BENEFICIAL PLANT-MICROBE INTERACTIONS: AN ECOLOGICAL PERSPECTIVE
The soil microbial community is intricately interwoven with plant health. Beneficial plant-microbe interactions are an indispensable component for restoring ecosystem loss due to excessive use of chemical fertilizers and pesticides. For example, nitrogen (N) fertilizers are responsible for nearly 5% emissions of global greenhouse gas (GHG) mainly nitrous oxide, which is 300 times more potent than CO2, in terms of heat-trapping (Y. Gao & Cabrera Serrenho, 2023; Wen et al., 2021). Similarly, phosphorus (P) is another rate-limiting nutrient and almost 80% of applied P-fertilizer is lost due to the inefficient acquisition by the plants, imposing an economic burden on the farmers. The long-term excessive application of N- and P-fertilizers causes soil acidification and eutrophication of fresh-water bodies and is therefore not sustainable. Many beneficial bacteria/fungi in the rhizosphere, collectively termed plant-growth promoting microbes (PGPMs), support plant growth by increasing nutrient-use efficiency, biotic/abiotic stress tolerance, and disease resistance. Rhizobacteria and free-living diazotrophs mediate biological N-fixation in nodulating and non-nodulating crops, respectively (Wen et al., 2021). PGPMs also secrete different organic acids to solubilize insoluble-P and hence, significantly reduce the usage of P-fertilizer, without jeopardizing crop yield. Apart from fertilizers, the over-application of chemical pesticides is another serious concern that can increase resistance among pathogenic microbes. Besides, entering of hazardous pesticides into the food chain can create a toxic ecosystem. PGPMs serve as biological alternatives to these pesticides and hence, maintain a disease-suppressive environment in soil, through multifaceted ways including antibiosis, parasitism, competition for resources, and predation in addition to providing induced systemic resistance in plants (Fig. 4A). Along with mitigating biotic-stress, PGPMs also provide the dual benefit of providing tolerance towards abiotic stresses, whose occurrence increased as a repercussion of global climate change (Mitter, Tosi, Obregón, Dunfield, & Germida, 2021). Intensive agricultural practices also decrease the soil’s organic carbon, deteriorating soil fertility along with accelerating global warming as more carbon reaches the environment. PGPMs use the photosynthesized CO2for maintaining their growth and hence increase soil organic carbon, contributing to climate restoration (Fig. 4A). Recently, a global scale study has also established a positive correlation between plant-mycorrhiza association and soil carbon content (Soudzilovskaia et al., 2019). Climate change is also reshaping forest ecosystems by driving species beyond their evolved resilience, with some of them even facing the fate of extinction. Nurturing trees by microbial symbionts acclimatized to specific climatic conditions safeguard their existence by providing climate tolerance (Allsup, George, & Lankau, 2023; Baldrian, López-Mondéjar, & Kohout, 2023). Taken together, supporting the beneficial microbe-plant interactions will not only reduce the negative impacts of climate change on plant fitness but, will also reduce the use of chemical-based fertilizers/pesticides.
BROADENING HOST-RANGE SPECIFICITY FOR PRODUCING “GREENER” CLIMATE
The increasing levels of CO2 in the atmosphere drive photosynthesis and biomass accumulation in C3 crops (Ainsworth & Long, 2021). This CO2 fertilization effect increases plant growth but negatively impacts crop nutritional quality (Myers et al., 2014) with marked reductions in N, P, and other essential mineral nutrients (McGrath & Lobell, 2013). The increasing requirement for essential soil nutrients is an important driver for improving symbiotic associations between plants and beneficial microorganisms (Chan, 2022; Dey & Ghosh, 2022). Multiple approaches are underway to broaden host-range specificity (Fig. 3) and to minimize high CO2-induced decreases in crop quality. Of these, altering and/or suppressing host-induced immunity is perhaps the most important. For example, the downstream target of MtRAM1, MtKIN3,suppresses host defenses and supports AMF symbiosis (Irving et al., 2022), while also regulating plant N responses. Rhizobia produces several effectors that manipulate host defense signaling pathways. For example, the soybean Nodulation outer protein T (NopT, an effector protease from Sinorhizobium sp.) activates the GmPBS1-mediated resistance pathway and impairs nodule formation (Khan et al., 2022). Similarly, the GmNNL1 (Nodule Number Locus 1; an R protein) protein directly interacts with the NopP effector from BradyrhizobiumUSDA110 to trigger immunity and inhibit nodulation (B. Zhang et al., 2021). Thus, genetic engineering of effector proteins to block defense but support symbiosis could broaden the range of beneficial plant-microbe interaction (Fig. 3A). Dual-sensing receptors can widen the host-range of beneficial microbes (Fig. 3B). For example, the expression of chimeric “Nod-Myc” receptor in which the ectodomains of OsMYR1 and OsCERK1 were replaced by homologous M. truncatula sequences in rice led to increased Nod factor-induced calcium oscillations (J. He et al., 2019). Similarly, the binding affinity of the L. Japonicas receptor kinaseEPR3a (Exopolysaccharide receptor 3a) that binds AMF-specific glucans, as well as with rhizobia-specific exopolysaccharide (EPS)could function as a dual receptor. In addition, trans-kingdom signaling can also be exploited to enhance interactions with beneficial microbes [85,86]. For example, barley lines expressing the plant-derived signal rhizopine, which controls the N2-fixation related gene expression in bacteria (Fig. 3C), can associate withAzorhizobium caulinodans , which has a rhizopine uptake system and usually forms a nitrogen-fixing symbiosis with Sesbania .
For any PGPM, it is crucial to colonize as well as sustain in the dynamic environment also called rhizo-competence which in part depends on host genetics. Identification of intraspecific variation controlling microbial selection and shaping root-associated microbiomes remains challenging (Zboralski, Saadia, Novinscak, & Filion, 2022). Nevertheless, genome-wide association studies (GWAS) appear to be a potentially powerful tool in identifying host genetic loci which are microbes responsive (Fig. 3D). To explore this, previous efforts have demonstrated, the dependence of rhizosphere microbial communities on distinct genotypes of the same host species including maize and sorghum. Moreover, in A. thaliana host SNPs controlling defense and cell wall integrity affected microbial community variation (Deng et al., 2021). Such precision-based microbiome management in the future could assist in engineering high-yielding/climate-resilient crops.