizers are anthropogenic in nature, they often impart adverse effect on various life forms exposed to them including the human beings ( Jayaraj et al., 2016; Karami-Mohajeri et al., 2017). Consequently, their application for agricultural practices is being gradually curtailed all over the world (The, 2017). In addition, during recent past, specifically since advent of the Recombinant DNA Technology and Transgenic Technology, several studies have been carried out to develop biotic and abiotic stress-resistant transgenic crop varieties to mitigate the potential damages caused by the biotic and abiotic stresses (Nicolas et al., 2014; Kikuchi et al., 2015; Ahanger et al., 2017; Ali et al., 2017; Liang et al., 2018). However, the use stress-resistant transgenic crop(s) has not been widely accepted due to various ethical issues pertinent to their development and environmental release (Rehmann-Sutter, 1993; Weale, 2010; Bawa and Anilakumar, 2013; Rastogi Verma, 2013). This situation presents a unique opportunity for exploration and exploitation of alternative plant stress mitigation mechanisms such as (i) plant-microbe interaction, (ii) allelopathy, etc. The plant-microbe interaction going on within the rhizospheric regions has been accepted for long to be critical for overall growth and productivity (Berg et al., 2014, 2016; Braga et al., 2016; Bandyopadhyay et al., 2017). Consequently, several studies have been carried out with the objective of isolation and characterization of bacterial strains from the rhizosphere of various plant species from diverse regions and ecosystems all over the world (Adair et al., 2017; Larousse et al., 2017; Montanari-Coelho et al., 2018; Wille et al., 2018). Noticeably, the characterization of rhizospheric bacterial has led to common understanding that a many rhizospheric bacteria have the potential to promote the growth of plants by improving the nutrition bioavailability and elimination of harmful pathogens. Furthermore, many of the isolated bacterial strains capable of promoting plant growth have also been characterized for their taxonomic characteristics as well as their mode of action for plant growth promotion (Vimal et al., 2016, 2017, 2018; Singh and Seneviratne, 2017a, b; Tiwari and Singh, 2017). Results presented in such studies indicated that most of the characterized strains are capable of enhancing bioavailability of limited nutrients (e.g., nitrogen, phosphorus) which results in promotion of the plant growth. Consequently, rhizospheric bacteria that are capable of promoting plant growth are collectively referred to as “plant growthpromoting rhizobacteria” (PGPR). Till date, a number of PGPR isolates have been isolated from diverse ecological niches all over the world and many of them have been successfully tested for their application in improvement of plant growth under laboratory-based trial or small field studies. Diverse places such as deserts, hot springs, mountains, etc. provide promising opportunities for finding bacteria with unique temperature, salinity, and alkalinity tolerance. Most of the studies in the literature deal with isolation of PGPRs from crop plants growing under normal and harsh environmental conditions. The emphasis is on the isolation and characterization of a single microbial strain with multiple plant growth-promoting capabilities and the development of consortia or mixtures of microorganisms each having at least one beneficial trait. Large-scale initiatives such as Pan-European Rhizosphere Resource Network (PERN) and other transnational repository of microorganisms have been presented for coordinating accessibility and availability of thousands of useful microbial taxa. The next step in implementation would be to produce them in large quantities using cost-effective ways. There is a lack of information on effective process development strategies for PGPRs. Consequently, the potential of PGPR

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technology is yet to be fully exploited. As indicated above, the current state of the art with regards to PGPR technology fits well within the reductionist and purist approach of isolating single pure bacterial strains and their subsequent application, however, this approach essentially undermines the significance of wide range of intraspecies and interspecies interactions that occur amongst the rhizospheric bacteria or plant-rhizospheric bacteria that may significantly contribute or even be necessary for the effectiveness of the PGPR functions (Kremer et al., 1990; Mayak et al., 1999; Galleguillos et al., 2000; Bloemberg and Lugtenberg, 2001). It is critical to understand that although fertilizers, pesticides and PGPR isolates (in case of a few discreet examples) have been successfully used for providing protection to the growing plants against nutrient limitation and attack by pathogens and enhancing their growth and survival under stress conditions (Erceg et al., 1990; Pretty, 2008; Dastager et al., 2010; Dodd and Perez-Alfocea, 2012; Sharma et al., 2016; Dias et al., 2017; Lojan et al., 2017; Pham et al., 2017; Qin et al., 2017), yet the most significant opportunity for progress in abiotic stress management for plants, however, lies in developing a comprehensive understanding pertaining to (i) composition and dynamics of rhizospheric microbial diversity; (ii) the metabolic potential of rhizospheric microbial diversity; and (iii) intraspecies and interspecies interactions occurring within the rhizosphere (including interactions amongst the microbial diversity and the host plant counterpart) (He et al., 2017; Nunan et al., 2017; Tuskan et al., 2017; Wu et al., 2017a, b; Yang and Wang, 2017; Durand et al., 2018; Fonseca et al., 2018; Ling et al., 2018; Luo et al., 2018; Moissl-Eichinger et al., 2018; Zhou et al., 2018). In not so distant past, characterization of non-cultivable microbial diversity was regarded to be a difficult proposition; however, with recent advances in field of “culture-independent characterization of bacterial diversity” it is now possible to not only determine the composition, diversity, and dynamics of microbial communities but also to utilize their genetic resources through cloning and heterologous expression of the gene(s)/gene cluster(s) associated with non-cultivable microorganisms (Mahenthiralingam et al., 2006; Hassa et al., 2018). Furthermore, with the development of “metatranscriptomics,” the understanding of transcriptionally relevant genetic resource associated with noncultivable microbial diversity is set to improve in the near future (Turner et al., 2013; Chaparro et al., 2014). Although the application of metagenomic/metatranscriptomic methodologies for characterization of plant rhizospheres is still rather nascent, yet results obtained with few initial studies have indicated that the total microbial community structure and dynamics may play a pivotal role in determining the efficacy of the plant growth promotion functions. It is speculated that rhizospheric microflora may help plant growth via not only improving the availability of nutrition and resources, but also by mitigating the abiotic stresses encountered by the concerned plant (Graner et al., 2003; Johri et al., 2003; Haldar and Sengupta, 2015). This chapter attempts to present a comprehensive account of existing state-of-the-art information with regards to the “plant stress response” and complement its review of recent research studies carried out with regards to total microbial diversity of rhizospheric regions and highlight findings which indicate that rhizospheric microbial diversity is an important component for abiotic stress management in crop plants and consequently for ensuring sustainable agriculture.

9.2 ENVIRONMENTAL STRESS AND THEIR IMPACT ON AGRICULTURE Crop plants growing in the fields face tough physical and biological environmental factors that adversely affect their growth and productivity (Singh, 2015a, b, c, d). Stresses caused by the physical environment, viz., climatic conditions and soil characteristics are termed as abiotic stress. These include drought, salinity, heat, cold, chilling, freezing, nutrient limitation, high light intensity, heavy metal contamination, ozone (O3), and anaerobic conditions (Brown et al., 2017; Hasan et al., 2017; Kumar and Verma, 2018; Lata et al., 2018). Stresses caused by biological agents constitute the biotic stresses and they include infection by pathogens (including bacteria, fungi, viruses, and nematodes) and attack by herbivore pests collectively. According to the reports published by the United Nations Office for Disaster Risk Reduction, the world has lost 1.4 trillion dollars worth of crops between 2005 and 2015, due to the natural disasters like draught, flooding, storms, cyclones, etc. In a similar study carried out by the National Center of Environment, USA, it was reported that crop losses due to environmental stresses between 1980 and 2014 exceeded a billion dollars each year. This report highlighted that drought alone caused combined agricultural losses of more than 200 billion dollars (http://www. ncdc.noaa.gov/billions/events). Another report released by the Food and Agriculture Organization (FAO), USA in 2015 indicated that an estimated total $140 billion losses were caused by 78 natural disasters in 48 developing countries between 2003 and 2013. Noticeably, as much as 22% of these losses (i.e., $30 billion) were directly related to the agricultural sector including crops, livestock, forestry, and fisheries (http://www.fao.org/3/a-i4434e.pdf).

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The environmental stresses impart their adverse effect on plant growth by inhibiting various physiological functions such as seed germination, seedling growth, root development and root system architecture (RSA), photosynthetic machinery, stomatal conductance, chloroplast structure and reproductive tissue development, etc. (Mittler, 2006; Suzuki et al., 2014). A number of studies have specifically characterized the effects of selective abiotic stresses, for example, drought, heat, and their combination on the growth and physiological traits of different plants and crops. Drought primarily causes a decrease in plant height, spike number, and grain weight (Lawas et al., 2018). By contrast, heat stress causes an increase in aborted spikes and a decrease in grain numbers. In reproductive tissues, drought primarily impacts pistil development, whereas heat stress primarily impacts pollen development (De Storme and Geelen, 2014; Muller and Rieu, 2016; Arshad et al., 2017). Similarly, roots are also extremely sensitive to changes in their surrounding microenvironment and changes in RSA have been reported to be adversely effected by abiotic stress such as increased temperature, salinity or alkalinity, decreased water content or nutrient availability, heavy metal toxicity (Schutzendubel and Polle, 2002; Clemens and Ma, 2016). Abiotic stresses have also been reported to impair the photosynthetic machinery in plants. The direct impact of abiotic stress on the photosynthetic activity is reported as disruption of all photosynthesis components such as photosystem I and II, electron transport, carbon fixation, adenosine triphosphate (ATP) generating system and stomatal conductance, etc. (Nouri et al., 2015). It is also speculated that abiotic environmental stresses may also alter the ultrastructure of cellular organelles like chloroplasts, cause changes in thylakoid complexes, and can alter the concentration of various pigments and metabolites. Apart from the abovementioned adverse effects, the abiotic stresses have also been reported to lead to generation of reactive oxygen species (ROS). For example, hypersaline environments with high salt concentrations lead to reduced uptake of essential nutrients which in turn causes loss of photosynthetic pigments. With loss of photosynthetic pigments, the photosynthetic process is abolished and stomata are closed. This in turn leads to reduced carbon dioxide availability in the leaves and inhibits carbon fixation, exposing chloroplasts to excessive excitation energy causing the • generation of ROS including superoxide (O•– 2 ), hydrogen peroxide (H2O2), hydroxyl radical (OH ), and singlet oxygen 1 ( O2). ROS are highly reactive and cause cellular damage through oxidation of lipids, proteins, and nucleic acids. Under ROS stress, the spatial configurations of various membrane proteins or enzymes are disturbed, leading to increased membrane permeability and ion leakage, chlorophyll destruction, metabolism perturbations, and even severe injury or death of plants (Parihar et al., 2015; Lopez-Raez, 2016). Abiotic stresses that cause most adverse effect to plant growth, viz., salinity and draught are mediated through the mechanism of decreased availability of water; which in turn causes the imbalances between nonenzymatic electron transport reactions and enzymatic reactions (Krebs cycle and Calvin cycle) in chloroplasts and mitochondria. In addition, when plants suffer from exposure to salinity and drought stress conditions, the dynamic equilibrium for intracellular generation and removal of ROS is broken and the excessive accumulation of ROS damages cells and the oxidative deterioration may ultimately lead to cell death (Parihar et al., 2015; Lopez-Raez, 2016). Similar effects are also observed in case of plants getting exposed to excessive high and low temperatures. In addition to the adverse effects mentioned above, the excessive heat also causes denaturation of proteins which is deleterious to most of the cellular functions and thus the survival of the cells (Bosl et al., 2006; Sharma et al., 2009). Another major abiotic stress encountered by plants is due to the exposure to heavy metal contaminants. Intuitively, heavy metal exposures are reported to cause greater detrimental effect on plant growth when combined with other abiotic stresses. Growth inhibition has been observed in both the shoot and root of different plants on exposure to nickel, cadmium, mercury, etc. (Kong et al., 1995; Sethy and Ghosh, 2013). The underlying mechanism of heavy metal exposure induced stress is not yet fully understood, yet it is commonly suggested that heavy metal exposure leads to depletion of GSH which may be a critical step in heavy metal-induced stress. Plant cultivars with improved capacities for GSH synthesis displayed higher tolerance. Furthermore, when not detoxified rapidly enough, heavy metals may trigger disturbance of redox control of the cell leading to a cascade of reactions leading to growth inhibition, stimulation of secondary metabolism, and finally the cell death (Zenk, 1996; Zhang and Shu, 2006; Jozefczak et al., 2012). On one hand, it observed that different abiotic stress induce different adverse effects on crop plants; similarly on the other hand, it is also observed that crop plants differ quite distinctly in their ability to tolerate abiotic stresses. For example, among the major food crops globally, barley, cotton, sugar beet, and canola are observed to be the most tolerant toward common abiotic stresses; bread wheat is moderately tolerant while rice and most legume species are sensitive to such stresses (Tolmay, 2001; Goel et al., 2017). The varying degree of tolerance of different crops to abiotic stress is suggested to be an outcome of several factors including: (i) genetic adaptation of the plant, (ii) interaction of the plant with other biotic components, for example, endophytic or rhizospheric bacteria, etc. The role of genetic adaptation in tolerance of the plants toward abiotic stresses such as draught and salinity has been demonstrated in large number studies related to characterization of molecular mechanism of tolerance, identification of gene(s) specifically

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overexpressed during the abiotic stress, and generation of stress tolerant transgenic plants of several model plants and crops such as Arabidopsis, wheat, rice, canola, etc. (Hirayama and Shinozaki, 2010; Shelp et al., 2012; Mickelbart et al., 2015) Similarly, the significance of plant-microbe interaction in stress tolerance has also been reported in a number of studies, wherein pretreatment of plant seed or seedling with suspension of well-characterized PGPRs results in improved survival. It is imperative to mention that the varying ability of plants to tolerate abiotic stress might involve other factors that are not yet characterized/understood. Therefore, there is an opportunity for studies that would aim at identifying other components of the tolerance toward abiotic stresses.

9.3 STRATEGIES IMPLEMENTED BY PLANTS AGAINST ABIOTIC STRESS The adaptation strategies that plants employ to circumvent the environmental stresses can be classified into two categories, viz., (i) stress avoidance and (ii) stress tolerance. Stress avoidance strategies are long-term adaptations of plants to their environment and they are mediated through mechanisms such as shorter life span, changes in leaf or stem or root morphology, etc. (Pierik and Testerink, 2014). Examples of stress avoidance also include shoot elongation away from the shade of neighboring plants, escape from submerged conditions to reach the air and root growth away from saline soil microsites or halo-tropism. These adaptations are relatively complex in nature and require multiple genes to be expressed (Pierik and Testerink, 2014). On the other hand, stress tolerance mechanisms are relatively simpler in terms of genetics involved. With respect to the time, the plant stress response is a dynamic process which includes several phases that could be distinguished as (i) alarm phase (lasting few hours); (ii) an acclimation phase (lasting few days); (iii) a resistance phase (lasting few weeks); (iv) an exhaustion phase (when stress lasts too long or is too severe), and (v) a recovery phase after a cessation of a stress factor which leads to an establishment of a novel homeostasis (Kosova et al., 2011). Each phase of plant stress responses is aimed at an establishment of novel homeostasis under altered environmental conditions and is therefore accompanied by profound alterations in plant cellular composition. The key pathway in plant stress management appears to be the antioxidant defense machinery. ROS are continually generated as a consequence of the normal metabolism in aerobic organisms. Growing evidence shows that the generation of reactive ROS is one of the most common plant responses to different stresses. Accumulation and release of ROS into cell take place in response to a wide variety of adverse environmental conditions including salt, temperature, cold stresses and pathogen attack, and among others (Fang and Xiong, 2015; Kosova et al., 2015). The signaling cascade that is activated on the signal perception of the stress causes activation of many stress-related genes that in-turn produce various biomolecules such as stress response proteins and enzymes, etc. that are directly involved in stress response or tolerance. Phytohormones also play a critical role in mediating plant defense responses (Verma et al., 2016). Several studies have shown that a sophisticated cross talk exists between elaborate signaling network and various phytohormones. Recent studies have provided considerable evidence for cross talk of abscisic acid (ABA), salicylic acid (SA), jasmonates (JAs), and ethylene (ET) with auxins, gibberellins (GA), cytokinins (CK) in regulating plant defense response. Typically, ABA is responsible for plant defense against abiotic stresses because environmental conditions such as drought, salinity, cold, heat stress, and wounding are known to trigger increase in ABA levels while ET, SA, and JA play a crucial role in response to biotic stress conditions namely pathogen infections (Nolan et al., 2017). Similarly, among the regulatory proteins, transcription factors (TFs) play a decisive role in the stress signal perception and stress-responsive gene expression by interacting with cis-acting elements present in the promoter region of various target stress-responsive genes in the signal transduction processes. Thus, they activate the signaling cascade of whole network of genes that act together in enhancing plant tolerance to the harsh environmental conditions. The important TF gene families that have been found to be involved in stress response include heat stress transcription factors (HSFs) and WRKY gene family (Gahlaut et al., 2016; Jiang et al., 2017). Some of the distinct and noticeable stress tolerance strategies that plants employ include: (i) enhanced biosynthesis of low-molecular osmolytes (proline, sugars, and betaines) and hydrophilic proteins like aquaporins, late embryogenesis adaptation (LEA) proteins to improve water retention; (ii) enhanced biosynthesis of ROS scavenging enzymes including superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione peroxidase (GPX), glutathione reductase (GR), glutathione S-transferase (GST), dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDAR), thioredoxin peroxidase (TPX), alternative oxidase (AOX), peroxiredoxin (PrxR/POD), etc., for peroxide homeostasis; (iii) downregulation of crucial photosynthetic enzymes; (iv) enhanced cell wall lignifications; (v) enhanced levels of ATP-dependent Na+/H+ transporters resulting in Na+ exclusion (through plasma membrane) or Na+ intracellular compartmentation (through tonoplast); (vi) enhanced accumulation of heat shock proteins; and (vii) enhanced levels of metal-chelating proteins (ferritin, phytochelatins, etc.) and pathways involved in their biosynthesis (Fang and Xiong, 2015; Kosova et al., 2015; Verma et al., 2016).

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It is not convincing to state that the abiotic stress tolerance mechanism followed by tolerant plants involves only the abovementioned mechanisms, as there might be a number of other mechanisms that are yet to be characterized and experimentally validated, yet the findings listed above have helped in the development and deployment of strategies for successful management of abiotic stresses encountered by the plants. Some of these strategies are in use for decades while others are relatively new. In the following paragraphs, we will describe these tools of stress management in detail.

9.4 TECHNICAL INTERVENTIONS FOR ABIOTIC STRESS TOLERANCE 9.4.1 Pesticides and Fertilizers Chemical compounds namely pesticides and fertilizers and have been used since decades to enhance growth and productivity of crop plants under normal and stressed environments. While pesticides are limited for alleviating biotic stress caused by the infection of pests and pathogenic microorganisms; the fertilizers are used to circumvent nutrient stress and various types of other abiotic stresses (del Pino et al., 2015; Wang et al., 2016c). Fertilizers containing essential nutrients and minerals are supplied to increase the concentration of these nutrients and minerals that are essential for plant growth and they are required in edible portions for the benefit of human health. There is clear cut evidence that an optimal supply of the nutrients and minerals is essential to improve the tolerance of plants against stresses of various kinds. For example, potassium is needed for the maintenance of low osmotic potential conditions in the plant roots. Low osmotic potential in roots is essential for enhanced water uptake under conditions of draught, high temperature, and increased salinity. Another noticeable example of essential nutrient for plant stress response is nitrogen (N) as it constitutes 1.5%–8% of plant dry matter and 16% of total plant protein. Despite the 80% N2 availability in atmosphere, plants are unable to use it directly due to the highly stable nature of molecular nitrogen (N2). Similarly, phosphorus (P) constitutes about 0.1%–0.5% of a plant’s dry weight and is a key component of nucleic acids, lipids, ATP, adenosine diphosphate (ADP), sugars, and further ATP involved in several energy-dependent cellular processes, for example, photo-, oxidative, and substrate-level phosphorylation. Under conditions of N and P deficiency, plants go through transcriptional, posttranslational response and accumulate high sugar which further stimulates sugar-signaling cascade to maintain homeostasis and energy demand. Starvation for N and P over a long duration leads to change in various plant metabolic processes including CO2 assimilation, photosystem II (PS-II) inhibition, downregulation of genes related to photosynthesis, and also the core energetic metabolism. Considering the significance of the K, N, and P in cellular homeostasis of plants, chemical fertilizers that present abundant source of these nutrient minerals have been generated and used globally in a universally accepted manner (Gupta, 2005; Kim et al., 2009; Nath and Tuteja, 2016). According to the estimates by the FAO of the United Nations, the global use of potassium, nitrogen, and phosphorusbased fertilizers is likely to rise above 200.5 million tons in 2018; this would be 25% higher than consumptions recorded in 2008 (http://www.fao.org/3/a-i4434e.pdf). Although continued supply of minerals is essential for sustainable agriculture but due to the nonbiodegradable nature of these chemicals of their transformation products, gross concerns have been raised regarding their continued use. It is also worth mentioning that the chemical synthesis of N-fertilizers by reacting CO2 with anhydrous ammonia under high temperature and pressure contributes significantly to the production of greenhouse gases (GHG) and nitrogenous fertilizers are the largest single source of GHG emissions from arable agriculture. The use of N- and P-fertilizers in agriculture is a major contributor to eutrophication processes in waters of both developed and developing nations. Numerous studies around the world have indicated the short- and long-term negative effects of the continuous use of these dangerous chemicals on human and animal health (Agarwal et al., 2015; Nath and Tuteja, 2016). Another concern is that the commercially viable reserves of sulfate and phosphate rocks used to produce P-fertilizers are being used up so rapidly that these will be exhausted within the next 25–100 years, raising uncertainty about its continued availability to the farmers. Also, since more than 50% of the applied fertilizer is lost from the soil, their booster doses (repeat applications) become essential for their effectiveness. Thus, for both commercial and environmental reasons, the input of chemical fertilizers has been recommended to be reduced along with implementation of improved agronomic practices, for example, use of organic manure for technically simple, environmental-friendly, cost-effective, and sustainable agriculture (Sharma and Reynnells, 2016; Loyon, 2017).

9.4.2 Seed Priming Priming applied to commercial seed lots is widely used by seed technologists to enhance seed vigor in terms of germination potential and increased stress tolerance (Beckers and Conrath, 2007). Priming is a water-based technique

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that allows controlled seed rehydration to trigger the metabolic processes normally activated during the early phase of germination (“pre-germinative metabolism”), but preventing the seed transition toward full germination. Priming can be done with water (hydro-priming), chemicals (chemo-priming), ionizing radiations (physical-priming), or microbes (bio-priming). Studies suggest that the initial exposure to chemical priming agents (in micromolar quantities) trigger the natural stress response machinery of the plants rendering them more tolerant to later stress events (Paparella et al., 2015; Ibrahim, 2016). One such compound is nitric oxide (NO)—a redox active molecule that is known to modulate plant responses to stressful conditions. It is supplied as S-nitrosoglutathione (GSNO) or sodium nitroprusside (SNP). In one of the study, it was reported that that sugarcane plants treated with GSNO at a range of 10–1000 μM showed significant improvement in relative water content and leaf, root dry matter under drought compared with sugarcane plants that were sprayed with water. Exogenous NO treatment with SNP has also been shown to decrease cadmium (Cd) accumulation in rice seedlings leading to better seed germination and seedling growth and alleviate arsenic (As)-induced oxidative stress in wheat seedling by enhancing antioxidant defense and glyoxalase system. SNP in combination with glutathione (GSH), at micromolar concentrations, has been reported to reduce copper uptake and Cu-induced oxidative damage in rice seedlings by a similar mechanism (Hasanuzzaman and Fujita, 2013; He et al., 2014; Mostofa et al., 2014, 2015). Another chemical used for seed priming is hydrogen peroxide (H2O2); although initially it was recognized as a toxic molecule that adversely affects the cell viability. However, it is now established that H2O2 acts as a central molecule responsible for integrating signaling networks in response to biotic and abiotic stress during the developmental processes. It is also involved in a cross talk with a number of signaling molecules, including plant phytohormones and reactive molecules such as NO and H2S; all of which are involved in signaling during seed germination. Seed priming using hydrogen peroxide has been used as a tool for improving seed quality and for enhancing seed stress tolerance during post-priming germination (Wojtyla et al., 2016). Very high concentrations of H2O2, however, can be detrimental for plant growth. Other studies have suggested that pre-sowing seed treatment (seed-priming) with ascorbic acid (AA) enhances tolerance to acidic soil and aluminum (Al) toxicity. Several studies have demonstrated that AA treatment decreased the activity of oxidative stress-related enzymes in the Al-tolerant genotype (Hossain et al., 2015; Wojtyla et al., 2016). In light of the role of seed priming in enhanced stress tolerance of plant, several types of priming protocols have been designed so far, all of them are optimized by accurate timing to stop the treatment before the occurrence of radicle emergence. Protocols developed for seed priming include at the end of the treatment, a rapid re-drying of seeds for storage purposes (Alcantara et al., 2015). However, in some cases, desiccation can alter the beneficial effects of priming, which are lost during storage. Indeed, reduced seed longevity is a well-reported disadvantage of seed priming. Another major reason for the slow adoption of seed priming is the current gap of knowledge on the pre-germinative metabolism which is hampering successful application of priming treatments. Nevertheless, researchers from academia and industry are currently focused on overcoming these issues. The recent advances on molecular highthroughput techniques (Omics technologies) combined with the recent release of new genomic resources on target species or crops are expected to improve the general understanding in this discipline. Defense priming, often called sensitization has been purposed as the crucial phenomenon in systemic plant immune responses (Borges and Sandalio, 2015; Conrath et al., 2015; Mauch-Mani et al., 2017). Synthetic agrochemicals and beneficial microbes are used for defense priming (pretreatment of seeds for enhanced defense). Earlier chemicals such as BABA, SA mimic 2,6-dichloroisonicotinic acid and its methyl ester (both abbreviated INA), and benzothiadiazole were used for priming; however, these pretreatments met with only limited economic success because of their moderate and strictly protective activity (Arasimowicz-Jelonek et al., 2013). Some of the recent examples of defense priming agents used in seed priming include 3,4-dichloro-2_-cyano-1,2-thiazole-5-carboxanilide and 1,2,3-thiadiazole-5-carboxamide, N-(3-chloro-4-methylphenyl)-4-methyl.

9.4.3 Transgenic Plants As mentioned above, plants are endowed with inherent capability to respond to different stress conditions by modulating (up and downregulating) the expression of stress responsive genes. Functional genomics and transcriptome analyses of plants exposed to/subjected to stress environments have been undertaken to obtain essential insight into the differentially expressed genes in stress-treated plants compared to non-treated plants (Kurotani et al., 2015a). In one such analyses, RNA-sequencing analysis carried out on berries collected at the three developmental stages before, at the onset, and at late ripening indicated that water deficit affected the expression of 4889 genes in grape plants (Kurotani et al., 2015a).

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With improving understanding of the molecular biology of stress response genes/stress-resistant conferring genes, significant progress has been made in the field of generation of transgenic or genetically modified (GM) crop varieties with improved stress tolerance. Out of the plethora of gene expression changes associated with stress response, certain distinctive sets of proteins have been targeted for the production of stress-tolerant transgenic plants. These include the overexpression of (i) TFs, (ii) enzymes, (iii) phytohormones, (iv) protease inhibitors, etc. for generation of abiotic stress tolerant transgenic lines. One of the example study reported introduction of dehydration responsive element-binding protein 1B (CBF1/DREB1B) from Arabidopsis thaliana into Salvia miltiorrhiza. The stable transgene line showed improved relative water content, chlorophyll content, and the net photosynthetic rate compared to the wild type (WT) under drought stress. Similarly, introduction of DREB1B from rice (Oryza sativa) into tobacco plants resulted in improved oxidative and freezing stress tolerance of the stable transgenic line (Gutha and Reddy, 2008). Another study reported that overexpression of SpWRKY1 into Phytophthora nicotianae resulted in increased tolerance to salt and drought stress in transgenic tobacco (Li et al., 2015). Expression of NAC protein form Solanum lycopersicum (SlNAC35) in tobacco was found to induce greater number of lateral roots and longer root length compared with derivative lines obtained with empty vectors after drought and salt treatment (Wang et al., 2016b). Transgenic black-gram (Vigna mungo) plants overexpressing the ALDRXV4 were shown to be able to survive longer periods of drought and salt stress and showed improved recovery as compared with the wild-type plants under laboratory and glass house conditions (Singh et al., 2016). Improved abiotic stress response has also been obtained when transgenes of PRR5 (PRR-VP), that is, pseudo-response regulator, which function was introduced as transgene in A. thaliana and transgenic plants were subjected to growth under stressed environments (Nakamichi et al., 2016). In agreement with abovementioned reports, other studies have also found that overexpression of selected transgene such as cysteine protease inhibitors from cereals successfully delayed sprouting and nutrient loss in potato tuber. Overexpression of CYP94C2b, that promotes deactivation of JA, was found to be most efficient for enhancing salt tolerance in rice (Kurotani et al., 2015b). Overexpression of AtMYB12 shows upregulation of genes involved in flavonoid biosynthesis, ABA biosynthesis, proline biosynthesis, stress responses and ROS scavenging under salt, and drought stresses in A. thaliana (Pandey et al., 2015; Wang et al., 2016a). Abiotic stress tolerant stable transgenic crops have numerous advantages over the wild-type cultivars. They can avoid food scarcity in the third world countries due to their higher yields, alleviate the deficiencies of protein, minerals, and vitamins and can be used to combat malnourishment in underdeveloped and developing countries (e.g., “Golden Rice,” genetically enriched with vitamin A and iron); confer resistance to insect pests through the bioengineering of a specific gene, from a soil-borne bacterium, Bacillus thuringiensis (Bt) resulting in the elimination of the pest damage without application of pesticides, increase the yield by enhancing tolerance against drought and salinity tolerance (Basu et al., 2010). The first transgenic plants were developed over 30 years ago with traits like tolerance to herbicide and insect resistances. In 1994, the transgenic “Flavr Savr tomato” with delayed ripening was approved by the Food and Drug Administration (FDA) for marketing in the United States. Currently, several varieties of GM crops such as cotton, soya, maize, potato, sugar beet, alfalfa, and canola are grown throughout the world (Basu et al., 2010; Kamthan et al., 2016). Transgenic crops producing B. thuringiensis (Bt) insecticidal proteins (Bt crops) has reduced the use of synthetic insecticides on cotton, maize, and soybean fields in 11 countries throughout Latin America (Blanco et al., 2016). According to a recent report of the 31 pests targeted and controlled by Bt crops in Latin America since more than a decade, only Spodoptera frugiperda has shown tolerance to certain Bt proteins (Basu et al., 2010; Kamthan et al., 2016). GM technology has thus increased the pace of genetic improvement of crop plants, leading to the rapid development of cultivars with higher yield, nutritional value, enhanced stress tolerance, and wider adaptability. In spite of considerable commercial value and success, GM crops have been facing increased disapproval and lack of consumer acceptance because of the associated risks to the environment and food safety. One of the main public concern that prevent the widespread use of crops developed using process of transgenesis is the introduction of foreign DNA in the plant genome without utilizing plant’s native genetic repertoire to achieve the desirable traits. In order to meet this concern, two novel transformation concepts—cisgenesis and intragenesis were developed as alternatives to transgenesis (Holme et al., 2013; Kamthan et al., 2016). Both concepts imply that plants must only be transformed with genetic material derived from the species itself or from closely related species capable of sexual hybridization (Holme et al., 2013). Another major concern of the use of transgenic technology in complementing crop breeding are the technical limitations faced for many economically important crop plants or elite varieties that are highly recalcitrant to genetic transformation and regeneration (Bawa and Anilakumar, 2013; Rastogi Verma, 2013; Kamthan et al., 2016).

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9.5 MICROORGANISMS IN PLANT STRESS MANAGEMENT The use of microorganisms is also a promising approach for stress management in crop plants. There are two major groups of microorganisms namely arbuscular mycorrhiza fungi (AMF) and PGPR that have been shown to improve plant stress tolerance (Dhawi et al., 2015). They live in symbiosis with the plants as they draw nutrition from the root exudates and in turn secrete various compounds that help in plant growth. The use of a combination of rhizospheric microbes namely AMF and PGPR has been widely reported to increase plant biomass and nutrient uptake in maize grown in mining-impacted soil under heavy metal contamination (Dhawi et al., 2015). The priming of seeds with PGPR has been widely reported to alleviate the levels of various oxidative stress-related enzymes. The successful examples are the coinoculation of AMF with rhizobia, AMF, and free-living N-fixing bacteria or different PGPR were reported to assure nutrients uptake comparable to chemically fertilized plants. Unlike their chemical counterparts, they are environmental friendly and safe. Once added to the soil, they can multiply and self-sustain themselves for years. The current agricultural practices can benefit greatly with the use of such technologies. AMF is also an equally promising candidate but for restricting the scope of this chapter, the focus shall be placed on the role of PGPRs in plant stress tolerance and potential role of rhizospheric microbial diversity in the enhancing the biotic and abiotic stress tolerance amongst crop plants (Adesemoye et al., 2008; Lucas et al., 2014; Garcia-Cristobal et al., 2015).

9.5.1 PGPR in Abiotic Stress Management The PGPR can help plants face abiotic stresses by enhancing plant nutrition via associative nitrogen fixation, phosphate solubilization, or phyto-siderophore production. They can improve root development and growth through the production of phytohormones or through other root development-associated enzymatic activities (Vassilev et al., 2015). Some PGPR can help plants withstand heavy metals or other pollutants and increase the capacity of plants to even sequester heavy metals. PGPRs can act as superior biocontrol reagents because of traits like synthesis of antibiotics, secretion of iron-binding siderophore to obtain soluble iron from the soil and provide it to the plants thereby deprive fungal pathogens in the vicinity of soluble iron, production of low molecular weight metabolites such as hydrogen cyanide, enzymes including chitinase, B-1,3-glucanse, protease, and lipase which can lyse fungal cells, outcompeting phytopathogens for nutrients and niches on root surface, lowering the production of (pathogen) stress ET in plants with the enzyme ACC deaminase (Glick, 2014). Thus, they can protect the plant through inhibition of phytoparasites, based on antagonism or competition mechanisms, and/or by eliciting plant defenses such as induced systemic resistance (ISR) (Glick, 2014). A brief account of various compounds secreted and by PGPR is presented below.

9.5.2 Secretion of Phytohormones by PGPRS Phytohormones are small molecules that play critical roles in regulating plant growth and development (Fahad et al., 2015). Many of the PGPR isolates are capable of producing these hormones and thus they can play a significant role in plant stress tolerance toward different abiotic stimuli. For example, indole-3-acetic acid (IAA), a phytohormone known to control a wide variety of processes in plants is known to be produced by many PGPR (Fierro-Coronado et al., 2014). Low concentrations of exogenous IAA can stimulate primary root elongation, whereas high IAA levels stimulate the formation of lateral roots, decrease primary root length, and increase root hair formation by modulating cell division and differentiation (Fahad et al., 2015). Another group of phytohormones called CK is known to stimulate plant cell division, control root meristem differentiation, induce proliferation of root hairs, but inhibit lateral root formation and primary root elongation. Similarly, CK and gibberellins producing PGPRs can stimulate plant growth under both normal and stressed environment (Fahad et al., 2015; Verma et al., 2016). Another phytohormone, viz., ABA is well known for its involvement in drought, salinity, and osmotic stress (Kaleem et al., 2018; Shu et al., 2018). Many PGPR strains have been characterized for synthesis and secretion of ABA (Kaleem et al., 2018; Shu et al., 2018). Furthermore, enhancement of ABA levels on secretion by PGPR has been shown to ameliorate the response of A. thaliana to drought stress. Yet, another key phytohormone, that is, ET which inhibits root elongation and auxin transport, promotes senescence and abscission of various organs, and leads to fruit ripening. ET is also involved in plant defense pathways. PGPR modulates the activity of ET by secretion of an enzyme called ACC deaminase (Tao et al., 2015; Van de Poel et al., 2015; Dubois et al., 2018).

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9.5.3 Production of Volatile Compounds Apart from synthesis of phytohormones, PGPRs also promote plant growth and their tolerance under stressed environment by emitting volatile organic compounds (VOCs). Microbial VOC emission was first reported in 2003 and subsequently, it has been recognized as an important aspect of plant-microorganism interactions. Some of the recent studies have even characterized the chemical nature of microbial VOCs and reported their potential effects on plant biomass production, disease resistance, and enhancement of plant abiotic stress response and abiotic stress resistance. VOC emissions have been studied in both Gram positive and Gram negative bacteria. VOC emission is indeed a common property of a wide variety of soil microorganisms, although the identity and quantity of volatile compounds emitted vary among species (Ryu et al., 2003; Blom et al., 2011; Rath et al., 2018). The most abundant compounds consistently released from VOC strains are 2, 3-butanediol and 3-hydroxy-2-butanone (also referred to as acetoin) identified as bioactive molecules that trigger both growth promotion and ISR. Oxidized and methylated products of these fusel alcohols were identified in later studies, including aldehydes, ethers, and acids.

9.5.4 Potassium and Phosphate Solubilization Soils generally contain a large amount of potassium and phosphorus, which accumulates in the wake of regular fertilizer applications, however, only a small proportion of the later is available for assimilation by plants. On their own, plants are able to absorb only mono and dibasic phosphate, therefore, organic or insoluble forms of phosphate must be mineralized by microorganisms, respectively, for it to be assimilated by plants. Many PGPR—such as Pseudomonas, Bacillus, Rhizobium, Azospirillum, Burkholderia, Erwinia, and Serratia are reported as phosphate solubilizing bacteria (Bhattacharyya and Jha, 2012; Bhardwaj et al., 2014). They are able to dissolve insoluble forms of phosphate through one of the following two processes: (i) acidification of the external medium through the release of low molecular weight organic acids (such as gluconic acid) that chelate the cations bound to phosphate and release assimilable phosphorus and (ii) production of phosphatases/phytases that hydrolyze organic forms of phosphate compounds (Bhattacharyya and Jha, 2012). In addition to phosphorus, PGPR can also increase assimilation of several other nutrients including N2 and essential minerals as Ca, K, Fe, Cu, Mn, and Zn. While mineral assimilation is augmented through a mechanism similar to the one described above for phosphorus assimilation and usually occurs through acidification of the rhizospheric soil via organic acid production or via stimulation of proton pump ATPase. In any case, the soil pH decrease improves solubilization of these nutrients (Perez-Montano et al., 2014).

9.5.5 Nitrogen Fixation Many PGPR also improve plant growth as well as stress response through fixing of the atmospheric N2 such that it could be assimilated by plants. Plants can assimilate nitrogen (N) from soil only as nitrite, nitrate, or ammonia (Bhattacharyya and Jha, 2012; Pham et al., 2017). Therefore, atmospheric N2-fixing bacteria such as Rhizobium and Bradyrhizobium are regarded as vital to plant growth as well as survival under both normal and stressed environment. N2-fixing PGPRs establish symbiosis forming nodules on roots of leguminous plants, in which they convert N2 into ammonia. However, this process is practically limited to legume crops. However, several nonsymbiotic bacteria have been identified as free-living N2-fixers (Azospirillum, Azoarcus, Azotobacter, Bacillus, Burkholderia, Gluconoacetobacter or Herbaspirillum, etc.). Together these three functions viz., phosphorus, potassium solubilization, and nitrogen fixation contribute as the most important mechanism for PGPR-mediated plant growth promotion as well as abiotic stress response by the host plants.

9.5.6 Secretion of ACC Deaminase Biotic and abiotic stresses exemplified by invasion by phytopathogenic fungi and parasitic nematodes or the presence of heavy metals, temperature, pH and water extremes, etc. results in an increase in ET concentration in cop plants. ET, also called stress ET, is believed to be involved in initiating the transcription of genes involved in the production of plant defensive and protective proteins. But the presence of huge levels of ET leads to senescence, chlorosis, leaf abscission, and death. ACC deaminase, that is, 1-aminocyclopropane-1-carboxylate (ACC) deaminase is a key enzyme responsible for the cleavage of the plant ET precursor, ACC, into ammonia and alpha-keto-butyrate. Due to the activity of PGPR-synthesized ACC deaminase, the amount of ET that could potentially form in the plant is reduced. ACC deaminase is produced by certain microbes that reside in rhizosphere and acts as a sink to the plant ACC

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(a non-ribosomal amino acid) that exudes from seeds, roots, or leaves. Thus, by decreasing ACC levels in plants, ACC deaminase-producing organisms decrease plant ET levels. As a result, plants which grow in association with ACC deaminase-containing plant growth-promoting bacteria generally have longer roots and shoots and are more resistant to growth inhibition by a variety of ET-inducing stresses (Glick, 2005; Gamalero and Glick, 2015). One of the noticeable studies on effect of a number of ACC deaminase expressing rhizobacterial strain priming was assessed on salt-affected maize fields. Amongst the tested ACC deaminase expressing rhizobacterial strains, the strain S5 (Pseudomonas syringae), S14 (Enterobacter aerogenes), and S20 (Pseudomonas fluorescens) were the most effective strains for promoting the growth and yield of maize, even at high salt stress (Nadeem et al., 2007). The observation was found to be consistent with the levels of ACC deaminase produced/expressed by different strains (Nadeem et al., 2007).

9.5.7 Secretion of Antibiotics/Inhibitory Substances Apart from the ability of PGPR to assist plants for abiotic stress management, PGPRs also exhibit activities that enable them to mitigate the biotic stress largely caused by invasion by a pathogenic organism. According to several recent reports, PGPRs exhibit distinct antagonistic activities against pathogens which invade the corresponding host plant. For example, Pseudomonas graminis 49M exhibit antagonistic potential against Erwinia amylovora, the causal agent of fire blight. The strain 49M produces siderophores as well as antibiotics. Another study with genome sequencing and annotation of Bacillus amyloliquefaciens subsp. plantarum FZB42, used commercially as biofertilizer and biocontrol agent in agriculture revealed that nearly 10% of its genome is devoted to synthesizing antimicrobial metabolites and their corresponding immunity genes (Mikicinski and Sobiczewski, 2016). In addition to classically defined antibiotics, the PGPR also synthesizes molecules such as cyclic lipopeptides and volatile compound that are capable for imparting ISR to host plants, which protect plants against attacks of pathogenic microbes, viruses, and nematodes. These report clearly highlights how PGPR is essential component of the plant defense mechanism against biotic stress caused by invading pathogens (Mhlongo et al., 2018).

9.6 PGPRs USAGE: STATUS AND RECOMMENDATIONS The global scenario for the application of PGPR technology is rather transient yet for past 1–2 decades, Southern American countries are among top consumers of biofertilizers: In Mexico, a program to support the introduction of N-fixing biofertilizers based on Azospirillum was carried on 1.5 million hectares. The global market for biofertilizers in terms of revenue was estimated to be worth about 5 billion USD in 2011 and, according to a detailed analysis of the current market and of the scenarios for its development in the different continents, is forecasted to double by 2017. Various governments including the Netherlands, Thailand, Russia, Canada, France, and Australia have passed strict legislation regarding the quality and quantity of the PGPR inocula; while in other countries such as the United States, Mexico, Argentina, and the United Kingdom product quality and rate of application has been left to the discretion of the manufacturer (Malusa and Vassilev, 2014). Amongst all of the developing and developed countries taking part in application of PGPR in agronomic practices, India is probably the country with the most complete legal framework related to biofertilizers. The Indian Ministry of Agriculture issued an order in 2006 that was amended in 2009. It included biofertilizers under the Essential Commodities Act of 1955, and within the order for the control of fertilizers of 1985. In this act, the term biofertilizers means “the product containing carrier based (solid or liquid) living microorganisms which are agriculturally useful in terms of nitrogen fixation, phosphorus solubilization or nutrient mobilization, to increase the productivity of the soil and/ or crop.” The term is also covered under the broad definition of fertilizers, which “means any substance used or intended to be used as a fertilizer of the soil and/or crop.” According to the estimates of the Indian National Biofertilizer Development Center (NBDC) and the Bio-Tech Consortium of India Ltd. (BCIL), about 350,000–500,000 tons of biofertilizers are potentially required for Indian agriculture (Ghose and Bisaria, 2000). Large-scale efforts are therefore needed so that the potential of this environmental friendly technology can be fully exploited by farmers in India and around the world (Ghose and Bisaria, 2000). Although the use of PGPRs is blossoming but still the use of this technology is in nascent stage as is evident from a closer look. Some reports in literature do highlight the technologically mediocre state of the available commercial products. There have been examples of inoculant products sold in both developed and developing countries that did not contain any rhizobia or showed a high level of contamination with other species (Trivedi et al., 2017). A recent study showed that among 65 analyzed commercial biofertilizers, only 37% of the products could be considered as “pure” and

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that 63% were contaminated with one or more bacterial strains. Moreover, 40% of the tested products did not contain any of the claimed strains but only contaminants. This is a scary scenario and indicates the lack of proper research in process development and optimization. Hence, in order to increase the widespread use of PGPRs in stress management, conditions for maximum growth without compromising the plant growth-promoting traits during large-scale production and formulation needs to be defined (Herrmann and Lesueur, 2013). The recommendations regarding the development of bioprocess for the beneficial inoculants are concerned, it is argued that it should be approached in two ways, that is, growing and formulating two (or more) different microorganisms separately and then mixing later or alternatively developing a mixed inoculant after a mixed fermentation which is then formulated together. Cocultivation approach is of course based on strain compatibility, that is, the strains in question do not interfere with growth of one another. Once it is firmly established that the two or more strains that are to be cultivated together have similar growth rates and are compatible to each other, then the bioprocess for cocultivation is developed. Either submerged or solid-state fermentation (SSF) could be used for the production of PGPRs. Since SSF is carried under low or no water conditions, it allows the use of agro-industrial waste like wheat bran, sugarcane bagasse, etc. Also, since it does not require any clarification/purification steps afterwards hence are very cost effective when compared to submerged fermentation. One of the reports has strongly advocated the use of SSF for the production of useful rhizobacteria. The authors have also rightly reasoned that after fermentation, the whole thing comprising of residual substrate and growing PGPRs can be formulated together ensuring stability and long-term survival of the bacterial inoculants/s and also increased soil fertility on application (Herrmann and Lesueur, 2013). Formulation refers to mixing the effective inoculant, that is, one or more strains of microorganisms with a particular carrier together with sticking agents or other additives which help in the protection of the cells during storage and transport. A good formulation will provide optimal conditions to enhance microorganism persistence in soil and maximize their activity in order to obtain the maximal benefits after inoculation to the host plants, it must be cost effective and easy to handle. In other words, the carrier ensures that the microorganisms are delivered to the target plant in the most appropriate manner and form. A number of studies have tabulated the available formulation strategies. Peat and talc have been used extensively in commercial formulations. In our view, the use of alginate seems to be more economical and user-friendly since the bacterial inoculants can be immobilized together using alginate beads that can be produced in macro or micro-sizes. Despite long history of research and development in the field of PGPR technology, till date the expected success with PGPR technology has not been achieve. The limited success with use of PGPRs as plant stress management tool or as biofertilizers has been debated from different perspectives, for example, ethical concerns, commercial viability, feasibility for technical improvement, etc. While other aspects are being looked upon, the scope for technical improvement of this technology has been focusing on the following key aspects: (i) development and optimization of bioprocesses for mass-scale production of functionally active PGPR biomass; (ii) development of PGPR consortia with bacterial isolates having complementary plant growth promotion functions; and (iii) formulation of media/matrix for in vivo application of PGPR biomass.

9.7 RHIZOSPHERIC MICROBIAL COMMUNITY: SIGNIFICANCE IN PLANT STRESS MANAGEMENT In addition to the developments in the field of PGPR technology listed above in the last section, there have been a lot of developments in the field of rhizosphere biology with respect to characterization of the microbial diversity and its metabolic functions. With advancement in the field of metagenomics and metatranscriptomics, a paradigm shift is being presently experienced in the field of rhizosphere biology and the impact of rhizosphere-associated microbial community structure on growth and survival of the crop plants under normal environments and perturbed environments (Ofaim et al., 2017). A lot of emphasis is being place of assessment of microbial ecology of rhizosphere for better its exploitation toward management of the plant stresses (Philippot et al., 2013). It is worth accentuating that despite this field of study being relatively nascent, there is already a noteworthy amount of research literature available which indicates that plant-rhizosphere community interaction is quite dynamic and exhibits the phenomenon of interdependence. Not only do the plants and their characteristics influence the composition, diversity, and dynamics of the rhizospheric microbial community compositions, but also other way around (i.e., the microbial community within the rhizosphere extensively impacts the fate of the plant, its growth and especially its tolerance/survival under stressed environments.

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9.7.1 Influence of Host Plant on Rhizospheric Microbial Community Till recent past the information about the total microbial community composition, diversity, and dynamics of the rhizospheric ecosystems were rather poor. However, with metagenomic approach, the diversity and structure of model rhizospheres are now being deciphered routinely (Tian and Zhang, 2017; Zhang et al., 2017). Since last decade, a number of studies have been carried out to determine the structure, composition, and dynamics of the microbial community structure of various microenvironments including the plant rhizospheres. The findings with such studies have been quite revealing. For example, in one of the recent studies, the rhizospheric microbial community structure has been shown to be affected by even the application of nitrogenous fertilizers (Kavamura et al., 2018). Another study analyzed the effects of plant root exudates on structure and activity of microbial community in a micro-polluted constructed wetland. Results from this study revealed that root exudates could act as endogenous source of carbon heterotrophic denitrifying bacteria and thus it could modulate the composition and function of the associated microbial community (Wu et al., 2017a). With accumulating information regarding plant-rhizosphere microbial community composition, this and other studies are postulating that (i) plant genotype selects the rhizosphere microbiome and (ii) the success of plant-rhizosphere microbe interactions is dependent on factors that directly or indirectly influence the plant rhizosphere microbial composition (Schlemper et al., 2017). Some of the studies in this direction are first of a kind investigation wherein the contributions of plant genotype, plant growth stage, and soil type in shaping rhizosphere bacterial community composition were analyzed. Results obtained during this study suggested that during the initial stages of plant development, the composition of rhizospheric microbiome was largely influenced by soil characteristics, whereas at the later stages of the plant development, the rhizospheric community structure shaped according to the genotype of the concern plants (Schlemper et al., 2017). A few other studies have also reported similar observations with respect to effect of plant genotype, plant growth stage, and soil types on the microbial community structure (Wieland et al., 2001; Qiao et al., 2017; Zogg et al., 2018). Apart from the studies reporting impact of the plant genotype and plant metabolism on the composition, diversity, and dynamics of microbial community, other studies have shown comparative analyses of rhizospheric microbial communities related to plant cultivars grown are standard vs perturbed environments are also being analyzed (Lucas et al., 2013; Naylor and Coleman-Derr, 2017). Plants when subjected to or exposed to stress environments also experience the alteration of the microbial community structure. This phenomenon was observed and reported in a recent report that highlighted drought-induced changes in microbial composition within the rhizosphere; it was observed that drought significantly altered the overall bacterial and fungal compositions (Santos-Medellin et al., 2017). The results obtained within this study strongly indicated that drought, which is an abiotic stress not only affects the plant physiology but also results in restructuring of root microbial communities. The authors discussed that there is a possibility that constituents of the altered plant microbiota might be important for survival of under extreme environmental conditions (Santos-Medellin et al., 2017). It is expected that with such comparative assessment, the dominant microbial taxa could be identified within the rhizosphere of the plant cultivars growing under stress environments. Such enriched taxa may have key involvement in stress response and mitigation. Based on such findings, it could be proposed with confidence that the composition, diversity, dynamics, and activity of microbial communities within the plant rhizospheres remain extremely dynamic and often shape up in response to the genotype and the activities of the host plants.

9.7.2 Influence of Rhizospheric Microbial Community on Host Plant Growth and Survival While it has been widely acknowledged for a long time that the plant-rhizospheric microbiome interaction is of symbiotic nature and it may be the pivotal resource for rhizosphere engineering, technology development, and intervention, yet the limitation of the microbial culturing (with 1% of total microbial diversity being acquiescent to laboratory-based growth and cultivation) has significantly hindered the progress in this direction. As mentioned above, with advent and advancement of metagenomics, that is, “culture independent methodologies for analyses of microbial community structure composition and dynamics, it is now feasible to predict the possible contribution of rhizospheric microbial communities with regards to growth and survival of host plants under various environments” (Berlec, 2012; Hirt, 2012). Several studies have highlighted the significance of rhizospheric microbial diversity of the adaptation of plant for growth under environment with adverse abiotic stresses. One of the research studies showing direct implication of the rhizospheric bacterial diversity in plant cultivars ability to tolerate abiotic stress, highlighted that the rhizospheric community structure of Cd accumulating and non-accumulating rice cultivar had noticeable difference (Zhou et al., 2018). While the rhizosphere associated with Cd accumulating cultivar was specifically enriched with

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Bacteroidetes, Firmicutes, and Deltaproteobacteria, the rhizosphere of Cd non-accumulating was dominated by Alphaproteobacteria and Gammaproteobacteria (Zhou et al., 2018). Thus, authors suggested that there might be a potential association of Cd uptake and accumulation with rhizosphere bacteria in rice grown on a contaminated soil (Zhou et al., 2018). Another study carried out the tripartite analyses of the three components viz., plant, bacteria diversity, and fungal diversity with regards to plant survival under soil contamination (Gonzalez et al., 2018). The study was carried out with metatranscriptomics analyses and determined the involvement of bacterial as well as fungal genes in the growth of the host plant. The authors highlighted that metatranscriptomics analyses could identify a wide spectrum of genes that remain cryptic under laboratory conditions, but they have a considerable involvement in functions ranging from eukaryotic interaction, biofilm formation, and dioxygenase hydrocarbon degradation (Gonzalez et al., 2018). Although the precise underlying mechanisms are yet to be deciphered, still it is reasonable to state that rhizospheric microbial communities not only play an important role in growth of the plant, but also they render stress response and survival capabilities to the plants growing under stress environments.

9.7.3 Rhizospheric Microbial Community Engineering for Plant Stress Management As highlighted above, there is substantial amount of literature available that clearly establishes the role of plant genotype, plant activities, and plant exposure to adverse environments in determining the structure, dynamics, and functions of the rhizospheric microbial communities; also there is an increasing literature which indicates that the rhizospheric microbial diversity must have a critical role in stress response mechanism of the plants to various biotic and abiotic stress. However, till date, there is only very little amount of information/literature available that unmistakably shows the influence of rhizospheric microbial diversity on plant stress response to the harsh environmental conditions imparting biotic or abiotic stresses and the underlying mechanism involved. Thus, there is scope for future research (specifically with “metagenomics” and “metatranscriptomics”) to dissect the precise role and mechanism of plant-microbial community interactions and their significance in stress response phenomenon. Information obtained from such studies could be vital in the development and execution of “rhizosphere engineering” processes toward improved and sustainable agriculture even under perturbed environments. Some of the discreet studies have taken initiative in this regard and their findings have suggested that rhizospheric microbes that got enriched during growth of host plant under drought condition might be vital for host plant’s response to abiotic stresses such as drought. These microbe could be referred as drought-responsive microbes and they may potentially benefit the plant as they could contribute to tolerance to drought and other abiotic stresses, as well as provide protection from opportunistic infection by pathogenic microbes (Santos-Medellin et al., 2017). The beneficial effects of soil microbiota on amelioration of salinity-induced abiotic stress has been reported previously amongst a number of plant cultivars and the same has been reviewed previously (Dodd and Perez-Alfocea, 2012). Another relatively direct study carried out with the objective of determining the effluence of microbial community associated with plants on alleviation of plant stress and increase plant growth when plants are grown under suboptimal growing conditions characterized by typical abiotic stresses. Using a microbiome inoculation strategy, authors studied microbiome associated with the rhizosphere of Populus deltoides changed in response to diverse environmental conditions, including water limitation, light limitation, and metal toxicity. The authors were able to identify an important group of bacterial genera that changed significantly in response to host stress. Authors referred this important group of bacterial genera as “stress microbiome” (Timm et al., 2018). Furthermore, they suggested that the ability of microbiome to buffer the plants from extreme environmental conditions and abiotic stress is extremely important and provides an opportunity for future efforts aimed at predictably modulating the microbiome to optimize plant growth (Timm et al., 2018). This suggestion is in close agreement with the previous opinion articles that biofertilizers mediated crops functional traits such as plant growth and productivity, nutrient profile, plant defense, and protection under stress environment cause cellular response and thereby they could be used to ensure sustained agriculture even under adverse environments with harsh abiotic stresses (Bhardwaj et al., 2014). As noted by a few reports, there is a general trend for increase in the abundance of certain microbial taxa within the rhizosphere of the plants growing under stressed environments as compared to bulk soil. These taxa are regarded as “stress microbiome.” However, the functional consequences of increase in a few taxa are only poorly understood. While the general acceptance is that increases in the abundance, activity, or diversity of soil microorganisms during plant growth under abiotic stress should have positive involvement of the increased taxa in stress and that the increase in abundance should also correlate with overall increase in the activity, higher levels of nutrient recycling, and competitive exclusion of pathogens. Unfortunately, the direct experimental evidence for these phenomena has not yet been reported.

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The plant-microbiome interaction(s) are rather complex and may be difficult to determine precisely. It is very challenging to understand the plant-microbiome communication. The present understanding is still mostly rudimentary as plant-microbiome interactions varies between crops species and their cultivar or even between individual members of the microbiome and with varying environmental conditions. Therefore, many complex aspects of the plant-rhizospheric microbiome relationship must be scrutinized thoroughly for exploiting the full potential of rhizosphere microbiome in plant abiotic stress management.

9.8 FUTURE DIRECTIONS IN RHIZOSPHERE MICROBIOME ENGINEERING IN SUSTAINABLE AGRICULTURE The plant-rhizosphere interactions are extremely complex; such that the plant and rhizosphere-associated microbiome are highly interdependent. Taking this phenomenon into consideration, the optimization must be carried out for the plant-rhizosphere microbiome as one unit instead of each of the part separately. In light of the recent findings, the rhizosphere microbiome has emerged as a critical component in plant homeostasis, growth, and survival under both normal and stressed environments. It has the potential for imparting both beneficial and detrimental effects on plant growth. The eventual outcome probably depends on complex chemical signals interplay between the plant and its rhizosphere microbiome. Further studies are required for determination of the interaction that occurs at the level of plant and its rhizosphere-associated microbial community to develop essential understanding of the factors controlling these interactions. Such studies would go a long way and provide promising avenues for developing rhizosphere microbiome as an important component for plant abiotic stress management toward sustainable agriculture. These studies would also help in reducing the greenhouse gas emissions, and decrease the rates of agriculture soil contamination with hazardous chemical pesticides and fertilizers.

9.9 CONCLUSIONS The rhizosphere microbial diversity is now being considered as the central determinant of all plant characteristics and trait including growth, yield, and survival under biotic and abiotic stress environments. Furthermore, it is being suggested that the microbial diversity can render beneficial as well as detrimental effects on plant functions depending on a very subtle balance between the host plant, environment, and the microbial diversity, which itself is controlled by multifaceted chemical signals being exchanged amongst and between the plant and its rhizosphere microbiome. Technical capabilities of controlling such interactions may enable rhizosphere engineering that could be valuable for abiotic stress management in crop plants toward sustainable agriculture. However, the present state of art with respect to plant-microbiome interaction is not completely discovered and further research aiming at understanding the interplay of plant to microbial community is needed to fully understand the factors controlling microbiome assemblage and its feedback to the plant host. An improved understanding of the role of rhizosphere microbial diversity in plant stress mitigation would help in optimization of the engineered plant-microbiome; leading to sustainable agriculture.

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Further Reading Green, H., Broun, P., Cook, D., Cooper, K., Drewnowski, A., Pollard, D., Sweeney, G., Roulin, A., 2018. Healthy and sustainable diets for future generations. J. Sci. Food Agric. 98, 3219–3224. Sifakis, S., Androutsopoulos, V.P., Tsatsakis, A.M., Spandidos, D.A., 2017. Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environ. Toxicol. Pharmacol. 51, 56–70. Szabala, B.M., Osipowski, P., Malepszy, S., 2014. Transgenic crops: the present state and new ways of genetic modification. J. Appl. Genet. 55, 287–294.