Regulatory mechanisms of plant rhizobacteria on plants to the adaptation of adverse agroclimatic variables

The mutualistic plant rhizobacteria which improve plant development and productivity are known as plant growth-promoting rhizobacteria (PGPR). It is more significant due to their ability to help the plants in different ways. The main physiological responses, such as malondialdehyde, membrane stability index, relative leaf water content, photosynthetic leaf gas exchange, chlorophyll fluorescence efficiency of photosystem-II, and photosynthetic pigments are observed in plants during unfavorable environmental conditions. Plant rhizobacteria are one of the more crucial chemical messengers that mediate plant development in response to stressed conditions. The interaction of plant rhizobacteria with essential plant nutrition can enhance the agricultural sustainability of various plant genotypes or cultivars. Rhizobacterial inoculated plants induce biochemical variations resulting in increased stress resistance efficiency, defined as induced systemic resistance. Omic strategies revealed plant rhizobacteria inoculation caused the upregulation of stress-responsive genes—numerous recent approaches have been developed to protect plants from unfavorable environmental threats. The plant microbes and compounds they secrete constitute valuable biostimulants and play significant roles in regulating plant stress mechanisms. The present review summarized the recent developments in the functional characteristics and action mechanisms of plant rhizobacteria in sustaining the development and production of plants under unfavorable environmental conditions, with special attention on plant rhizobacteria-mediated physiological and molecular responses associated with stress-induced responses.


Introduction
Plant rhizobacteria-mediated abiotic stress reduction occurs directly through hormone induction or indirectly via signaling in the host plant.The direct function in nitrogen fixation, phosphate solubilization, auxin, cytokinin, gibberellin, and abscisic acid production are all documented.It also makes it easier for necessary mineral elements to be absorbed from the rhizospheric soil along with the production of plant growth regulators.However, the indirect roles include the production of metabolites, siderophores, antibiotics, volatile HCN, etc.Some of the compounds that the microbes may produce include deaminase enzyme, microbiocidal enzyme, siderophores, plant hormones, and PO 4 -solubilizing enzyme (Gujral et al., 2013;Ekinci et al., 2014;Saleem et al., 2015;Kumari and Khanna, 2016;Moustaine et al., 2017).Plants have unique microbiota, and the microbial structure in the rhizosphere is influenced by the bacteria and plants' production of signal molecules and the chemical composition of root exudates (Zhang et al., 2017;Jalmi and Sinha, 2022).Plant-growth regulators, phytohormones, and various secondary metabolites can be produced by PRs to stimulate plant development (Islam et al., 2014;Kaushal and Wani, 2016) (Figure 1).
The upregulated synthesis of metabolites, such as phytohormone, exopolysaccharides, siderophores, antioxidant enzymes, and volatile compounds, primarily minimizes plant resistance to environmental challenges.The production of phytohormones by rhizobacteriainoculated plants, including cytokinins (CK), gibberellic acid (GA), indole-3-acetic acid (IAA), and abscisic acid (ABA) is employed during plant stressed conditions.1-aminocyclopropane-1carboxylate (ACC) deaminase plays a significant role in conferring stress resistance capacity to plants by downregulating the level of stress-induced ethylene level in plant roots system (Etesami and Maheshwari, 2018;Shahid et al., 2023).Plant-rhizobacteria downregulated the effects of abiotic stresses by modifying the expression of genes associated with the biosynthesis of hormones, i.e., ACO and ACS genes (ethylene biosynthesis), MYC2 (Jasmonate), PR1 (SA), genes encoding antioxidant enzymes, transcription factor NAC1, etc. (Tiwari et al., 2017) (Tables 1, 2).Extensive field trials are required to investigate the interaction between the functional activities of signaling networks and their association.The interaction between PRs and plants based on various factors, such as root composition, strains of bacteria, and exudation patterns from their roots (Kumar et al., 2019).Numerous secondary metabolites and root exudates depend as chemo-attractants in the rhizosphere, attracting beneficial soil bacteria and inhibiting phytopathogens, thereby stimulating a delicate network of signaling between microbes and plants (Ullah et al., 2021;Joshi et al., 2022;Mellidou and Karamanoli, 2022;Joshi et al., 2023).The physiological and molecular responses activated in plants in response to stress resistance are regulated by various key genes with metabolic and regulatory roles.Research demonstrations focusing on plant gene expression following plant-rhizobacteria inoculation may help understand which can be an effective environmentally friendly approach to alleviate the adverse environmental variables (Ferrante  , 2023;Verma et al., 2023).The formation of the enzyme ACC deaminase by rhizobacteria and reduction in ethylene level had been the main function for enhanced plant growth and resistance ability during different stresses (Bharti et al., 2014;Jalmi and Sinha, 2022).
Eco-physiological and omic responses of plant rhizobacteria required more attention and extensive field research demonstrations to increase stress resistance efficiency.Hence, the present article focused on the interactions between plants and rhizobacteria and their impact on tolerance to adverse agroclimatic variables for agricultural sustainability in an ecofriendly environment.

Impact of plant development, biomass, and productivity
Plant rhizobacteria (PRs) effectively improve plant morphological structures during adverse environmental conditions.Abiotic stresses, such as acidic and alkaline soil, insufficient water supply, low and high temperature, UVradiation, soil flooding, and contaminated/toxic soil, affect agronomic, anatomical, cellular, and metabolic activities (Glick et al., 2007;Verma et al., 2020a, b).Higher levels of phytohormones, defense-related proteins and enzymes, antioxidants, and epoxypolysaccharides cause PGPR-induced resistance (Kaushal and Wani, 2016).It is accomplished by changing transcriptional and signaling processes, which lead to altered gene expression when PRs are present.Because PRs produce phytohormones that change root shape and improve root development, surface area, uptake, and accumulation of nutrients, plant productivity increases in the presence of PRs (Mellidou and Karamanoli, 2022).They can also increase total plant productivity by helping to induce ACC-deaminase activity in plants.The potential of PRs enhancing plant growth and development varies due to differences in their properties, such as ACC-deaminase activity, IAA generation, root colonization, P-solubilization, etc (Ghosh et al., 2018;Gupta and Pandey, 2019).The defense mechanisms of plants against unfavorable agroclimatic conditions depend on the variation in the development of roots (Khoshru et al., 2023).Different PGPR strains can enhance the overall root system by increasing the total number of root tips, surface area, and structure of the roots under stressful conditions (Brambilla et al., 2022).Lowering the ethylene content increases the plant's capacity to withstand stress by facilitating improved nutrition and water uptake capacity (Chieb and Gachomo, 2023) (Figure 1).
When under stress, PRs also improve the uptake of water and nutrients.The absorption of nutrients and antioxidant activities are associated with stress management.By diminishing the negative consequences of saline soil, inoculation with Klebsiella oxytoca (Rs-5) containing ACC-deaminase boosted plant establishment and increased the absorption of key mineral nutrients (Yue et al., 2007;Zahir et al., 2012).In a similar way, Pseudomonas spp.inoculation increased the antioxidative enzymatic activities and promoted the growth of plants during unfavorable climatic conditions (Fu et al., 2010;Jalmi and Sinha, 2022) (Table 1).
According to Zahir et al. (2009) and Orozco-Mosqueda et al. ( 2020), rhizobacterial strains have been explored to have a substantial influence on the improvement of a variety of plants,  (Kang et al., 2019).
It can be indicated by the significantly increased levels of chlorophyll, total phenolics, flavonoids, soluble sugars, protein contents, and antioxidative enzymatic activities, as well as the higher expression of stress-related genes, that resulted from inoculating Cd-stressed with Serratia marcescens BM1 in Glycine max L. plants.Phaseolus vulgaris subjected to the rhizobacterial consortia experienced reduced stress caused by salinity and improved overall plant growth and photosynthetic pigments (Gupta and Pandey, 2019).In tomato plants, Streptomyces sp. has been shown to reduce stress and promote growth (Palaniyandi et al., 2014).It has been observed that Burkholderia phytofirmans helps plants under drought stress (Naveed et al., 2014).They generate exopolysaccharides (EPS) during water-deficit conditions, enhancing seed germination and growth.Of all the strains, Pseudomonas fluorescens has the highest capacity to produce EPS and ACC deaminase.The saline rice field was employed by Sultana et al. (2020) to isolate rhizobacterial strains, which they found to enhance stomatal conductance, transpiration, and photosynthetic CO 2 assimilation rate, all of which contributed to increased crop yield, fruit and grains quality.According to the latest research, Azospirillum brasilense Sp245 increased Arabidopsis thaliana growth, suggesting that MAMPs produced from plant-  1, 2).

Photosynthetic leaf gas exchange and chlorophyll fluorescence efficiency
Plant-rhizobacteria enhance inoculated plants' photosynthetic response and leaf gas exchange capability during stress (Verma et al., 2020b;Jalmi and Sinha, 2022).By modifying the photosynthetic characteristics, osmolytes production, antioxidant machinery, and expression of stress-related genes, inoculating soybean plants with Serratia marcescens BM1 (PR) provides Cd tolerance to plants (El-Esawi et al., 2020).Under salt stress, Bacillus amyloliquefaciens SQR9 has demonstrated higher efficiency in photosynthesis and overexpression of the RBCS and RBCL genes in Zea mays plants (Chen et al., 2016).During bacterial strain inoculation, Arabidopsis helleri showed elevated photosynthesis and proteins associated with abiotic stress (Khan et al., 2021).
Enhanced photosynthetic pigments and the expression of important genes (RBCS and RBCL) regulating RUBISCO activities during stress condition (Sherin et al., 2022;Amaral et al., 2023).By modulating ion homeostasis, redox potential, photosynthetic CO 2 assimilation rate, and the expression of stress-related genes, maize plants inoculated with Serratia liquefaciens KM4 revealed enhanced growth and stress tolerance (El-Esawi et al., 2018).Reduced phenol, flavonoid, and leaf relative water content and photosynthetic responses in maize plants have resulted from salinity stress, which also decreased root damage and water uptake.However, inoculating maize under salt stress with Serratia liquefaciens KM4 enhanced LRWC, photosynthetic characteristics, and the biosynthesis pathways of phenols and flavonoids, enhancing plant stress tolerance efficiency.In comparison to uninoculated plants, rhizobacteria-inoculated maize and white clover have demonstrated enhanced photosynthesis, soluble proteins, sugars, and enzymatic activities following inoculation with HAS31 rhizobacteria (Han et al., 2014) (Figure 1; Table 1).

Uptake and accumulation of mineral nutrients and water balance
By altering the solubility and absorption of nutrients, PRs improve the bioavailability of nutrients in plants under abiotic factors.Through N 2 -fixation, mobilization, and the promotion of N 2 -fixers through their secretions, several rhizobacteria can reduce the volume of nitrogen (N 2 ) supplementation required for plant growth (Shah et al., 2022;Khoso et al., 2024).Additionally, they change the shape and surface area of the roots, improving nitrogen bioavailability (Olenska et al., 2020).Elevating ammonium transporters' expression improves nutritional absorption during stresses (Calvo et al., 2019).According to Gomez-Godıńez et al. (2023), phosphorus (P) solubilizing PRs, such as Azotobacter, Bacillus, Burkholderia, Erwinia, Pseudomonas, Serratia, and Rhizobium, generate organic acids that chelate P-bound cations and make it available to plant roots.Furthermore, under Fedeficient conditions, PRs assist in acquiring iron (Fe) by generating siderophores, which are low molecular weight organic molecules (Mohanty et al., 2021).Reducing metal ion availability and decreasing metal uptake, siderophores that generate PRs enhance plants' survival under heavy metal stress (Dimkpa et al., 2009;Kumar et al., 2021) (Tables 1, 2).
Ocimum basilicum L. has demonstrated the ability of PRs to enhance nutrient absorption and downregulate abiotic stresses (Rakshapal et al., 2013).Under salinity stress, PRs, such as Pseudomonas sp. and Azospirillum sp., increase nutrient availability, improving plant growth, biomass, and productivity (Noorieh et al., 2013).The application of rhizobial inoculants has been observed to trigger delayed senescence, as evidenced by higher potassium (K) ion levels and lower ethylene and cytokinin production.In plants with a higher K + /Na + ratio, PRs boost the absorption of K + ions by synthesizing AtHKT1, a high-affinity ion channel that promotes stress tolerance (Mahmud et al., 2021) (Figure 1).
According to dos Santos et al. ( 2020), gibberellin-releasing PRs such as Azospirillum, Shingomonas, Bacillus amyloliquafaciens, and Bacillus pumilus can also promote plant growth and yield.Regulation of abscisic acid also played a significant role in stress resistance capacity influenced by rhizobacteria (Herrera-Medina et al., 2007).When pepper (Capsicum annum) is inoculated with Serratia nematodiphila (that produces gibberellin), the plant expands more under low-temperature stress, releases more GA 4 and ABA, and lower salicylate and jasmonate activities (Kang et al., 2015).
The plant and bacterial species may impact the mechanism of ABA-mediated tolerance to stressful conditions.Under abiotic stress, specific PRs (strains of Rhizobium spp., B. pumilus, B. lycheniformis, Achromobacter xylosoxidans, and Azospirillium brasiliense) serve as ABA-stimulators or ABA-producers (Salomon et al., 2014;Egamberdieva et al., 2017).It can assist plants minimize water loss by activating Ca +2 channels that cause stomatal closure (Goswami and Deka, 2020;Grover et al., 2021).Greater ABA biosynthesis has been observed in Arabidopsis plants inoculated with the spermidine-producing B. megaterium strain (Zhou et al., 2016).By upregulating the gene expression that regulates ABA production, the rhizobacteria inoculation of rice with Pseudomonas fluorescens enhanced the plant's resistance to stress.The upregulation of TaWRKY and TaMYB expression in ABAsignaling cascades has also been observed.It has also been suggested that specific rhizobacteria can use ABA as a carbon and energy source, limiting ABA uptake throughout the plant organs.These results indicated the changes in ABA-mediated signaling pathways as a means by which inoculated plants can survive abiotic challenges (Olenska et al., 2020;Mellidou and Karamanoli, 2022) (Figure 1).
It has also been demonstrated that using rhizobacteria minimizes the negative effects of ethylene generated under abiotic stress circumstances (Grichko and Glick, 2001;Nadeem et al., 2007;Zahir et al., 2008).Under abiotic stresses, rhizobacteria-inoculated plants have been demonstrated to modify ethylene biosynthesisrelated gene expression (Lephatsi et al., 2021;Verma et al., 2021;Fadiji et al., 2022).Plants can be spared the toxicity of ethylene through the presence of rhizobacteria that contain ACC deaminase, which can hydrolyze ACC, the precursor of ET (Mellidou and Karamanoli, 2022).
The impact of Paenibacillus lentimorbus B-30488 inoculation on the reduction of abiotic stress in Arabidopsis thaliana, as well as by modifications in plant hormones and RSA-related gene expression.According to Khoshru et al. (2023), specific PRs also generate polyamines, which enhance root architecture and promote stomatal conductance and photosynthesis.The microbial community in the rhizosphere is mainly influenced by the exudates produced by plant roots, such as organic acids, mucilage, carbohydrates, sugars, and proteins, which also confer tolerance to inoculated rhizobacterial plants (Backer et al., 2018).Under abiotic stress, Azospirillum sp. has been demonstrated to accumulate appropriate solutes such as glutamate, proline, glycine, betaine, and trehalose (Saleena et al., 2002).Phaenibacillus polymyxa has been shown to possess the drought-responsive gene ERD15 (Timmusk and Wagner, 1999).Conjugated phytohormones and flavonoids in root tissue can be extracted or hydrolyzed by Azospirillum, releasing them in their active forms (Spaepen et al., 2007;Dardanelli et al., 2008;Saikia et al., 2010;Fahad et al., 2015).
The mechanisms of photosynthetic activity, hydraulic conductance, osmotic accumulation, and sequestering toxic ions are associated with rhizobacteria-stimulated resilience to stress (Figure 1).Groundnut inoculated with Bradyrhizobium under drought conditions demonstrated stress resistance due to amino acids produced from the nitrogenase to catalyzed the conversion of atmospheric nitrogen (N 2 ) to ammonia (NH 3 ) ions (Delfini et al., 2010;Enebe and Babalola, 2018).Furthermore, nitrogenase assists the supply of nitrogen to inoculated legumes, and these plants have been shown to produce more leaves due to more root nodules (Ferreira et al., 2011).To avoid desiccation, lower toxicity, and promote root growth, PRs also generate polysaccharides (Arora et al., 2010).A vital aspect of stress mitigation under environmental stress at the plant rhizosphere consists of forming biofilm and exopolysaccharide.One fascinating strategy PRs employ to mitigate the impacts of heat stress in plants involves the induction of osmoprotectants and heat shock proteins (HSPs) (Enebe and Babalola, 2018).Under stressful conditions, pepper plants treated with gibberellin-producing rhizobacteria showed a reduction in the level of salicylate and jasmonate.When the bacteria Burkholderia phytofirmans occurs, tomato plants produce more phenolics, proline, and starch under stress (Issa et al., 2018).
In plants under abiotic stress, PRs also improve proline synthesis.Arthrobacter, Bacillus, and Burkholderia are the main rhizobacteria that synthesize proline.Better stress tolerance in rhizobacteria-inoculated plants is mostly due to increased dissolved sugar levels and solute storage.Other potential strategies to reduce oxidative stress include stabilizing membranes, protein-protein complexes, and osmolytes, such as proline, glycine betaine, amino acids, and total sugars (Chieb and Gachomo, 2023).

Influence of enzymatic, nonenzymatic, and lignin biosynthesis
The synthesis of the enzyme ACC deaminase is a well-known mechanism for rhizobacteria-led abiotic stress tolerance (Etesami et al., 2015;Gupta and Pandey, 2019).By lowering ABA levels, plants inoculated with ACC-producing PRs expand more rapidly; the growth hormones regulate the synthesis of secondary metabolites (Kang et al., 2019).By promoting the activity of antioxidant enzymes (SOD, APX, and CAT) and upregulating the genes involved in the ROS pathway, it enhanced stress tolerance (Habib et al., 2016).Because ethylene causes stress-induced H 2 O 2 accumulation and apoptosis induction, ACC deaminase-producing PRs provide plants resistance against abiotic stress by lowering ethylene synthesis.It has been observed that inoculating different crops under stress with strains that include ACC-deaminase enhances plant development (Li et al., 2017;Singh and Jha, 2017;Namwongsa et al., 2019;Danish et al., 2020;Mellidou et al., 2021;Mellidou and Karamanoli, 2022).
Plant-to-microbe communication also occurs by an array of non-hormonal signaling molecules.Microbes produce volatile compounds (VOCs), signaling molecules that control plant growth and modify soil and plant health in response to stress (Ullah et al., 2021).Moreover, plants tolerate heavy metal stress due to rhizobacteria-releasing extracellular polymeric substances (EPS), which primarily help by lowering the metals' bioavailability in the soil (Mishra et al., 2017).Some species of Bacillus, Azotobacter, Burkholderia, Enterobacter, and Pseudomonas can reprogram plants' redox states, increasing their tolerance to environmental stresses.During stress, the overproduction of reactive oxygen species (ROS) changes redox states and causes DNA damage, proteins, and membrane fluidity, ultimately resulting in cell death.However, plants inoculated with PRs defended against abiotic stressors by activating their defense mechanisms.
Additionally, rhizobacteria are essential in reducing oxidative damage caused by various stressors, including heavy metals, water deficit, low and high temperatures, salt, and water scarcity.By lowering ROS levels in plant roots, rhizobacteria-induced antioxidant enzymes assist in reducing the stressors that plants experience in the environment.Additionally, they accelerate the growth rate in response to abiotic stressors by promoting the generation of antioxidant enzymes.Better stress tolerance in inoculated plants may be due to increased activities of antioxidant enzymes, such as catalase (CAT), ascorbate peroxidase (APX), or glutathione peroxidase (GPX) (Mellidou et al., 2021;Swain et al., 2021;Fadiji et al., 2022).Ascorbate peroxidase increased when tomato seedlings were inoculated with Enterobacter and subjected to abiotic stress.Gladiolus plants treated with rhizobacteria revealed increased levels of CAT and SOD activities as compared to their control group (Figure 1).
Tomato seedlings inoculated with P. oryzihabitans AXSa06 (having ACC deaminase) experienced mild oxidative stress and enhanced lipid peroxidation to trigger the antioxidant machinery (Mellidou et al., 2021).Under abiotic stress, tomato plants inoculated with a strain of Sphingomonas sp.revealed reduced lipid peroxidation, increased glutathione levels, and antioxidant enzyme activities (Halo et al., 2015;Mellidou and Karamanoli, 2022).In contrast, rhizobacteria inoculation has been demonstrated in additional studies to decrease the production of ROS-scavenging or stress-responsive enzymes that are important for plant protection in stressful environments (Gupta and Pandey, 2019;Goswami and Deka, 2020;Song et al., 2021;Verma et al., 2022a, b, c).The generation of defensive enzymes like chitinase and glucanase to the rhizobacteria stress-tolerance mechanism (Garcıá-Fraile et al., 2015).Glycine max plants inoculated with Bacillus firmus SW5 exhibit stress tolerance through alterations in root ultrastructure, antioxidant levels, and stress-related gene expression (El-Esawi et al., 2020).The production of oxalic acid, gluconic acid, and citric acid by stressed rhizobacteria plays a crucial role in the mobilization of heavy metals.Biofilm-forming rhizobacteria were inoculated into Spartina densiflora plants, resulting in increased levels of SOD, CAT, and APOX activities as well as a decrease in the induced oxidative stress index (OSI) (Perez et al., 2019;Khan et al., 2021;Bhat et al., 2022).
In Cicer arietinum plants, Pseudomonas putida MTCC5279 has been shown to reduce stress by enhanced ROS scavenging ability, modulation of membrane integrity, and accumulation of osmolyte (proline, glycine, betaine).These findings have also been validated by differential expression of genes involved in dehydrationresponsive element binding, transcription factors expressed under abiotic stress, salicylic acid, jasmonate, transcription activation, SOD, CAT, APX, and GST (Tiwari et al., 2016;Chieb and Gachomo, 2023).In Abelmoschus esculentus plants, the presence of ACC-producing PRs was associated with increased activities of antioxidant enzymes (SOD, APX, and CAT) and up-regulated genes of the ROS pathways (CAT, APX, GR, and DHAR) (Habib et al., 2016).These pathways have also been linked to enhanced POD/CAT activity, decreased cell death, and increased glutathione levels for ROS scavenging.When Dietzia natronolimnaea was inoculated into wheat (Triticum aestivum), it was observed that the ABA-signaling cascade genes, ion transporters, salt overly sensitive (SOS) pathway, and antioxidant enzymes upregulated (Bharti et al., 2016) (Figure 1).

Conclusion and future prospects
Adverse environmental variables severely affect crop growth, development, and output and downregulate the overall socioeconomic growth of sustainable agriculture.Different application strategies have been developed to challenge stress, its benefits, and its applications.Nowadays, the requirement for higher food grain productivity and safety, enhanced plant yield, fertility of soil properties, and agricultural sustainability are upregulating.The research demonstrations are shifting toward soil rhizospheric-biobased engineering to facilitate a better pollution-free environment for combining plants and rhizobacteria.The application of PRs is more beneficial in overcoming stressed conditions besides providing other significant direct and indirect ways to upregulate overall plant responses.PRs are more convenient, economical, and eco-enviro-friendly and can be applied in small cultivating areas to large fields.Variations in the modifications of plant responses under stress have been observed in inoculated plants, and these variations are dependent on the PRs mode of action, which represents the multifactorial processes regulated in stressful environments.The positive symbiotic associanship that plants develop with microbial physiology is fundamental for the plant development, especially in terms of biotic and abiotic stresses.It is necessary to set up deeply extensive field research demonstrations to understand better the interaction between the PRs-mediated signal and the metabolic/ molecular reprogramming that improves plant tolerance to unfavorable environmental variables.Multi-strain bacterial strains can be substantial if a single strain of bacteria is not more significant in reducing stress resistance efficiency.The application, duration, and applicability of inoculation are more crucial as unmanaged methods may lead to consistent and correct results.Its successful agro-commercialization will based on the involvement of plant physiologists, plant biologists, plant pathologists, biotechnologists, agro-industrialists, and farmers.A better and deep understanding of the action mechanisms and interactions of plants and associated plant rhizobacteria directly in the matrix of interest can be favored by the adoption of a holistic approach that uses "omic" applications.

TABLE 1
PR-mediated abiotic stress reduction in crop plants and their tolerance mechanism.

TABLE 2
PR-mediated biotic stress reduction in crop plants and their tolerance mechanism.