1 Introduction

As the main food crop for more than half of the world's population, the yield and quality of rice are directly related to global food security. However, its production is subject to a variety of abiotic stresses such as drought, cold, and heavy metal pollution, which not only significantly reduce the yield and quality of rice, but also may lead to the accumulation of harmful substances such as cadmium (Cd) and arsenic (As) in the edible part, posing a threat to human health (Ding et al., 2019). Therefore, researching and improving the stress resilience of rice is essential to ensure food security, especially in the context of climate change and increasing environmental pollution.

Methods to improve rice stress resistance mainly focus on the development of rice varieties tolerant to abiotic stress and optimization of planting techniques. For example, biochemical inducers and beneficial rhizosphere bacteria have shown promising prospects in improving rice tolerance to cold and drought stresses (Kakar et al., 2016). Enhancing the uptake of silicon and calcium in rice can help improve rice resistance, enhance the resistance of rice stalks to iodine, and resist diseases and pests (Huang et al., 2012). In addition, managing the composition of the rhizosphere bacterial community can reduce the accumulation of harmful heavy metals in rice, thereby improving crop yield and safety (Huang et al., 2021).

In this review, we systematically analyzed the role of rice roots and rhizosphere microorganisms in the process of stress resistance, including the morphological and physiological adaptation changes of roots under stress conditions, the composition and function of rhizosphere microbial communities, and the interaction mechanism between root exudates and microorganisms. The case study will explore the synergistic effect of roots and microorganisms under stresses such as drought, salinity, and disease and its impact on rice stress resistance. It is expected that this review will provide new ideas and methods for improving rice stress resistance, and provide a scientific basis for the application of microbial inoculants and genetic engineering technologies in agricultural practice.

2 Root Physiology and Stress Response of Rice

2.1 Root morphological changes under stress

When exposed to various abiotic stresses such as salinity, drought and heavy metals, rice roots undergo significant morphological changes. For example, under salinity, drought and heavy metal stress, rice roots showed changes in root structure, including changes in root length, surface area and volume. These changes are essential to enhance the plant's ability to absorb water and nutrients in the face of adversity (Santos-Medellín et al., 2017; Gupta et al., 2023). Moreover, the presence of beneficial microorganisms in the rhizosphere can further affect root morphology. For example, endophytes and rhizosphere bacteria have been shown to improve root parameters such as root length and root volume under saline-alkali stress (Gupta et al., 2023).

2.2 Physiological adaptation of rice roots to stress

Rice roots exhibit multiple physiological adaptations in response to abiotic stresses. A key adaptation is to regulate ion transport to maintain ion homeostasis in plants. For example, under salt stress, rice with mutant SST gene exhibited increased potassium accumulation and decreased sodium accumulation, which is essential for maintaining a stable intracellular environment (Lian et al., 2020). In addition, rice roots can enhance their antioxidant enzyme activities, such as catalase (CAT), superoxide dismutase (SOD), and peroxidase (POD), to alleviate oxidative stress caused by abiotic factors (Jain et al., 2020; Gupta et al., 2023). Under drought stress, root auxin (IAA) and zeatin riboside (ZR) decreased, and the content of cytokinin (CTK) decreased significantly, but the content of abscisic acid (ABA) increased. The reduction of IAA and CTK can reduce the growth rate of the plant and reduce the need for water. Beneficial microorganisms such as Bacillus and Aspergillus can further enhance these physiological responses by stimulating the plant's defense mechanisms (Jain et al., 2020).

2.3 Genetic and molecular basis of root stress response

The genetic and molecular basis of rice root stress response involves the regulation of specific genes and signaling pathways. For example, SST genes in rice play a key role in shaping rhizosphere microbial communities and regulating soil metabolites, which in turn affect plant responses to salt stress (Figure 1). Genetic and microbial community analysis revealed significant changes in rhizosphere bacterial communities under salinity stress, which contributes to the improvement of ionic homeostasis in rice plants. Furthermore, potential strategies for using microbial management and genetic modification to enhance crop stress resistance were proposed (Lian et al., 2020). In addition, the expression of stress-responsive genes such as OsPIP1, MnSOD1, and CATa are regulated under salt stress, enhancing the overall stress resistance of plants (Gupta et al., 2023). The recruitment of specific microbial groups by aluminum-tolerant rice genotypes also highlights the genetic basis of root-microbial interactions in enhancing stress tolerance (Xiao et al., 2022). Plant growth-promoting rhizobia (PGPR) and fungi with good characteristics including rhizobia, mycorrhizal fungi, and trichoderma, which have been successfully applied in agriculture to enhance nutrient absorption, fight pathogens, and promote growth (Genre et al., 2020; Yang et al., 2022; Woo et al., 2023). In addition, the presence of arbuscular mycorrhizal fungi (AMFs) can affect gene expression associated with nutrient uptake and stress resistance, thereby improving plant resistance to heavy metal stress (Hao et al., 2021). AMF is also involved in the regulation of specific metabolic pathways in the root system of host plants, promoting the synthesis and secretion of terpenes and phenolic compounds, as well as the deposition of resistant substances such as phytoantitoxin and lignin, thereby inhibiting the growth and reproduction of pathogenic bacteria (Chen et al., 2021).

Figure 1 (A) Venn analysis of the OTUs that significantly differed in relative abundance between comparisons of Na-HHZ and Na-HHZcas, Na-ZH11 and Na-ZH11cas, and Na-WT and Na-sst plants. (B to D) The relative abundances of the OTUs that were coenriched in the roots of plants with loss of function of SST under salt stress and coexisted in soils of three pairs of plant materials (B), in soils of Na-ZH11 and Na-ZH11cas and Na-WT and Na-sst plant materials (C), and in soils of Na-HHZ and Na-HHZcas and Na-WT and Na-sst plant materials (D) (DESeq2, n = 6, P < 0.05). In panels B to D, different background colors correspond to different components in the Venn diagram (Adopted from Lian et al., 2020)

Figure 1 from Lian et al. (2020) provides a detailed analysis of the genetic and molecular basis of root stress responses, focusing on the rhizosphere microbial community under different SST gene variations and stress conditions. The Principal Component Analysis (PCA) plots (a) and (b) show distinct separations in microbial community structures under various treatments, indicating the significant impact of SST gene modifications. The network diagrams (c) and (d) reveal complex interactions among microbial communities, highlighting the key role of specific operational taxonomic units (OTUs) in stress responses. This figure effectively demonstrates how SST gene variations regulate microbial communities, thereby enhancing plant stress tolerance.

In summary, rice roots exhibit a range of morphological, physiological, and genetic adaptations to cope with abiotic stresses. These adaptations are further enhanced by the presence of beneficial microbes in the rhizosphere, which play a synergistic role in improving the plant's stress tolerance. Understanding these complex interactions between roots and rhizosphere microbes is crucial for developing strategies to enhance rice productivity under adverse environmental conditions.

3 Rhizosphere Microbial Communities

3.1 Composition and diversity of rhizosphere microbes

The rhizosphere is the soil region immediately surrounding plant roots, which hosts a diverse array of microbial communities that play crucial roles in plant health and stress tolerance (Figure 2) (Ding et al., 2019). Rhizosphere microorganisms are mainly composed of bacteria, actinomycetes, fungi, algae, protozoa and viruses, and bacteria can account for 90% of the total number of microorganisms, which is the largest group in the composition of soil microorganisms.

Figure 2 Schematic of a rice root section presenting the structure of the rhizosphere, rhizoplane and endosphere in a flooded paddy soil. The rhizosphere is a small soil compartment that is around the rice roots and is affected by the rice roots. In flooded paddy soils, O2 is secreted through the aerenchyma of rice roots leading to oxic zones around the roots (e.g. the rhizosphere) which are surrounded by the anoxic bulk soil. The rhizoplane is the surface of the rice roots (including root hairs). The endosphere is a compartment inside the rice roots (Adopted from Ding et al., 2019)

Studies have shown that the composition and diversity of these microbial communities can vary significantly depending on several factors, including plant genotype, soil type, and environmental conditions (Hu et al., 2020; Lazcano et al., 2021). For instance, research has demonstrated that drought stress leads to a significant restructuring of the rice root-associated microbiomes, with notable changes in the bacterial and fungal compositions in the rhizosphere and endosphere compartments (Santos-Medellín et al., 2017). Previous studies have shown that the diversity index of rhizosphere soil bacterial community did not change significantly under drought stress, and the composition of rhizosphere soil bacterial community was different under drought stress and normal irrigation. Furthermore, through the analysis of bacterial community structure and species differences, it is found that drought stress significantly affected the structure and composition of bacterial community in rice rhizosphere soil. The change of bacterial community structure in rice rhizosphere soil may be a positive response of the rice-rhizosphere soil bacterial community to drought stress. Similarly, the microbial community structure in the rhizosphere of rice plants is influenced by the plant's growth stage and the specific soil environment, with certain bacterial phyla such as Gemmatimonadetes, Proteobacteria, and Verrucomicrobia being particularly affected (Breidenbach et al., 2016).

3.2 Functional roles of rhizosphere microbes in plant health

Rhizosphere microbes are essential for enhancing plant growth and stress tolerance through various mechanisms. The edge of the plant root system is enriched with many rhizosphere microorganisms, which act as decomposers to transform the organic matter in the soil into inorganic matter that can be absorbed by plants, and at the same time, soil rhizosphere microorganisms secrete some plant hormones in the process of metabolism to provide necessary energy and hormones for the growth of plants, and finally achieve the role of promoting plant growth. Plant rhizosphere growth promoters can also stimulate plants to synthesize a variety of osmotic regulators such as proline, etc., to maintain cell osmotic balance, prevent cell dehydration, enhance antioxidant enzyme activity, help plants remove excess reactive oxygen species and other harmful substances, reduce oxidative damage, and thus improve plant drought tolerance. These microbes can improve nutrient uptake, promote plant growth, and protect plants from pathogens. For example, specific bacterial and fungal taxa such as Bacillus, Pseudomonas, Aspergillus, and Rhizopus have been associated with phosphorus solubilization and plant growth promotion in aluminum-tolerant rice genotypes (Xiao et al., 2022). PGPR inoculants indirectly promote plant growth and health by altering the composition and function of the rhizosphere microbial community (Kong et al., 2020; Hakim et al., 2021). Additionally, the presence of AMF in the rhizosphere has been shown to enhance plant tolerance to heavy metal stress by altering the microbial community structure and promoting the enrichment of beneficial microbes (Hao et al., 2021). Furthermore, the interactions between roots, rhizosphere, and rhizobacteria are critical for improving plant growth and tolerance to abiotic stresses such as drought, salinity, and heavy metals (Khan et al., 2021).

3.3 Impact of environmental factors on rhizosphere microbial communities

Environmental factors such as soil type, salinity and drought significantly affected the composition and function of rhizosphere microbial communities. Soil pH, heavy metals, soil texture and nitrogen are the most important factors affecting rhizosphere microbial communities, and they play different roles in different fields (Deng et al., 2017; 2022). Under drought stress, plants affect the community structure and function of rhizosphere microorganisms by changing the type and quantity of their own root exudates. Drought stress induced changes in the main components of rhizosphere and endophytic microbial communities. Drought increases soil heterogeneity, restricts nutrient flow and access, and often leads to dramatic reductions in bacterial biomass. The changes in root exudates affected the diversity, richness and structure of microbial communities, and recruited and enriched plant rhizosphere growth-promoting bacteria. Rhizosphere microorganisms affect the growth and development of plants by interacting with them. The composition of endogenous bacterial communities in the roots of sensitive rice is significantly changed under drought stress, but the community composition of endophytic bacteria in the roots of early-tolerant rice is similar under normal irrigation and drought stress. The enrichment of drought-responsive microorganisms may be beneficial to plants by enhancing their drought resistance (Santos-Medellín et al., 2017). Similarly, saline-alkali stress affects rhizosphere microbial communities, and specialized microbial communities from specific environments enhance plant tolerance to salinity by promoting plant growth and shaping microbial community composition (Santos et al., 2021). In addition, soil salinization has also been shown to affect rhizosphere bacterial communities and soil metabolites, and certain plant-specific resistance genes play a role in regulating these changes (Lian et al., 2020). The application of silicate fertilizers in arsenic-rich soils also alters rhizosphere bacterial communities and increases the genetic potential of microorganisms to tolerate various environmental stresses (Das et al., 2021).

The composition and diversity of rhizosphere microbial communities are shaped by a complex interaction of plant genotypes, environmental factors, and soil conditions. These microbial communities play an important functional role in enhancing plant health and stress tolerance, making them a key focus for improving crop stress resistance and productivity.

4 Interactions Between Rice Roots and Rhizosphere Microbes

4.1 Mechanisms of root exudate-microbe interactions

Rice roots are able to release root exudates, which leads to the influence of the rhizosphere environment on microorganisms, and rhizosphere effects are expressed through this pathway. Root exudates play a crucial role in mediating interactions between rice roots and rhizosphere microbes. These exudates, which include a variety of organic compounds such as sugars, amino acids, and secondary metabolites, serve as chemical signals that attract beneficial microbes to the rhizosphere. The composition of root exudates is influenced by the plant genotype, environmental conditions, and interactions with biotic factors (Gupta et al., 2023; Sharma et al., 2023). For instance, stress-induced changes in root exudate composition can modulate the rhizospheric microbial community, enhancing the plant's ability to cope with stress (Sharma et al., 2023). Additionally, specific root exudates have been shown to recruit beneficial microbes that can alleviate plant stress by altering soil properties and microbial community structure (Vives-Peris et al., 2019).

4.2 Microbial modulation of root architecture and function

Rhizosphere microbes, including PGPR and mycorrhizal fungi, have a significant impact on root structure and function. Soil bacteria can change the growth morphology of rice roots, and the more the number of soil bacteria can promote the root morphology, the more obvious the promotion effect on root morphology. Rhizosphere growth-promoting bacteria could promote the increase of root surface area, root volume and root diameter of rice to varying degrees (Figure 2) (Ding et al., 2019). The fungus absorbs the organic matter secreted by the root system and decomposes the organic matter in the soil around the rice root system in a parasitic or saprophytic way to maintain its normal life activities and affect the morphology of the rice root system. Actinomycetes, as one of the main driving forces involved in the transformation of soil nitrogen, phosphorus, potassium and other elements, directly affect the pH value, redox potential and fertility of soil, and their abundance, activity and species also indirectly affect the morphological indexes such as dry weight, root length and root volume of rice roots. Backer's study illustrates the gradient of microbial diversity and interactions from the soil to the root surface and within root tissues, highlighting how microbes in the rhizosphere, on the root surface, and inside the roots differently contribute to plant health and stress tolerance. These microbes can enhance nutrient uptake, improve root growth, and increase root surface area, which are critical for plant stress tolerance (Backer et al., 2018; Hao et al., 2021; Hussain et al, 2022). For example, AMF have been shown to alter the rhizosphere microbiome, interacting with plant rhizosphere growth-promoting bacteria and plants, promoting the enrichment of beneficial bacteria and fungi that enhance plant growth and stress tolerance (Hao et al., 2021). Similarly, PGPR can modulate root architecture by producing plant growth regulators and solubilizing nutrients, thereby improving the plant's ability to withstand abiotic stresses such as salinity and drought (Backer et al., 2018).

Backer's study illustrates the different levels of intimacy and impact of plant-microbe interactions, highlighting the complexity of the rhizosphere environment. The figure shows that the diversity and abundance of microbes depend on their proximity to the plant roots, soil type, crop species, and plant tissue. It emphasizes the close interactions of microbes with the plant root surface (rhizosphere) and within the roots (endophytes), playing critical roles in nutrient acquisition, soil health, and promoting plant growth (Backer et al., 2018).

4.3 Synergistic effects of root-microbial interactions against adversity

The synergy between rice roots and rhizosphere microorganisms plays a key role in enhancing plant stress resistance. These interactions can improve nutrient access, promote root growth, and enhance resistance to environmental stresses. For example, the presence of specific microbial communities in the rhizosphere can mitigate the negative effects of salinity on rice by regulating soil metabolites and microbial community structure (Lian et al., 2020; Santos et al., 2021). In addition, combined inoculation of PGPR and mycorrhizal fungi has been shown to have a cumulative effect on plant growth and stress resistance, highlighting the importance of microbial synergies in sustainable agriculture (Nadeem et al., 2014). In addition, the root system can secrete malic acid, which is an effective chemotant of Bacillus subtilis, which is a rhizosphere growth-promoting bacterium that activates the secretion of osmotic substances to enhance drought resistance, while interacting with other rhizosphere bacteria to enhance the plant's ability to resist drought. These microorganisms are able to produce antioxidants and other stress-related compounds that further enhance the resilience of plants under adverse conditions (Gupta et al., 2023).

5 Case Studies and Experimental Evidence

5.1 Drought stress tolerance through root-microbe synergy

Several studies have demonstrated the root-related microorganisms play an important role in improving drought stress tolerance in rice. For instance, a consortium of rhizobacteria, Bacillus amyloliquefaciens Bk7 and Brevibacillus laterosporus B4, along with biochemical elicitors such as salicylic acid and β-aminobutyric acid, was shown to improve drought tolerance in rice plants. The treated plants exhibited 100% survival after 16 days without water, with notable improvements in seedling height, shoot number, and reduced symptoms of chlorosis, wilting, and necrosis. The mechanisms underlying this enhanced tolerance included increased activities of antioxidant enzymes and up-regulation of stress-responsive genes (Kakar et al., 2016).

Another study highlights the role of drought-tolerant PGPR isolated from drought-tolerant rice genotypes. These PGPRs are associated with increased soil enzyme activities and improved growth status under drought conditions. The inoculation of drought-sensitive rice genotypes with these PGPRs leds to the up-regulation of several growth and stress-responsive genes, thereby enhancing drought tolerance (Omar et al., 2021). Additionally, research on the restructuring of rice root-associated microbiomes under drought stress revealed significant changes in microbial composition, with an enrichment of drought-responsive taxa that potentially contribute to plant survival under extreme conditions (Santos-Medellín et al., 2021).

5.2 Alleviate salt stress through rhizosphere microbial support

The alleviation of salt stress in rice through rhizosphere microbial support is also widely studied. An experiment tested the effects of endophytic and rhizosphere microorganisms on two rice varieties under high salt conditions. The results showed that these microorganisms improved the photosynthesis apparatus and induced antioxidant enzyme activity, leading to better salt stress tolerance (Figure 3). The regulation of the expression of salt stress-responsive genes and the improvement of root structure parameters were also observed (Gupta et al., 2023).

Figure 3 Effect of inoculation of Halotolerant endophytes and rhizobacteria on two rice varieties (A) CO51, and (B) Pusa Basmati 1. Sequence of pots from left to right (in both of the figures): T1 = Negative control, T2 = Positive control (200 mM NaCl), T3 = 200 mM NaCl + Trichoderma viride, T4 = 200 mM NaCl + Bacillus haynesii 2P2, T5 = 200 mM NaCl + Bacillus safensis BTL5, T6 = 200 mM NaCl + Brevibacterium frigoritolerans W19, and T7 = 200 mM NaCl + Pseudomonas fluorescens (Adopted from Gupta et al., 2023)

Bacillus subtilis GB03 strain stimulated the expression of HKTI gene in Arabidopsis thaliana buds, and under salt stress (100 mmol/L NaCl), the GB03 strain down-regulated the expression of HKT1 gene in roots and up-regulated buds, respectively, resulting in lower Na* accumulation in the whole plant than in the control. Piriformospora indica, on the other hand, colonized Arabidopsis roots under salt stress and showed enhanced expression of HKT1 gene in rice. In addition, AMF is also involved in the regulation of specific metabolic pathways in the root system of host plants, promoting the synthesis and secretion of terpenes and phenolic compounds, as well as the deposition of resistant substances such as phytoalexin and lignin, thereby inhibiting the growth and reproduction of pathogenic bacteria (Chen et al., 2021a).

Further studies of microbiota from specific environments have demonstrated that these microbiotas can enhance rice tolerance to salinity. Inoculation of paddy fields and salt-tolerant microbiotas led to an increase in stem and root biomass at moderate salinity levels. The study concluded that the interaction of rice with these specialized microbiota forms the composition of the rhizosphere microbiota, which supports the growth of plants under salt stress (Santos et al., 2021). In addition, the role of SST gene in rice is also related to rhizosphere bacterial community and soil metabolites. The study found that the presence of SST genes significantly affected rhizosphere bacterial communities and soil metabolites, thereby enhancing rice tolerance to high salt levels (Lian et al., 2020).

5.3 Role of microbes in enhancing rice resistance to pathogens

Microbes also play a crucial role in enhancing rice resistance to pathogens. The inoculation of rice plants with beneficial rhizobacteria has been shown to induce systemic resistance against various pathogens. For example, the application of a consortium of rhizobacteria not only improved drought tolerance but also enhanced the overall health of rice plants, potentially providing resistance against opportunistic infections (Kakar et al., 2016).

Additionally, the restructuring of root-associated microbiomes under drought stress is found to include shifts in microbial communities that can provide protection from pathogenic microbes. The enrichment of specific bacterial taxa under drought conditions suggests that these microbes might contribute to both abiotic and biotic stress tolerance (Santos-Medellín et al., 2021).

The synergistic roles of roots and rhizosphere microbes are pivotal in enhancing rice stress tolerance. The integration of beneficial microbes into rice cultivation practices offers a promising strategy to mitigate the adverse effects of drought, salinity, and pathogen attacks, thereby contributing to sustainable agriculture.

6 Biotechnological and Agronomic Approaches

6.1 Genetic engineering of rice for enhanced root-microbe interactions

Genetic engineering offers a promising avenue to enhance root-microbe interactions in rice, thereby improving stress tolerance. One approach involves manipulating specific genes that influence the rhizosphere microbiome. For instance, the squamosa promoter binding protein box (SBP box) family gene (SST/OsSPL10) in rice has been shown to affect the rhizosphere bacterial community and soil metabolites, which are crucial for salt stress tolerance. CRISPR-edited lines with altered SST function demonstrated significant changes in rhizobacterial assembly and soil metabolite profiles, leading to improved salt stress adaptation (Lian et al., 2020). Additionally, breeding strategies that promote beneficial plant-microbiome interactions, such as selecting for traits that enhance root exudate profiles, can further optimize these interactions (Yang et al., 2023).

6.2 Application of beneficial microbial inoculants

The application of beneficial microbial inoculants, such as PGPR and mycorrhizal fungi, has been extensively studied for their role in enhancing rice stress tolerance. PGPR, including Bacillus amyloliquefaciens and Aspergillus spinulosporus, have been shown to prime rice plants for improved defense against pathogens like Xanthomonas oryzae pv. oryzae by reprogramming host defense responses and enhancing the expression of defense-related enzymes and proteins (Jain et al., 2020). Similarly, AMF can improve plant growth under stress conditions by enhancing nutrient uptake and altering the rhizosphere microbial community structure (Hao et al., 2021). These microbial inoculants not only promote plant growth but also enhance tolerance to various abiotic stresses, such as salinity and heavy metal contamination (Nadeem et al., 2014; Santos et al., 2021).

6.3 Agronomic practices to promote root and microbial health

Agronomic practices play a crucial role in promoting root and microbial health, thereby enhancing rice stress tolerance. Practices such as silicate fertilization have been shown to improve microbial functional potentials for stress tolerance in arsenic-enriched rice cropping systems. Silicate fertilization alters rhizosphere bacterial communities, increasing the abundance of stress-resistant microbial communities and enhancing their genetic potential to tolerate various environmental stresses (Das et al., 2021). Additionally, the use of organic and inorganic amendments can support the growth of beneficial microbes in the rhizosphere, further promoting plant health and stress resilience (Yang et al., 2023). Implementing these agronomic practices can create a more favorable environment for root and microbial interactions, ultimately leading to improved crop productivity and stress tolerance.

By integrating genetic engineering, microbial inoculants, and agronomic practices, we can develop comprehensive strategies to enhance rice stress tolerance through synergistic root-microbe interactions. These approaches not only improve plant health and productivity but also contribute to sustainable agricultural practices in the face of global climate change.

7 Challenges and Future Directions

7.1 Understanding the complexity of root-microbe interactions

The intricate interactions between roots and rhizosphere microbes are pivotal for enhancing rice stress tolerance. However, the complexity of these interactions under various abiotic stresses remains a significant challenge. The rhizosphere is a dynamic environment where plants interact with a multitude of microorganisms, yet the precise mechanisms and timing of these interactions are not fully understood (Khan et al., 2021). For instance, the role of AMF in modulating rhizosphere microbial communities to improve plant growth under heavy metal stress highlights the need for a deeper understanding of these complex relationships (Hao et al., 2021). Additionally, the differential effects of endophytic and rhizospheric microbes on salinity stress alleviation in rice cultivars further underscore the complexity of these interactions (Gupta et al., 2023). Future research should focus on elucidating the specific pathways and molecular mechanisms through which these microbes confer stress tolerance to rice plants.

7.2 Integrating multi-omics approaches for comprehensive insights

To gain a holistic understanding of root-microbe interactions, integrating multi-omics approaches such as genomics, transcriptomics, proteomics, and metabolomics is essential. These approaches can provide comprehensive insights into the functional roles of microbial communities and their interactions with plant roots under stress conditions. For example, the use of high-throughput sequencing to study the effects of the SST gene on rhizosphere microbial communities and soil metabolites under salt stress has revealed significant differences in microbial assembly and soil metabolite profiles between plants with and without the SST gene (Lian et al., 2020). Similarly, proteomic analyses have identified differentially expressed proteins involved in stress alleviation and disease resistance in rice plants primed with beneficial microbes (Jain et al., 2020). By integrating these multi-omics data, researchers can uncover the complex networks and regulatory mechanisms that underpin root-microbe interactions, ultimately leading to the development of more resilient rice varieties.

7.3 Translating research results into practical applications

Translating the results of rhizosphere microbial interaction research into practical applications in rice cultivation presents another challenge. Although laboratory and controlled environment studies have shown the potential of microbial inoculants to enhance stress resistance, their effectiveness under field conditions may vary. For example, the application of PGPR and mycorrhizal fungi has shown promising promise in improving crop productivity in stress settings (Nadeem et al., 2014). However, factors for the success of these microbial inoculants in the field include soil type, environmental conditions, and compatibility of microbial strains with specific rice genotypes. In addition, it is important to develop microbial associations that can provide consistent benefits across different stress conditions and rice varieties. Future research should focus on optimizing the formulation and application methods of microbial inoculants, and conducting large-scale field trials to verify their effectiveness in diverse agricultural environments.

8 Concluding Remarks

By analyzing the synergistic role of root and rhizosphere microbes in improving rice stress resistance, we have gained some important insights. Specific microbial communities enhanced the growth of rice under salt stress by promoting denser and more complex root microbial communities. Aluminum-tolerant rice genotypes recruit specific microbial groups that contribute to phosphorus dissolution and plant growth. The use of rhizosphere bacterial complexes and biochemical inducers has shown effectiveness in improving rice cold tolerance and drought resistance. SST genes in rice were found to affect rhizosphere bacterial communities and soil metabolites, providing a genetic basis for improving salt stress tolerance. The role of endophytic and rhizosphere microorganisms in alleviating salt stress through antioxidant enzyme activity and root structure regulation has also been demonstrated.

This review analyses the potential of using root and rhizosphere microbial interactions to improve rice stress resistance. Understanding specific microbial groups and their functions can lead to the development of targeted microbial inoculants to enhance rice resistance to abiotic stresses. Strategies that harness microbial associations and manipulate key plant genes offer promise for improving rice stress resistance through microbial and genetic approaches. The genotype of aluminum-tolerant rice recruits beneficial microorganisms and regulates root microbial communities through phosphorus input, emphasizing the importance of integrating microbial management with traditional agricultural practices to achieve sustainable rice production under stress conditions.

The future of rice root-microbe research lies in the development of innovative solutions to enhance crop stress resistance and productivity. Continuing to explore the complex interactions of rice roots and their associated microbial communities will be critical to identifying key microbial roles and their mechanisms of action in stress resistance. Advances in high-throughput sequencing and metagenomics will enable detailed characterization of microbial communities and their functional potential. Collaboration between microbiologists, plant geneticists, and agronomists will translate these findings into practical applications that benefit rice farmers and contribute to global food security.

Acknowledgments

The authors would like to thank the two anonymous peer reviewers for their thorough review and suggestions, which have played a significant role in improving the quality of this manuscript.

Funding

This work was supported by the grants from the Central Leading Local Science and Technology Development Project (grant no. 202207AA110010) and the Key and Major Science and Technology Projects of Yunnan (grant nos. 202202AE09002102, 202402AE090026-04).

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

References

Backer R., Rokem J.S., Ilangumaran G., Lamont J., Praslickova D.L., Ricci E., Subramanian S., and Smith D., 2018, Plant growth-promoting rhizobacteria: context mechanisms of action and roadmap to commercialization of biostimulants for sustainable agriculture, Frontiers in Plant Science, 9: 1473.

https://doi.org/10.3389/fpls.2018.01473

Breidenbach B., Pump J., and Dumont M.G., 2016, Microbial community structure in the rhizosphere of rice plants, Frontiers in Microbiology, 6: 1537.

https://doi.org/10.3389/fmicb.2015.01537

Das S., Kim G., Lee J., Bhuiyan M., and Kim P., 2021, Silicate fertilization improves microbial functional potentials for stress tolerance in arsenic-enriched rice cropping systems, Journal of Hazardous Materials, 417: 125953.

https://doi.org/ 10.21203/RS.3.RS-147549/V1

Deng S., Ke T., Li L., Cai S., Zhou Y., Liu Y., Guo L., Chen L., and Zhang D., 2017, Impacts of environmental factors on the whole microbial communities in the rhizosphere of a metal-tolerant plant: Elsholtzia haichowensis sun, Environmental Pollution, 237: 1088-1097.

https://doi.org/10.1016/j.envpol.2017.11.037

Deng Z.Y., Wang Y.C., Xiao C.C., Zhang D.X., Feng G., and Long W.X., 2022, Effects of plant fine root functional traits and soil nutrients on the diversity of rhizosphere microbial communities in tropical cloud forests in a dry season, Forests, 13(3): 421.

https://doi.org/10.3390/f13030421

Ding L.J., Cui H.L., Nie S.A., Long X.E., Duan G., and Zhu Y., 2019, Microbiomes inhabiting rice roots and rhizosphere, FEMS Microbiology Ecol., 95(5): fiz040.

https://doi.org/10.1093/femsec/fiz040

Gupta A., Singh A.N., Tiwari R.K., Sahu P.K., Yadav J., Srivastava A.K., and Kumar S., 2023, Salinity alleviation and reduction in oxidative stress by endophytic and rhizospheric microbes in two tice cultivars, Plants, 12(5): 976.

https://doi.org/10.3390/plants12050976

Hao L., Zhang Z., Hao B., Diao F., Zhang J., Bao Z., and Guo W., 2021, Arbuscular mycorrhizal fungi alter microbiome structure of rhizosphere soil to enhance maize tolerance to La, Ecotoxicology and Environmental Safety, 212: 111996.

https://doi.org/10.1016/j.ecoenv.2021.111996

Hu J., Wei Z., Kowalchuk G., Xu Y., Shen Q., and Jousset A., 2020, Rhizosphere microbiome functional diversity and pathogen invasion resistance build up during plant development, Environmental Microbiology, 22(12): 5005-5018.

https://doi.org/ 10.1111/1462-2920.15097

Huang L., Wang X., Chi Y., Huang L., Li W., and Ye Z., 2021, Rhizosphere bacterial community composition affects cadmium and arsenic accumulation in rice (Oryza sativa L.), Ecotoxicology and Environmental Safety, 222: 112474.

https://doi.org/10.1016/j.ecoenv.2021.112474

Hussain M.B., Shah S.H., Matloob A., Mubaraka R., Ahmed N., Ahmad I., and Jamshaid M.U., 2022. Rice interactions with plant growth promoting rhizobacteria, Modern Techniques of Rice Crop Production, 2022: 231-255.

https://doi.org/10.1007/978-981-16-4955-4_14

Jain A., Chatterjee A., and Das S., 2020, Synergistic consortium of beneficial microorganisms in rice rhizosphere promotes host defense to blight-causing Xanthomonas oryzae pv. Oryzae, Planta, 252(6): 106.

https://doi.org/10.1007/s00425-020-03515-x

Kakar K., Ren X., Nawaz Z., Cui Z., Li B., Xie G., Hassan M., Ali E., and Sun G., 2016, A consortium of rhizobacterial strains and biochemical growth elicitors improve cold and drought stress tolerance in rice (Oryza sativa L.), Plant Biology, 18(3): 471-83.

https://doi.org/10.1111/plb.12427

Khan N., Ali S., Shahid M.A., Mustafa A., Sayyed R.Z., and Curá J.A., 2021, Insights into the interactions among roots rhizosphere and rhizobacteria for improving plant growth and tolerance to abiotic stresses: a review, Cells, 10(6): 1551.

https://doi.org/ 10.3390/cells10061551

Kong Z.Y., and Liu H.G., 2022, Modification of rhizosphere microbial communities: a possible mechanism of plant growth promoting rhizobacteria enhancing plant growth and fitness, Frontiers in Plant Science, 13: 920813.

https://doi.org/10.3389/fpls.2022.920813

Lazcano C., Boyd E., Holmes G., Hewavitharana S., Pasulka A., and Ivors K., 2021, The rhizosphere microbiome plays a role in the resistance to soil-borne pathogens and nutrient uptake of strawberry cultivars under field conditions, Scientific Reports, 11(1): 3188.

https://doi.org/10.1038/s41598-021-82768-2

Lian T.X., Huang Y.Y., Xie X.N., Huo X., Shahid M.Q., Tian L., Lan T., and Jin J., 2020, Rice SST variation shapes the rhizosphere bacterial community conferring tolerance to salt stress through regulating soil metabolites, mSystems, 5: 10

https://doi.org/10.1128/ mSystems.00721-20

Nadeem S., Ahmad M., Zahir Z., Javaid A., and Ashraf M., 2014, The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments, Biotechnology Advances, 32(2): 429-448.

https://doi.org/ 10.1016/j.biotechadv.2013.12.005

Omar S., Fetyan N., Eldenary M., Abdelfattah M., Abd-Elhalim H., Wróbel J., and Kalaji H., 2021, Alteration in expression level of some growth and stress-related genes after rhizobacteria inoculation to alleviate drought tolerance in sensitive rice genotype, Chemical and Biological Technologies in Agriculture, 8: 1-19.

https://doi.org/10.1186/s40538-021-00237-4

Santos S., Rask K., Vestergård M., Johansen J., Priemé A., Frøslev T., González A., He H., and Ekelund F., 2021, Specialized microbiomes facilitate natural rhizosphere microbiome interactions counteracting high salinity stress in plants, Environmental and Experimental Botany, 186: 104430.

https://doi.org/10.1016/J.ENVEXPBOT.2021.104430

Santos-Medellín C., Edwards J., Liechty Z., Nguyen B., and Sundaresan V., 2017, Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes, mBio, 8(4): 10.1128.

https://doi.org/10.1128/mBio.00764-17

Sharma I., Kashyap S., and Agarwala N., 2023, Biotic stress-induced changes in root exudation confer plant stress tolerance by altering rhizospheric microbial community, Frontiers in Plant Science, 14: 1132824.

https://doi.org/10.3389/fpls.2023.1132824

Vives-Peris V., Ollas C., Gómez-Cádenas A., and Pérez-Clemente R., 2019, Root exudates: from plant to rhizosphere and beyond, Plant Cell Reports, 39(3): 17.

https://doi.org/10.1007/s00299-019-02447-5

Xiao X., Wang J.L., Li J.J., Li X.L., Dai X.J., Shen R.F., and Zhao X.Q., 2022, Distinct patterns of rhizosphere microbiota associated with rice genotypes differing in aluminum tolerance in an acid sulfate soil, Frontiers in Microbiology, 13: 933722.

https://doi.org/ 10.3389/fmicb.2022.933722

Yang S.D., Liu H.W., Xie P.H., Wen T., Shen Q.R., and Yuan J., 2023, Emerging pathways for engineering the rhizosphere microbiome for optimal plant health, Journal of Agricultural and Food Chemistry, 71(11): 4441-4449.

https://doi.org/10.1021/acs.jafc.2c08758