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.