A microbiota–root–shoot circuit favours Arabidopsis growth over defence under suboptimal light

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.

Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

“…Consistent with previous reports ( 15 – 17 , 20 ), we observed that the composition of root-associated bacterial communities was significantly altered in several immunocompromised mutants, validating that diverse immune sectors differentially sculpt root bacterial assemblages in nature ( 13 , 14 ). However, we observed that these differences were subtle and that genotype-specific differences in bacterial community composition were not sufficient to explain variation in microbiota-induced differences in growth phenotypes.…”

“…A total of 183 bacterial strains isolated from healthy A. thaliana roots ( 20 , 74 ) were grown for 7 d in 600 μL 50% tryptic soy broth liquid media from a glycerol stock. A total of 100 μL of each strain was taken, combined together, centrifuged, and the pellet was resuspended in 10 mM MgCl 2 .…”

“…A total of 100 μL of each strain was taken, combined together, centrifuged, and the pellet was resuspended in 10 mM MgCl 2 . A total of 25 fungal and 6 oomycetes strains were grown individually on potato glucose agar media for 2 wk and harvested 1 d before the experiments ( 20 ). Harvested F and O mycelium (average of 50 mg/strain) was suspended in 1 mL 10 mM MgCl 2 inside a sterile 2-mL screwcap tube containing one stainless steel bead (3.2-mm diameter) and left at 4 °C overnight.…”

“…Although the plant innate immune system has been extensively studied under laboratory conditions, typically in leaves upon inoculation with particular host-adapted microbial pathogens, our understanding of this complex machinery in accommodating commensal microbes in roots and in maintaining host–microbe homeostasis remains fragmented ( 12 – 14 ). Earlier studies indicated that 1) specific sectors of the plant innate immune system, namely phytohormones, have a role in sculpting root microbiota assemblages ( 15 – 17 ); 2) host responses to the root microbiota and environmental stresses are connected through the innate immune system to promote plant health ( 18 – 20 ); and 3) innate immune outputs are needed for accommodation and beneficial activities of model rhizobacterial strains and fungal root symbionts ( 21 – 25 ). Particularly, tryptophan (Trp)-derived, specialized metabolites were previously shown to represent key molecules necessary for microbe-mediated plant growth promotion in monoassociation experiments with A. thaliana ( 23 – 25 ).…”

Rhizosphere microbiome: Functional compensatory assembly for plant fitness

“…Finally, the rhizosphere microbiome can regulate the growth-defense trade-off of the host plant [77] . For instance, the transcriptional regulator MYC2 in A. thaliana regulates a microbiome-root-shoot circuit favoring growth over defense under suboptimal light [78] . Defensive secondary metabolites of the benzoxazinoids that are released by cereal roots increase jasmonate signaling for plant defense, however, plant growth can be decreased and the rhizosphere microbial composition is modified to improve insect herbivore resistance, even in the next plant generation [79] .…”