Abstract
Bidirectional root–shoot signalling is probably key in orchestrating stress responses and ensuring plant survival. Here, we show that Arabidopsis thaliana responses to microbial root commensals and light are interconnected along a microbiota–root–shoot axis. Microbiota and light manipulation experiments in a gnotobiotic plant system reveal that low photosynthetically active radiation perceived by leaves induces long-distance modulation of root bacterial communities but not fungal or oomycete communities. Reciprocally, microbial commensals alleviate plant growth deficiency under low photosynthetically active radiation. This growth rescue was associated with reduced microbiota-induced aboveground defence responses and altered resistance to foliar pathogens compared with the control light condition. Inspection of a set of A. thaliana mutants reveals that this microbiota- and light-dependent growth–defence trade-off is directly explained by belowground bacterial community composition and requires the host transcriptional regulator MYC2. Our work indicates that aboveground stress responses in plants can be modulated by signals from microbial root commensals.
Highlights
Unlike animals, plants are sessile organisms that must simultaneously integrate various responses to biotic and abiotic stresses to prioritize either growth or defence depending on rapidly changing surrounding conditions[1]
Eight versions of this BFO synthetic microbial consortium (SynCom) containing B, F and O communities mixed at different relative abundances (RAs) in the starting inoculum were used to recolonize the roots of germ-free A. thaliana in the gnotobiotic FlowPot system[30]
Reminiscent of the bidirectional communication mechanisms described along the microbiota–gut–brain axis in animals[15,54,55], we report here that aboveground stress responses in plants can be orchestrated through long-distance communication with belowground commensals
Summary
Plants are sessile organisms that must simultaneously integrate various responses to biotic and abiotic stresses to prioritize either growth or defence depending on rapidly changing surrounding conditions[1]. We show that microbial root commensals can alleviate A. thaliana growth deficiency under suboptimal light, and we observe a direct link between bacterial community composition and the prioritization of microbiota-induced growth over defence responses in shoots. We report that this microbiota- and light-dependent growth–defence trade-off requires the host transcriptional regulator MYC2. Our results imply that belowground responses to microorganisms and aboveground responses to light are integrated along a microbiota–root–shoot circuit to boost plant growth when the light condition is suboptimal
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