ENGINEERING PLANT-MICROBE INTERACTION FOR NEXT GENERATION AGRICULTURE
The one health concept is based on a growing understanding that humans, animals, plants, microbiomes, and the environment are inseparably linked and impact each other constantly. The presence and stress levels experienced by different organisms within an ecosystem could therefore be transmitted from one to another through cell-to-cell ROS wave signaling. Stress experiences may be transmitted between plants and the soil microbiomes, by variations in the exchange of ROS signals. The application of genetic engineering approaches that serve to support symbiosis by blocking or minimizing the recognition-induced oxidative burst and activating host defenses must take such interactions into account, not only because they could increase the susceptibility of plants to pathogen attack but because they could also disrupt or interfere with a wide range of inter-organism communications within a given ecosystem.
Next-generation agriculture will be comprised of at least three components: enhanced crop production, minimal agri-inputs in the form of pesticides/fertilizers, and enhanced microbial carbon sequestration (Fig. 4A). Although, tailored plant-microbe interactions promise to meet all these three expectations, the AKP (Anna Karenina Principle) must be addressed. AKP considers that dysbiotic microbiomes are intrinsically different, while healthy microbiota are similar (Arnault, Mony, & Vandenkoornhuyse, 2023). Nevertheless, some strategies have already proved to be successful. For example, rhizosphere microbiome transplantation (RMT), in which microbial communities from either extreme environments or from a tolerant cultivar are inoculated to enhance growth or suppress stress responses (Fig. 4B) (Poppeliers, Sanchez-Gil, & de Jonge, 2023). RMT-mediated enhanced plant growth is poorly understood but could be stress-specific in nature. For example, changes in the drought and cold tolerance of tree species were associated with increased and decreased AMF diversity, respectively (Allsup et al., 2023).
Manipulation of the soil microbiome, associated crop management practices, and applied crop design are important components of solutions to address climate change. Much attention has also focussed on engineering nitrogen-fixing nodulation traits in non-leguminous crop plants (Huisman & Geurts, 2020). However, environmental perturbations exert effects on the diversity of plant microbial communities, with varying effects depending on the plant species and developmental stage. For example, drought increases the release of flavonoids in root exudates. These reshape the root microbiome by attractingAeromonas species that enhance dehydration resistance in plants (He et al., 2022). In addition, core bacterial commensals and host tryptophan-derived specialized metabolites participate in the control of fungal species (Wolinska et al., 2021). The changes in the relative abundance of Actinobacteria and Proteobacteria were reported in rice cultivated under drought conditions, an effect that persisted after stress alleviation (Santos-Medellin et al., 2021). In sorghum, drought increased the abundance of Actinobacteria and decreased pathogenic genera (Fusarium, Gibberella, and Sarocladium ) compared with well-watered controls (Gao et al., 2020; Xu et al., 2018). Drought-stressed sorghum plants in soils with Arthrobacterbacteria suffered more than those in which bacteria of the genusVariovorax were abundant (Qi et al., 2022). In contrast,Arthrobacter alleviated drought-stress effects in wheat (Hone et al., 2021). The presence of endospheric Streptomyces was correlated with drought tolerance in several plant species (Fitzpatrick et al., 2018).
Microbiome-inspired methods are promising innovations to enhance the stress resilience of crops. Roots grown in natural- and agro-ecosystems preferentially recruit PBB and AMF in drought situations (Song & Haney, 2021; Williams & de Vries, 2020; Zhao et al., 2023). Therefore, commercial AMF inoculants, added as a supplement to agricultural lands, have considerable potential in the alleviation of drought and nutrient deficiency in plants (Salomon et al., 2022). The application of microbial consortia may be more efficient than single-strain inocula in enhancing stress tolerance (Bradáčová et al., 2019). However, while AMF richness increases in barley roots under drought, AMF performance (colonization and the abundance of arbuscules and vesicles) decreases, indicating antagonistic interactions (Sendek et al., 2019). However, while drought increases the prevalence of beneficial microbes in rhizosheaths, it also increases the risk of penetration by harmful fungi (Lei et al., 2023). Moreover, a limitation factor in the application of such information concerns the diverse nature of AMF functionality depending on environmental effects.
Native synthetic microbial communities (SynComs) from plants grown under optimal conditions can be used to boost plant growth in poor soils (Fig. 4C) (M. Jiang et al., 2023). For example, SynComs application promotes the growth of A. thaliana , in an innate immunity-dependent manner (Wolinska et al., 2021). Cross-kingdom (fungi and bacteria) SynComs were more effective in suppressing fusarium-wilt disease in tomato than fungi or bacteria alone (X. Zhou et al., 2022). RMT and SynComs have yet to be tested for field applications, due to low efficiency in isolating functionally beneficial microbiomes. Multiple approaches based on screening natural variation, mathematical modeling, RAMAN-spectra, and successive passaging are being used to map the microbial community networks (Chen et al., 2021; X. He et al., 2021; Morella et al., 2020). The root-secreted chemicals or exudates comprised of photosynthetically fixed carbon as well as diverse signaling molecules including γ-aminobutyric acid, malate, and citrate, also contribute to shaping rhizosphere microbiome (Fig. 4D) (W. Zhang & Mason, 2022).In addition, microbe-derived secretory proteins YukE cause iron leakage in plant roots, which contributes to root colonization by beneficial rhizobacterium Bacillus velezensis (Y. Liu et al., 2023). Microbiome engineering to improve the composition of root exudates/secretomes will help determine the host-derived factors that synchronize interactions between beneficial and resident microbiomes (Escudero-Martinez & Bulgarelli, 2023). QTLs that determine the root-microbiota composition of crops contain genes such as the iron regulator FIT and water channel aquaporin SlTIP2.3 in tomato (Oyserman et al., 2022) and Nucleotide-Binding-Leucine-Rich-Repeat (NLR) in barley (Escudero-Martinez et al., 2022). Apart from the genotypes, the heritable component also needs to be accounted, especially in the context of microbiome-assisted molecular crop breeding.