Phyllosphere microbiome induces host metabolic defence against rice false-smut disease

Xiaoyu Liu, Haruna Matsumoto, Tianxing Lv, Chengfang Zhan, Hongda Fang, Qianqian Pan, Haorong Xu, Xiaoyan Fan, Tianyi Chu, Sunlu Chen, Kun Qiao, Youning Ma, Li Sun, Qiangwei Wang, Mengcen Wang

Research output: Contribution to journalArticlepeer-review

26 Citations (Scopus)

Abstract

Mutualistic interactions between host plants and their microbiota have the potential to provide disease resistance. Most research has focused on the rhizosphere, but it is unclear how the microbiome associated with the aerial surface of plants protects against infection. Here we identify a metabolic defence underlying the mutualistic interaction between the panicle and the resident microbiota in rice to defend against a globally prevalent phytopathogen, Ustilaginoidea virens, which causes false-smut disease. Analysis of the 16S ribosomal RNA gene and internal transcribed spacer sequencing data identified keystone microbial taxa enriched in the disease-suppressive panicle, in particular Lactobacillus spp. and Aspergillus spp. Integration of these data with primary metabolism profiling, host genome editing and microbial isolate transplantation experiments revealed that plants with these taxa could resist U. virens infection in a host branched-chain amino acid (BCAA)-dependent manner. Leucine, a predominant BCAA, suppressed U. virens pathogenicity by inducing apoptosis-like cell death through H2O2 overproduction. Additionally, preliminary field experiments showed that leucine could be used in combination with chemical fungicides with a 50% reduction in dose but similar efficacy to higher fungicide concentrations. These findings may facilitate protection of crops from panicle diseases prevalent at a global scale.

Original languageEnglish
Pages (from-to)1419-1433
Number of pages15
JournalNature Microbiology
Volume8
Issue number8
DOIs
Publication statusPublished - Aug 2023

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