The RIPENING-INHIBITOR (RIN) transcriptional factor is a key regulator governing fruit ripening. While RIN also affects other physiological processes, its potential roles in triggering interactions with the rhizosphere microbiome and plant health are unknown. Here we show that RIN affects microbiome-mediated disease resistance via root exudation, leading to recruitment of microbiota that suppress the soil-borne, phytopathogenic Ralstonia solanacearum bacterium. Compared with the wild-type (WT) plant, RIN mutants had different root exudate profiles, which were associated with distinct changes in microbiome composition and diversity. Specifically, the relative abundances of antibiosis-associated genes and pathogen-suppressing Actinobacteria (Streptomyces) were clearly lower in the rhizosphere of rin mutants. The composition, diversity, and suppressiveness of rin plant microbiomes could be restored by the application of 3-hydroxyflavone and riboflavin, which were exuded in much lower concentrations by the rin mutant. Interestingly, RIN-mediated effects on root exudates, Actinobacteria, and disease suppression were evident from the seedling stage, indicating that RIN plays a dual role in the early assembly of disease-suppressive microbiota and late fruit development. Collectively, our work suggests that, while plant disease resistance is a complex trait driven by interactions between the plant, rhizosphere microbiome, and the pathogen, it can be indirectly manipulated using “prebiotic” compounds that promote the recruitment of disease-suppressive microbiota.
Bibliographical noteFunding Information:
This research was supported by the National Key Research and Development Program of China ( 2021YFD1900100 , 2022YFD1500202 , and 2022YFF1001804 ) the Fundamental Research Funds for the Central Universities ( KYT2023001 ), and the National Natural Science Foundation of China ( 42325704 , 41922053 , 31972504 , and 42377118 ). V.P.F. is funded by the Royal Society ( RSG∖R1∖180213 and CHL∖R1∖180031 ) and jointly by a grant from UKRI , Defra , and the Scottish Government , under the Strategic Priorities Fund Plant Bacterial Diseases program ( BB/T010606/1 ) at the University of York .
© 2023 The Author
- bacterial wilt
- disease-suppressive microbiota
- plant-microbe interactions
- rhizosphere immunity
- rhizosphere microbiome
- tomato root exudates