ABSTRACT
Arid regions are characterized by extreme temperature shifts, unpredictable rainfall, strong winds, water shortages, and sandy soils, creating challenging conditions for agriculture. These conditions lead to reduced crop yields and quality, posing significant challenges to farmers and researchers alike. To address these issues, there's growing interest in harnessing microbial communities that enhance plant health and provide protection against pathogens. Plant Growth Promoting Microorganisms (PGPM) are gaining attention for their roles in bio-control, stimulating growth, boosting stress tolerance, and fostering antagonistic interactions against soil-borne pathogens. Specifically, plant growth promoting rhizobia, found in the plant root zone (rhizosphere), are noteworthy for their ability to thrive in arid conditions due to their adaptations to drought and heat. While these microbes have been studied in labs, their practical use in the field requires deeper insights into their behavior and extensive field testing.
Keywords: Biocontrol agents (BCAs), climate change; drought tolerant, soil; PGPR; soil-borne phytopathogens
INTRODUCTION
Agriculture in desert soils with scant water resources faces challenges from soil-borne pathogens, notably affecting legumes, oilseeds, and various fruit crops like Ziziphus mauritiana (ber) and date palm. Diseases such as dry root rot by Macrophomina phaseolina in legumes, wilt disease in cumin from Fusarium oxysporum f. sp. cumini, and tree mortality due to Ganoderma lucidum are prevalent. Fruit crops suffer from powdery mildew, fruit rots, and rust, leading to yield losses and economic impacts. In response, research is targeting microbial solutions to boost plant health and counteract these pathogens. This chapter explores microbial biocontrol agents, root microbiomes, and other Plant Growth Promoting Microorganisms (PGPM) from arid areas. The objective is to harness these drought- and heat-resistant PGPMs to bolster sustainable agriculture in arid regions.
Mycorrhizae, endophytes, and symbionts in plant growth promotion
The synergistic relationship between mycorrhiza and mycorrhizal-associated bacterial communities (MAB) plays a vital role in enhancing soil and plant health. This relationship improves soil nutrient allocation through MAB-assisted nutrient solubilization and prevents the intraradical colonization of soil-borne phytopathogens, particularly in arid and semi-arid regions of India. Integrating MAB with diverse plant growth-promoting rhizobacteria (PGPR) attributes such as phytohormone production, siderophores, and lignocellulose decomposing enzymes, alongside suitable mycorrhizal types, can further enhance this interaction process. This extension of microorganism applicability holds promise for sustainable plant and soil health management (Mitra et al., 2019). A study has highlighted Arbuscular Mycorrhizal Fungi (AMF) as an alternative option to conventional fertilization methods. However, successful soil inoculations require careful planning, and results may vary depending on the nature of the host plant and fungal association. Factors influencing success rates and fungal persistence include species compatibility with the soil environment, spatial competition, and inoculation timing (Berruti et al., 2016). Recent advances in genomics and transcriptomics have expanded our understanding of fungal interactions with host plants and other soil organisms, revealing various important factors. Apart from enhancing soil fertility, AMF can improve plant systemic resistance, protecting host plants against biotic stresses like plant-parasitic nematodes. This protection occurs through enhanced root tolerance, direct competition for nutrients and space, altered rhizospheric interactions, and induced systemic resistance, making AMF a potential biocontrol agent against nematode pests (Schouteden et al., 2015). Various species of mycorrhizal fungi have been isolated, with some showing higher frequencies of occurrence than others. Spore populations show correlations with root colonization, organic carbon content, and rainfall, among other factors (Oyediran et al., 2019). Apart from mycorrhizal fungi, plant root niches harbor diverse endophytic microbes that contribute to plant health. These endophytic microbes, including bacterial endophytes, have been confirmed to play a role in plant resistance against pathogens. Resistant cultivars often exhibit higher densities of bacterial endophytes, which can produce siderophores, HCN, and antibiotics, positively influencing plant health (Upreti and Thomas, 2015). Studies have demonstrated the inhibition of soil-borne pathogens by genetically modified Streptomyces spp. colonizing the rhizosphere and roots of lettuce. These transformed strains exhibit rhizospheric or endophytic behavior, showing potential for biocontrol (Bonaldi et al., 2015). Furthermore, microbial symbionts can affect plant health and contribute to the competitiveness of invasive plant species. Interactions between plants and their microbiomes hold biocontrol potential, with research focusing on developing novel microbe-based biocontrol strategies, particularly for invasive plant species like Phragmites australis (Kowalski et al., 2015).
Plant growth promoting metabolites
In pot experiments, a notable enhancement in cumin plant root length was observed when treated with Aspergillus versicolor and Trichoderma harzianum individually, as well as when integrated. However, the integration of both biocontrol agents (BCAs) with Verbisina led to increased shoot length and weight. The synergistic effect of these BCAs was evident in the enhanced shoot length and weight compared to the control group. This suggests that A. versicolor contributes to cumin root length enhancement, indicating its potential for growth promotion (Israel and Lodha, 2005). Nonetheless, further studies are necessary to fully comprehend the interaction dynamics of BCAs before drawing conclusive results. Additionally, A. versicolor releases various compounds including hydrocarbons, alcohols, ketones, ethers, and sulfur-containing compounds. Among these, sulfur-containing compounds have been identified as volatile metabolites toxic to fungal growth (Lewis and Papavizas, 1970). Furthermore, apart from antibiotics, A. versicolor also produces other metabolites (Sunsseson et al., 1995). Variations in the release of specific metabolites by different strains of BCAs, particularly those tolerant to heat, are likely. Thus, isolating and characterizing the specific metabolites released quantitatively and qualitatively by heat-tolerant strains of A. versicolor is imperative (Mawar and Lodha, 2019).
Similarly, in another pot experiment, guar seedlings treated with the bacterial bioagent Bacillus firmus exhibited significant increases in fresh and dry weights compared to both the control group and pathogen-inoculated seedlings. This evidence suggests that the bacterium effectively promotes the growth of the test plant (Lodha et al., 2013).
Microbial volatiles and other compounds in plant growth and defense
Plant roots are always in contact with soil microorganisms and flow of molecules released by them. Microbial exudates whether volatiles or particulates affect plants through variety of mechanisms such as biochemical signaling that elicits local plant defense toward soil borne pathogens or by inducing systemic resistance. Report evidenced volatile triggered secretion of plant root exudates which enhance or modulate overall plant fitness against fungi and bacteria and act as plant defense inducer. (Kai et al., 2007; Chung et al., 2016; Yi et al., 2016). Besides providing defense to plants, soil-microbes also affect plant metabolism and nutrient assimilation. A study conducted with Arabidopsis reported a novel mechanism through gene activation where plant growth-promoting (PGP) bacteria like Bacillus amyloliquefaciens GB03 activates gene responsible for sulfur assimilation and uptake by plant. Further, expression of transcripts coding for proteins which play a key role in biosynthesis of sulfur-rich aliphatic and indolic glucosinolates were reported. The increased concentration of sulfur in plants favored glucosinolate biosynthesis which in turn conferred protection against the beet armyworm Spodoptera exigua (Aziz et al. 2016). In another report, members of Lysobacter spp. were found abundantly in soils that are suppressive towards the pathogen Rhizoctonia solani and were predicted to affect soil-borne pathogens through secretions of extracellular enzymes and metabolites. The isolated strains acted antagonistically, in-vitro against phytopathogens including Rhizoctonia solani, Pythium ultimum, Aspergillus niger, Fusarium oxysporum, and Xanthomonas campestris, however not much suppression was observed in fields of sugar beet, cauliflower, onion and Arabidopsis thaliana implicating their poor rhizospheric colonization capabilities (Folman et al., 2003). The antagonistic potentials of Lysobacter spp. in disease suppressiveness need further exploration and confirmations and they could emerge as novel source of versatile antimicrobial compounds (Gómez Expósito et al. 2015). Other than providing defense against pathogenic microorganisms, several of microbial metabolites protect plants from herbivores. Foul odors and toxins from microbial exudates protect plants from gazing and act barrier for insect vectors (Mithöfer and Boland, 2012). Fungal metabolites are also known to protect plants against feeding of the cereal aphid Rhopalosiphum padi upon association by Trichoderma citrinoviride isolates. Various long chain primary alcohols (LCOHs) were reported to have phago-deterrent effect, restraining aphids from settling on treated leaves. These LCOHs act through taste receptor neurons even at low concentrations and hold potential for insect management strategies in synergy with other control parameters (Ganassi et al, 2016).
Bio control potential of PGPM
The preceding discussion highlights the presence of native heat-tolerant PGPM in the harsh climate of the Indian arid region, where soil temperatures can soar up to 55°C during summer. Despite such extreme conditions, resting structures like chlamydospores and sclerotia of soil-borne plant pathogens endure, alongside the survival of native PGPM propagules. However, there's a need to bolster the population of these PGPM to effectively combat soil-borne plant pathogens. Significant progress has been made in identifying suitable food substrates to support the survival and proliferation of these bioagents (Mawar et al., 2019). Studies conducted at the Central Arid Zone Research Institute (CAZRI) have demonstrated the compatibility of combining beneficial BCAs such as T. harzianum and B. firmus with suitable carriers and food substrates to ensure their survival (Mawar and Lodha, 2012). This combined approach offers multiple advantages, leveraging different mechanisms of biocontrol activity.
Furthermore, soil moisture plays a crucial role in the multiplication and efficacy of bioagents, particularly B. firmus. Optimal soil moisture levels significantly enhance the biocontrol activity of this bacterium. Recent interventions aimed at mitigating large-scale mortality observed in Indian mesquite trees involved a simple yet effective technique of incorporating onion residues into the soil beneath the trees, thereby fostering the multiplication of Aspergillus nidulans, a known bioagent against G. lucidum (Mawar et al., 2021). Incorporating PGPM as a biocontrol agent can be achieved through different application methods such as soil incorporation, foliar spray, seed biopriming, or seed treatment to enhance disease control. Additionally, there's a need to explore and harness more endophytic and drought-tolerant aggressive native strains of PGPM from the soil to further bolster disease management strategies.
Soil amendments in biocontrol
Variety of organic matter amendments were characterized and still under exploration for their potential to favor biocontrol agents and influence soil resident communities (Bailey and Lazarovits, 2003; Bonilla et al., 2012). Similarly, soil amended with composted almond shell reported positive effect. Amended soil suppressed growth of pathogens including Rosellinia necatrix (a causal agent of white root rot on avocado) and favored Proteobacteria, Actinobacteria and Ascomycota specifically Pseudomonas, Burkholderia spp. and Mortierellales (Vida et al. 2016). A study therefore, was undertaken to investigate survival of bio-agents, microbial population dynamics and activity, availability of micronutrients during the process of composting and in mature composts prepared from certain on-farm wastes (Mawar et al., 2020). Use of compost is an easy alternative for amending soil in arid soils where moisture retention is poor (Lodha and Burman, 2000). Efforts were also made to inactivate released propagules of M. phaseolina from infected crop residues during heat phase of composting by increasing nitrogen concentration and exposing mature compost to dry summer heat. Trichoderma harzianum disappeared during peak heating but reinfestation occurred at mature stage with maximum counts in P. juliflora compost, while Bacillus spp. was present throughout the composting period (Mawar et al., 2020). Similarly, neem cake also came out as an excellent carrier as it gave a prolonged shelf life of 200 days of T. viridae. Antifungal assay against plant pathogenic fungi revealed complete inhibition of growth and sporulation of fungal pathogens (Zope et al., 2019).
Suppressive soil and biocontrol
Once a biocontrol agent has proved its potential in control of a target pathogen, some specific aspects need investigations particularly in relation to the host and climate under which its use can be promoted. Studies are required to know its survival rate at different soil depths in fluctuating weather conditions and how other bio-ecological factors are governing population dynamics of the biocontrol agent. By generating this information, manipulation of soil environment and other associated bio-ecological factors in favor of PGPM, its population and activity can be enhanced in order to develop soil suppressiveness. Mode of action, survival in soil, growth promotion abilities of Trichoderma harzianum and T. viride as BCAs have been studied in detail. (John et al., 2010; Harman et al., 2004) but no information is available on population dynamics of A. versicolor a potent BCA. Studies on population dynamics over time and space have two basic goals: (a) to identify recurring patterns in population dynamics; and (b) to understand how these patterns are generated. Therefore, a study was undertaken to understand how biotic and abiotic factors influence population of A. versicolor at different soil depths in arid soils. Availability of organic matter and warmer temperatures at lower soil depth, in turn, favored survival of A. versicolor and other soil fungi. Positive correlation of soil moisture with fungal population has also been established by other workers (Panda et al., 1996). Variations in earlier findings can be attributed to seasonal conditions of both climates, particularly of arid region where soils are low in organic matter and temperature exceeds beyond 55°C in summer months. This is also evident from the fluctuations in A. versicolor population at lower soil depth where because of lower levels of temperature compared to upper soil depth, population continued to increase up to June (Singh et al., 2014). Occurrence of highest population in October at lower soil depth when the temperature reached 51°C is yet another evidence for the hypothesis (Singh et al., 2014). Soil suppressiveness is an uncommon property of soil to selectively affect survival of some microorganisms negatively. The infrequent phenomenon of soil suppression is known to regulate noxious organisms including root-knot nematodes Meloidogyne spp. and favor plant health (Bent et al., 2008). A number of studies have stated that Lawsonia (heena) plants can be used for suppression of the root knot nematode Meloidogyne javanica. Significant suppression of larval hatching in the nematode M. incognita by bark extract of henna has also been reported (Rafiq et al., 1991). A rich biodiversity of plants in Indian arid region has also provided a number of plants possessing insecticidal and fungicidal activity against insects, pests and diseases occurring in this region. Nature has bestowed arid region with diverse vegetation, which can be explored as botanical pesticides for soil suppressiveness. A study conducted in two organic horticulture greenhouses in Spain reported progressively decline in nematodes population with crop rotation and found associated cause as egg parasitism by the hyphomycete Pochonia chlamydosporia. Further suppressive nature of soil confirmed through the control non-sterilized soil where lower egg densities and reduced Meloidogyne reproduction was observed with higher microbial density in soil (Giné et al., 2012). However, soil suppressiveness needs more exploration to reveal its potentials for common use.
PGPM in induced resistance in plants
Plants do possess specific mechanisms to tackle attacking pests, pathogens and parasites. To escape from plant immunity, pathogens also have strategies and varying degree of virulence. Different exudates, formulations, toxin compounds and enzymes are attributed to virulence shown by pathogens. A report suggested the active role of Abscisic acid (ABA) in interactions between blast fungal pathogen Magnaporthe oryzae and the antagonistic bacterium P. chlororaphis EA105 with rice host. The pathogen, Magnaporthe oryzae-produced ABA enhanced plant susceptibility by affecting plant defense against fungi by acting antagonistically on salicylic acid (SA), jasmonic acid (JA), and ethylene signaling and thereby accelerating pathogenesis through higher rates of spore germination and appressoria formation.
Micromonospora strains have been reported to control fungal pathogens by provoking plant immunity. The strain dwells in nitrogen fixing nodules of healthy leguminous plants and posses PGP effect. This Gram-positive antifungal isolate reduced leaf infection by Botrytis cinerea through durable induced systemic resistance when inoculated on tomato roots. Further, gene expression analyses revealed mechanism of action of Micromonospora, which later confirmed using defense-impaired tomato mutants. Strain stimulated plant defense by enhancing jasmonate-regulated defense pathways and appear as extraordinary biocontrol agents with additional antifungal activity than eliciting plant immunity (Martínez-Hidalgo et al., 2015).
Report on Trichoderma parareesei transformants with reduced chorismate mutase (CM) activity (An intermediate of aromatic amino acids, essential in protein synthesis and precursor of many secondary metabolites) through Tparo7 gene silencing confirms reduced pathogen colonization by limiting growth rates and mycoparasite behavior against phytopathogenic fungi including R. solani, F. oxysporum, and B. cinerea in dual in-vitro cultures. Transformants reported to reduce susceptibility of tomato towards pathogens, also produced higher amounts of aromatic metabolites like tyrosol, 2-phenylethanol and salicylic acid (SA) (Pérez et al., 2015).
Omics approaches in PGPM
Recent advances in soil microbiology research are shedding light on the immense potential of plant growth-promoting (PGP) microbes. Cutting-edge “-omics” technologies have revolutionized our ability to gather valuable data swiftly, authentically, and cost-effectively. This enables a deeper understanding of previously unexplored interactions within rhizospheric ecosystems and the identification of novel soil microbes (Massart et al., 2015). A study investigating 12 strains of Bacillus subtilis, known for their PGP capabilities, revealed high genomic diversity, except for highly conserved strains of B. amyloliquefaciens. Genomic analysis uncovered numerous genes associated with the biocontrol and colonization capacities of these bacteria, including 73 genes involved in signaling, transport, secondary metabolite production, and carbon utilization in B. amyloliquefaciens subsp. Plantarum. Deletion of certain genes, such as those within conserved polyketide biosynthetic clusters encoding difficidin and macrolactin-like secondary metabolites, demonstrated their crucial role in reducing damage caused by pathogens like Xanthomonas axonopodis pv. Vesicatoria on tomato plants (Hossain et al., 2015). Further exploration through genome sequencing and analysis of Pseudomonas sp. SH-C52, isolated from soil suppressive to Rhizoctonia solani, unveiled its antifungal activity attributed to the chlorinated 9-amino-acid lipopeptide thanamycin. This isolate closely resembled Pseudomonas corrugata and possessed a genome size of 6.3 Mb, housing 5579 predicted open reading frames (ORFs). Notably, it harbored six non-ribosomal peptide synthetase gene clusters, including those responsible for thanamycin and brabantamide production. While thanamycin exhibited antifungal properties, brabantamide displayed anti-oomycete activity, targeting phospholipases of Phytophthora infestans. A third lipopeptide cluster, thanapeptin, exhibited activity against P. infestans with structural variations compared to known secondary metabolites, while the remaining cluster encoded unknown products. Collectively, these findings underscore the potential of SH-C52 lipopeptides, which exhibit diverse antimicrobial, antifungal, and anti-oomycete activities (Van der Voort et al., 2015).
Ameliorating arid lands through PGPM
Over decades, extensive research has been dedicated to developing sustainable management strategies for combating soil-borne plant pathogens affecting key crops and trees in arid regions. These strategies encompass various approaches, including moisture conservation techniques (Lodha, 1996), soil solarization (Lodha, 1995), utilization of soil amendments such as cruciferous residues (Mawar and Lodha, 2002) and composts (Bareja et al., 2013), screening for tolerant genotypes (Lodha and Solanki, 1992), bio-management practices, and the integration of different control methods. For instance, integrating sub-lethal heating with cruciferous residues and employing synergistic applications of chemicals with bio-control agents have shown promise (Singh et al., 2012; Mawar and Lodha, 2009). These collective efforts aim to sustain agriculture in arid zones by effectively managing soil-borne pathogens.
Growing concerns about the environmental impact of pesticide use, along with increasing pathogen resistance to these chemicals, have spurred research into microbial communities capable of tolerating arid conditions. These microbes, when associated with typical arid plants, can bolster plant resistance, improving overall plant health, production, and quality. PGPMs offer plants enhanced tolerance to various biotic and abiotic stresses. They also boost plant immunity and improve nutrient uptake and assimilation capabilities, as illustrated in Figure 1.
Soil samples were gathered from various arid ecosystems and subjected to analysis to isolate effective drought-tolerant bio-agents. Among the native biocontrol agents identified to exhibit antagonistic effects in vitro were Trichoderma harzianum, T. longibrachiatum, Aspergillus versicolor, A. nidulans, Bacillus firmus, B. tequilensis, and Streptomyces mexicanus (Mawar et al., 2017; Lodha et al., 2019; Mawar et al., 2021a; Mawar et al., 2021b). However, the field efficacy of these identified bio-agents on major arid crops and their impact on soil resident microflora necessitates extensive field trials and further understanding of their behavior. Various soil amendments and natural residues, including food substrates, have been explored to enhance the survival of these agents in arid soil. The mechanisms through which these agents exhibit antagonism include direct operations such as parasitism, antibiosis, and competition, as well as indirect effects through manipulating the host rhizosphere, reducing host susceptibility, secreting exudates, resistance through host-mediated interactions, hypovirulence, and plant growth-promoting effects.
A two-year study was conducted to assess the collective effect of two different drought-tolerant biocontrol agents, Bacillus firmus and Aspergillus versicolor, which can survive temperatures up to 62°C, against plant pathogens Macrophomina phaseolina and Fusarium oxysporum f. sp. cumini, causing charcoal rot in cowpea and wilt in cumin, respectively. The study suggested better root colonization with both biocontrol agents in combinational treatments. Moreover, the efficiency of biocontrol agents increased when soil amendments such as radish compost, farmyard manure, and neem compost were applied alongside bio-agents (Singh et al., 2012). B. firmus was reported as a potential plant growth-promoting bacterium and specific biocontrol agent against the phytopathogen M. phaseolina, with successful field demonstrations conducted at the Central Arid Zone Research Institute, Jodhpur, Rajasthan (Lodha et al., 2013; Mawar et al., 2018). Similarly, the efficacy of T. harzianum was demonstrated against dry root rot of sesame and wilt of cumin, resulting in a significant reduction in disease incidence and increased seed yield. Significant yield promotion was observed in sesame and cumin during experimentation in various districts of Rajasthan. Additionally, a consortium of B. firmus and T. harzianum increased seed yield in guar at Jodhpur. These demonstrations have garnered wider acceptance among rain-fed farmers, particularly cumin growers under irrigated conditions (Mawar et al., 2019). Likewise, a study conducted on Indian mesquite, focusing on the arid zone tree Khejri (Prosopis cineraria Druce), to combat large-scale mortality caused by Ganoderma lucidum, identified three major biocontrol agents, including T. harzianum, T. longibrachiatum, and A. nidulans, along with two bacterial antagonists, including Streptomyces sp. strain AZAC-1 and Bacillus sp. strain AZ-11 (Mawar et al., 2021a and b).
Future challenges
This article provides polyhedral view on various subjects concerning beneficial microbes and their potential applications in agriculture sustainability. Information complied indeed demands deeper exploration for microbial reservoirs and resources with positive influence on plant health and devising proper plans for their field applications. With increasing populations and food demands, agriculture sustainability has become a topic of concern and thereby necessitates quick solutions to emerge as permanent option. However, it indeed isn’t a simple task considering the huge microbial diversity present on the planet. We have only explored a pinch of available microbial resources however information enough about their ecosystem services. Challenges for future research work concern not only exploration but the rightful application of already explored microbial species. Deeper knowledge on biology and excessive trials are required to widen their potential in a vast range of arid agricultural soils.
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Utilizing Drought-Resilient Plant Growth Promoting Microorganism for Managing Plant Diseases and Improving Soil Quality in Arid Agricultural Environments
ABSTRACT
Arid regions are characterized by extreme temperature shifts, unpredictable rainfall, strong winds, water shortages, and sandy soils, creating challenging conditions for agriculture. These conditions lead to reduced crop yields and quality, posing significant challenges to farmers and researchers alike. To address these issues, there's growing interest in harnessing microbial communities that enhance plant health and provide protection against pathogens. Plant Growth Promoting Microorganisms (PGPM) are gaining attention for their roles in bio-control, stimulating growth, boosting stress tolerance, and fostering antagonistic interactions against soil-borne pathogens. Specifically, plant growth promoting rhizobia, found in the plant root zone (rhizosphere), are noteworthy for their ability to thrive in arid conditions due to their adaptations to drought and heat. While these microbes have been studied in labs, their practical use in the field requires deeper insights into their behavior and extensive field testing.
Keywords: Biocontrol agents (BCAs), climate change; drought tolerant, soil; PGPR; soil-borne phytopathogens
INTRODUCTION
Agriculture in desert soils with scant water resources faces challenges from soil-borne pathogens, notably affecting legumes, oilseeds, and various fruit crops like Ziziphus mauritiana (ber) and date palm. Diseases such as dry root rot by Macrophomina phaseolina in legumes, wilt disease in cumin from Fusarium oxysporum f. sp. cumini, and tree mortality due to Ganoderma lucidum are prevalent. Fruit crops suffer from powdery mildew, fruit rots, and rust, leading to yield losses and economic impacts. In response, research is targeting microbial solutions to boost plant health and counteract these pathogens. This chapter explores microbial biocontrol agents, root microbiomes, and other Plant Growth Promoting Microorganisms (PGPM) from arid areas. The objective is to harness these drought- and heat-resistant PGPMs to bolster sustainable agriculture in arid regions.
Mycorrhizae, endophytes, and symbionts in plant growth promotion
The synergistic relationship between mycorrhiza and mycorrhizal-associated bacterial communities (MAB) plays a vital role in enhancing soil and plant health. This relationship improves soil nutrient allocation through MAB-assisted nutrient solubilization and prevents the intraradical colonization of soil-borne phytopathogens, particularly in arid and semi-arid regions of India. Integrating MAB with diverse plant growth-promoting rhizobacteria (PGPR) attributes such as phytohormone production, siderophores, and lignocellulose decomposing enzymes, alongside suitable mycorrhizal types, can further enhance this interaction process. This extension of microorganism applicability holds promise for sustainable plant and soil health management (Mitra et al., 2019). A study has highlighted Arbuscular Mycorrhizal Fungi (AMF) as an alternative option to conventional fertilization methods. However, successful soil inoculations require careful planning, and results may vary depending on the nature of the host plant and fungal association. Factors influencing success rates and fungal persistence include species compatibility with the soil environment, spatial competition, and inoculation timing (Berruti et al., 2016). Recent advances in genomics and transcriptomics have expanded our understanding of fungal interactions with host plants and other soil organisms, revealing various important factors. Apart from enhancing soil fertility, AMF can improve plant systemic resistance, protecting host plants against biotic stresses like plant-parasitic nematodes. This protection occurs through enhanced root tolerance, direct competition for nutrients and space, altered rhizospheric interactions, and induced systemic resistance, making AMF a potential biocontrol agent against nematode pests (Schouteden et al., 2015). Various species of mycorrhizal fungi have been isolated, with some showing higher frequencies of occurrence than others. Spore populations show correlations with root colonization, organic carbon content, and rainfall, among other factors (Oyediran et al., 2019). Apart from mycorrhizal fungi, plant root niches harbor diverse endophytic microbes that contribute to plant health. These endophytic microbes, including bacterial endophytes, have been confirmed to play a role in plant resistance against pathogens. Resistant cultivars often exhibit higher densities of bacterial endophytes, which can produce siderophores, HCN, and antibiotics, positively influencing plant health (Upreti and Thomas, 2015). Studies have demonstrated the inhibition of soil-borne pathogens by genetically modified Streptomyces spp. colonizing the rhizosphere and roots of lettuce. These transformed strains exhibit rhizospheric or endophytic behavior, showing potential for biocontrol (Bonaldi et al., 2015). Furthermore, microbial symbionts can affect plant health and contribute to the competitiveness of invasive plant species. Interactions between plants and their microbiomes hold biocontrol potential, with research focusing on developing novel microbe-based biocontrol strategies, particularly for invasive plant species like Phragmites australis (Kowalski et al., 2015).
Plant growth promoting metabolites
In pot experiments, a notable enhancement in cumin plant root length was observed when treated with Aspergillus versicolor and Trichoderma harzianum individually, as well as when integrated. However, the integration of both biocontrol agents (BCAs) with Verbisina led to increased shoot length and weight. The synergistic effect of these BCAs was evident in the enhanced shoot length and weight compared to the control group. This suggests that A. versicolor contributes to cumin root length enhancement, indicating its potential for growth promotion (Israel and Lodha, 2005). Nonetheless, further studies are necessary to fully comprehend the interaction dynamics of BCAs before drawing conclusive results. Additionally, A. versicolor releases various compounds including hydrocarbons, alcohols, ketones, ethers, and sulfur-containing compounds. Among these, sulfur-containing compounds have been identified as volatile metabolites toxic to fungal growth (Lewis and Papavizas, 1970). Furthermore, apart from antibiotics, A. versicolor also produces other metabolites (Sunsseson et al., 1995). Variations in the release of specific metabolites by different strains of BCAs, particularly those tolerant to heat, are likely. Thus, isolating and characterizing the specific metabolites released quantitatively and qualitatively by heat-tolerant strains of A. versicolor is imperative (Mawar and Lodha, 2019).
Similarly, in another pot experiment, guar seedlings treated with the bacterial bioagent Bacillus firmus exhibited significant increases in fresh and dry weights compared to both the control group and pathogen-inoculated seedlings. This evidence suggests that the bacterium effectively promotes the growth of the test plant (Lodha et al., 2013).
Microbial volatiles and other compounds in plant growth and defense
Plant roots are always in contact with soil microorganisms and flow of molecules released by them. Microbial exudates whether volatiles or particulates affect plants through variety of mechanisms such as biochemical signaling that elicits local plant defense toward soil borne pathogens or by inducing systemic resistance. Report evidenced volatile triggered secretion of plant root exudates which enhance or modulate overall plant fitness against fungi and bacteria and act as plant defense inducer. (Kai et al., 2007; Chung et al., 2016; Yi et al., 2016). Besides providing defense to plants, soil-microbes also affect plant metabolism and nutrient assimilation. A study conducted with Arabidopsis reported a novel mechanism through gene activation where plant growth-promoting (PGP) bacteria like Bacillus amyloliquefaciens GB03 activates gene responsible for sulfur assimilation and uptake by plant. Further, expression of transcripts coding for proteins which play a key role in biosynthesis of sulfur-rich aliphatic and indolic glucosinolates were reported. The increased concentration of sulfur in plants favored glucosinolate biosynthesis which in turn conferred protection against the beet armyworm Spodoptera exigua (Aziz et al. 2016). In another report, members of Lysobacter spp. were found abundantly in soils that are suppressive towards the pathogen Rhizoctonia solani and were predicted to affect soil-borne pathogens through secretions of extracellular enzymes and metabolites. The isolated strains acted antagonistically, in-vitro against phytopathogens including Rhizoctonia solani, Pythium ultimum, Aspergillus niger, Fusarium oxysporum, and Xanthomonas campestris, however not much suppression was observed in fields of sugar beet, cauliflower, onion and Arabidopsis thaliana implicating their poor rhizospheric colonization capabilities (Folman et al., 2003). The antagonistic potentials of Lysobacter spp. in disease suppressiveness need further exploration and confirmations and they could emerge as novel source of versatile antimicrobial compounds (Gómez Expósito et al. 2015). Other than providing defense against pathogenic microorganisms, several of microbial metabolites protect plants from herbivores. Foul odors and toxins from microbial exudates protect plants from gazing and act barrier for insect vectors (Mithöfer and Boland, 2012). Fungal metabolites are also known to protect plants against feeding of the cereal aphid Rhopalosiphum padi upon association by Trichoderma citrinoviride isolates. Various long chain primary alcohols (LCOHs) were reported to have phago-deterrent effect, restraining aphids from settling on treated leaves. These LCOHs act through taste receptor neurons even at low concentrations and hold potential for insect management strategies in synergy with other control parameters (Ganassi et al, 2016).
Bio control potential of PGPM
The preceding discussion highlights the presence of native heat-tolerant PGPM in the harsh climate of the Indian arid region, where soil temperatures can soar up to 55°C during summer. Despite such extreme conditions, resting structures like chlamydospores and sclerotia of soil-borne plant pathogens endure, alongside the survival of native PGPM propagules. However, there's a need to bolster the population of these PGPM to effectively combat soil-borne plant pathogens. Significant progress has been made in identifying suitable food substrates to support the survival and proliferation of these bioagents (Mawar et al., 2019). Studies conducted at the Central Arid Zone Research Institute (CAZRI) have demonstrated the compatibility of combining beneficial BCAs such as T. harzianum and B. firmus with suitable carriers and food substrates to ensure their survival (Mawar and Lodha, 2012). This combined approach offers multiple advantages, leveraging different mechanisms of biocontrol activity.
Furthermore, soil moisture plays a crucial role in the multiplication and efficacy of bioagents, particularly B. firmus. Optimal soil moisture levels significantly enhance the biocontrol activity of this bacterium. Recent interventions aimed at mitigating large-scale mortality observed in Indian mesquite trees involved a simple yet effective technique of incorporating onion residues into the soil beneath the trees, thereby fostering the multiplication of Aspergillus nidulans, a known bioagent against G. lucidum (Mawar et al., 2021). Incorporating PGPM as a biocontrol agent can be achieved through different application methods such as soil incorporation, foliar spray, seed biopriming, or seed treatment to enhance disease control. Additionally, there's a need to explore and harness more endophytic and drought-tolerant aggressive native strains of PGPM from the soil to further bolster disease management strategies.
Soil amendments in biocontrol
Variety of organic matter amendments were characterized and still under exploration for their potential to favor biocontrol agents and influence soil resident communities (Bailey and Lazarovits, 2003; Bonilla et al., 2012). Similarly, soil amended with composted almond shell reported positive effect. Amended soil suppressed growth of pathogens including Rosellinia necatrix (a causal agent of white root rot on avocado) and favored Proteobacteria, Actinobacteria and Ascomycota specifically Pseudomonas, Burkholderia spp. and Mortierellales (Vida et al. 2016). A study therefore, was undertaken to investigate survival of bio-agents, microbial population dynamics and activity, availability of micronutrients during the process of composting and in mature composts prepared from certain on-farm wastes (Mawar et al., 2020). Use of compost is an easy alternative for amending soil in arid soils where moisture retention is poor (Lodha and Burman, 2000). Efforts were also made to inactivate released propagules of M. phaseolina from infected crop residues during heat phase of composting by increasing nitrogen concentration and exposing mature compost to dry summer heat. Trichoderma harzianum disappeared during peak heating but reinfestation occurred at mature stage with maximum counts in P. juliflora compost, while Bacillus spp. was present throughout the composting period (Mawar et al., 2020). Similarly, neem cake also came out as an excellent carrier as it gave a prolonged shelf life of 200 days of T. viridae. Antifungal assay against plant pathogenic fungi revealed complete inhibition of growth and sporulation of fungal pathogens (Zope et al., 2019).
Suppressive soil and biocontrol
Once a biocontrol agent has proved its potential in control of a target pathogen, some specific aspects need investigations particularly in relation to the host and climate under which its use can be promoted. Studies are required to know its survival rate at different soil depths in fluctuating weather conditions and how other bio-ecological factors are governing population dynamics of the biocontrol agent. By generating this information, manipulation of soil environment and other associated bio-ecological factors in favor of PGPM, its population and activity can be enhanced in order to develop soil suppressiveness. Mode of action, survival in soil, growth promotion abilities of Trichoderma harzianum and T. viride as BCAs have been studied in detail. (John et al., 2010; Harman et al., 2004) but no information is available on population dynamics of A. versicolor a potent BCA. Studies on population dynamics over time and space have two basic goals: (a) to identify recurring patterns in population dynamics; and (b) to understand how these patterns are generated. Therefore, a study was undertaken to understand how biotic and abiotic factors influence population of A. versicolor at different soil depths in arid soils. Availability of organic matter and warmer temperatures at lower soil depth, in turn, favored survival of A. versicolor and other soil fungi. Positive correlation of soil moisture with fungal population has also been established by other workers (Panda et al., 1996). Variations in earlier findings can be attributed to seasonal conditions of both climates, particularly of arid region where soils are low in organic matter and temperature exceeds beyond 55°C in summer months. This is also evident from the fluctuations in A. versicolor population at lower soil depth where because of lower levels of temperature compared to upper soil depth, population continued to increase up to June (Singh et al., 2014). Occurrence of highest population in October at lower soil depth when the temperature reached 51°C is yet another evidence for the hypothesis (Singh et al., 2014). Soil suppressiveness is an uncommon property of soil to selectively affect survival of some microorganisms negatively. The infrequent phenomenon of soil suppression is known to regulate noxious organisms including root-knot nematodes Meloidogyne spp. and favor plant health (Bent et al., 2008). A number of studies have stated that Lawsonia (heena) plants can be used for suppression of the root knot nematode Meloidogyne javanica. Significant suppression of larval hatching in the nematode M. incognita by bark extract of henna has also been reported (Rafiq et al., 1991). A rich biodiversity of plants in Indian arid region has also provided a number of plants possessing insecticidal and fungicidal activity against insects, pests and diseases occurring in this region. Nature has bestowed arid region with diverse vegetation, which can be explored as botanical pesticides for soil suppressiveness. A study conducted in two organic horticulture greenhouses in Spain reported progressively decline in nematodes population with crop rotation and found associated cause as egg parasitism by the hyphomycete Pochonia chlamydosporia. Further suppressive nature of soil confirmed through the control non-sterilized soil where lower egg densities and reduced Meloidogyne reproduction was observed with higher microbial density in soil (Giné et al., 2012). However, soil suppressiveness needs more exploration to reveal its potentials for common use.
PGPM in induced resistance in plants
Plants do possess specific mechanisms to tackle attacking pests, pathogens and parasites. To escape from plant immunity, pathogens also have strategies and varying degree of virulence. Different exudates, formulations, toxin compounds and enzymes are attributed to virulence shown by pathogens. A report suggested the active role of Abscisic acid (ABA) in interactions between blast fungal pathogen Magnaporthe oryzae and the antagonistic bacterium P. chlororaphis EA105 with rice host. The pathogen, Magnaporthe oryzae-produced ABA enhanced plant susceptibility by affecting plant defense against fungi by acting antagonistically on salicylic acid (SA), jasmonic acid (JA), and ethylene signaling and thereby accelerating pathogenesis through higher rates of spore germination and appressoria formation.
Micromonospora strains have been reported to control fungal pathogens by provoking plant immunity. The strain dwells in nitrogen fixing nodules of healthy leguminous plants and posses PGP effect. This Gram-positive antifungal isolate reduced leaf infection by Botrytis cinerea through durable induced systemic resistance when inoculated on tomato roots. Further, gene expression analyses revealed mechanism of action of Micromonospora, which later confirmed using defense-impaired tomato mutants. Strain stimulated plant defense by enhancing jasmonate-regulated defense pathways and appear as extraordinary biocontrol agents with additional antifungal activity than eliciting plant immunity (Martínez-Hidalgo et al., 2015).
Report on Trichoderma parareesei transformants with reduced chorismate mutase (CM) activity (An intermediate of aromatic amino acids, essential in protein synthesis and precursor of many secondary metabolites) through Tparo7 gene silencing confirms reduced pathogen colonization by limiting growth rates and mycoparasite behavior against phytopathogenic fungi including R. solani, F. oxysporum, and B. cinerea in dual in-vitro cultures. Transformants reported to reduce susceptibility of tomato towards pathogens, also produced higher amounts of aromatic metabolites like tyrosol, 2-phenylethanol and salicylic acid (SA) (Pérez et al., 2015).
Omics approaches in PGPM
Recent advances in soil microbiology research are shedding light on the immense potential of plant growth-promoting (PGP) microbes. Cutting-edge “-omics” technologies have revolutionized our ability to gather valuable data swiftly, authentically, and cost-effectively. This enables a deeper understanding of previously unexplored interactions within rhizospheric ecosystems and the identification of novel soil microbes (Massart et al., 2015). A study investigating 12 strains of Bacillus subtilis, known for their PGP capabilities, revealed high genomic diversity, except for highly conserved strains of B. amyloliquefaciens. Genomic analysis uncovered numerous genes associated with the biocontrol and colonization capacities of these bacteria, including 73 genes involved in signaling, transport, secondary metabolite production, and carbon utilization in B. amyloliquefaciens subsp. Plantarum. Deletion of certain genes, such as those within conserved polyketide biosynthetic clusters encoding difficidin and macrolactin-like secondary metabolites, demonstrated their crucial role in reducing damage caused by pathogens like Xanthomonas axonopodis pv. Vesicatoria on tomato plants (Hossain et al., 2015). Further exploration through genome sequencing and analysis of Pseudomonas sp. SH-C52, isolated from soil suppressive to Rhizoctonia solani, unveiled its antifungal activity attributed to the chlorinated 9-amino-acid lipopeptide thanamycin. This isolate closely resembled Pseudomonas corrugata and possessed a genome size of 6.3 Mb, housing 5579 predicted open reading frames (ORFs). Notably, it harbored six non-ribosomal peptide synthetase gene clusters, including those responsible for thanamycin and brabantamide production. While thanamycin exhibited antifungal properties, brabantamide displayed anti-oomycete activity, targeting phospholipases of Phytophthora infestans. A third lipopeptide cluster, thanapeptin, exhibited activity against P. infestans with structural variations compared to known secondary metabolites, while the remaining cluster encoded unknown products. Collectively, these findings underscore the potential of SH-C52 lipopeptides, which exhibit diverse antimicrobial, antifungal, and anti-oomycete activities (Van der Voort et al., 2015).
Ameliorating arid lands through PGPM
Over decades, extensive research has been dedicated to developing sustainable management strategies for combating soil-borne plant pathogens affecting key crops and trees in arid regions. These strategies encompass various approaches, including moisture conservation techniques (Lodha, 1996), soil solarization (Lodha, 1995), utilization of soil amendments such as cruciferous residues (Mawar and Lodha, 2002) and composts (Bareja et al., 2013), screening for tolerant genotypes (Lodha and Solanki, 1992), bio-management practices, and the integration of different control methods. For instance, integrating sub-lethal heating with cruciferous residues and employing synergistic applications of chemicals with bio-control agents have shown promise (Singh et al., 2012; Mawar and Lodha, 2009). These collective efforts aim to sustain agriculture in arid zones by effectively managing soil-borne pathogens.
Growing concerns about the environmental impact of pesticide use, along with increasing pathogen resistance to these chemicals, have spurred research into microbial communities capable of tolerating arid conditions. These microbes, when associated with typical arid plants, can bolster plant resistance, improving overall plant health, production, and quality. PGPMs offer plants enhanced tolerance to various biotic and abiotic stresses. They also boost plant immunity and improve nutrient uptake and assimilation capabilities, as illustrated in Figure 1.
Soil samples were gathered from various arid ecosystems and subjected to analysis to isolate effective drought-tolerant bio-agents. Among the native biocontrol agents identified to exhibit antagonistic effects in vitro were Trichoderma harzianum, T. longibrachiatum, Aspergillus versicolor, A. nidulans, Bacillus firmus, B. tequilensis, and Streptomyces mexicanus (Mawar et al., 2017; Lodha et al., 2019; Mawar et al., 2021a; Mawar et al., 2021b). However, the field efficacy of these identified bio-agents on major arid crops and their impact on soil resident microflora necessitates extensive field trials and further understanding of their behavior. Various soil amendments and natural residues, including food substrates, have been explored to enhance the survival of these agents in arid soil. The mechanisms through which these agents exhibit antagonism include direct operations such as parasitism, antibiosis, and competition, as well as indirect effects through manipulating the host rhizosphere, reducing host susceptibility, secreting exudates, resistance through host-mediated interactions, hypovirulence, and plant growth-promoting effects.
A two-year study was conducted to assess the collective effect of two different drought-tolerant biocontrol agents, Bacillus firmus and Aspergillus versicolor, which can survive temperatures up to 62°C, against plant pathogens Macrophomina phaseolina and Fusarium oxysporum f. sp. cumini, causing charcoal rot in cowpea and wilt in cumin, respectively. The study suggested better root colonization with both biocontrol agents in combinational treatments. Moreover, the efficiency of biocontrol agents increased when soil amendments such as radish compost, farmyard manure, and neem compost were applied alongside bio-agents (Singh et al., 2012). B. firmus was reported as a potential plant growth-promoting bacterium and specific biocontrol agent against the phytopathogen M. phaseolina, with successful field demonstrations conducted at the Central Arid Zone Research Institute, Jodhpur, Rajasthan (Lodha et al., 2013; Mawar et al., 2018). Similarly, the efficacy of T. harzianum was demonstrated against dry root rot of sesame and wilt of cumin, resulting in a significant reduction in disease incidence and increased seed yield. Significant yield promotion was observed in sesame and cumin during experimentation in various districts of Rajasthan. Additionally, a consortium of B. firmus and T. harzianum increased seed yield in guar at Jodhpur. These demonstrations have garnered wider acceptance among rain-fed farmers, particularly cumin growers under irrigated conditions (Mawar et al., 2019). Likewise, a study conducted on Indian mesquite, focusing on the arid zone tree Khejri (Prosopis cineraria Druce), to combat large-scale mortality caused by Ganoderma lucidum, identified three major biocontrol agents, including T. harzianum, T. longibrachiatum, and A. nidulans, along with two bacterial antagonists, including Streptomyces sp. strain AZAC-1 and Bacillus sp. strain AZ-11 (Mawar et al., 2021a and b).
Future challenges
This article provides polyhedral view on various subjects concerning beneficial microbes and their potential applications in agriculture sustainability. Information complied indeed demands deeper exploration for microbial reservoirs and resources with positive influence on plant health and devising proper plans for their field applications. With increasing populations and food demands, agriculture sustainability has become a topic of concern and thereby necessitates quick solutions to emerge as permanent option. However, it indeed isn’t a simple task considering the huge microbial diversity present on the planet. We have only explored a pinch of available microbial resources however information enough about their ecosystem services. Challenges for future research work concern not only exploration but the rightful application of already explored microbial species. Deeper knowledge on biology and excessive trials are required to widen their potential in a vast range of arid agricultural soils.
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Mawar R, Kumar M, Lodha S (2020) Changes in Temperature, Microbial Population and Activity during the Process of Composting.
Mawar R, Ladhu Ram, Sharma D, Jangid K (2021 b). Bacterial antagonists against Ganoderma lucidum . Indian Phytopathology 74(3), 843-848
Mawar R, Sharma D, Ladhu Ram (2021 a) Potential of biocontrol agents against Ganoderma lucidum causing basal stem rot in mesquite (Prosopis cineraria) growing in arid region of India. Journal of Forestry Research 32, 1269–1279 DOI 10.1007/s11676-020-01161-3 (ISSN 1007-662X)
Mawar R, Tomer A S, Dheeraj Singh (2019). Demonstration of efficacy of bio-control agents in managing soil-borne diseases of various crops in arid region of India. In special issue of Fusarium.Indian Phytopathology 72: 699-703.
Mawar R and Lodha S (2019) Native bio-agents: An integral component for managing soil borne plant pathogens in arid region. pp 97-113 In: Microbial Antagonists: Their Role in Biological Control of Plant Diseases (Eds: Pandey et al) Today & Tomorrow Publisher, New Delhi.
Mawar R, Singh V, Lodha S (2017) Combining Food Substrates for Improved Survival of Aspergillus versicolor, a Bio-agent. Bio-pesticide International 13:140-148.
Mawar R and Sanyal A (2021). Problem, Concern and Approaches of Plant Disease Management in Arid Zone In: Plant Disease Management Strategies (Eds: Sampat Nehra) p. 119-154 Agrobios Research: An Imprint of Agrobios (India), Jodhpur
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Oyediran O K, Kumar AG and Jain N, 2018. Arbuscular mycorrhizal fungi associated with rhizosphere of tomato grown in arid and semi-arid regions of Indian desert. Asian J. Agric. Res., 12: 10-18.
Pérez E, Rubio MB, Cardoza RE, Gutiérrez S, Bettiol W, Mont E, Hermosa R (2015) The importance of chorismate mutase in the biocontrol potential of Trichoderma parareesei. Front. Microbiol. 6:1181. doi: 10.3389/fmicb.2015.01181
Schouteden N, De Waele D, Panis B, Vos CM (2015) Arbuscular Mycorrhizal Fungi for the Biocontrol of Plant-Parasitic Nematodes: A Review of the Mechanisms Involved. Front. Microbiol. 6:1280. doi: 10.3389/fmicb.2015.01280
Singh V, Mawar R, Lodha S (2012) Combined effect of biocontrol agents and soil amendments on soil microbial populations, plant growth and incidence of charcoal rot on cowpea and wilt on cumin. Phytopathologia Mediterranea 51 (2): 307-316
Singh V, Mawar R, Lodha S. (2014). Influence of bio-ecological factors on population dynamics of a native bio control agent Aspergillus versicolor in arid soil. Indian phytopathology 67 : 86-91.
Upreti R, Thomas P (2015) Root-associated bacterial endophytes from Ralstonia solanacearum resistant and susceptible tomato cultivars and their pathogen antagonistic effects. Front. Microbiol. 6:255. doi: 10.3389/fmicb.2015.00255
Van Der Voort M, Meijer HJG, Schmidt Y, Watrous J, Dekkers E, Mendes R, Dorrestein, PC, Gross H, Raaijmakers JM (2015) Genome mining and metabolic profiling of the rhizosphere bacterium Pseudomonas sp. SH-C52 for antimicrobial compounds. Front. Microbiol. 6:693. doi: 10.3389/fmicb.2015.00693
Vida C, Bonilla N, de Vicente A, Cazorla FM (2016) Microbial Profiling of a Suppressiveness-Induced Agricultural Soil Amended with Composted Almond Shells. Front Microbiol. 7:4. doi: 10.3389/fmicb.2016.00004. PMID: 26834725; PMCID: PMC4722121.
Zope VP, Jadhav HP, Sayyed RZ (2019) Neem cake carrier prolongs shelf life of biocontrol fungus Trichoderma viridae, Indian J. Exp Biology, 57(5):372-375.