Abstract
Plants evolved an array of disease resistance genes (R genes) to fight pathogens. In the absence of pathogen infection, NBS-LRR genes, which comprise a major subfamily of R genes, are suppressed by a small RNA cascade involving microRNAs (miRNAs) that trigger the biogenesis of phased siRNAs (phasiRNAs) from R gene transcripts. However, whether or how R genes influence small RNA biogenesis is unknown. In this study, we isolate a mutant with global defects in the biogenesis of miRNAs and phasiRNAs in Arabidopsis thaliana and trace the defects to the over accumulation and nuclear localization of an R protein SNC1. We show that nuclear SNC1 represses the transcription of miRNA and phasiRNA loci, probably through the transcriptional corepressor TPR1. Intriguingly, nuclear SNC1 reduces the accumulation of phasiRNAs from three source R genes and concomitantly, the expression of a majority of the ~170R genes is up-regulated. Taken together, this study suggests an R gene-miRNA-phasiRNA regulatory module that amplifies plant immune responses.
Highlights
resistance genes (R genes) are classified into at least five groups according to domain composition[5]
Given that R genes are globally repressed by a miRNA–phasiRNA cascade, how do plants overcome this repression to induce and maintain R gene expression during defense? Do R genes influence small RNA biogenesis? In a genetic screen designed to uncover players of miRNA biogenesis, we isolated a mutant with global defects in miRNA biogenesis
We showed that nuclear SNC1 likely inhibited miRNA biogenesis by repressing the transcription of MIR genes together with its interacting protein TPR1, a transcriptional corepressor
Summary
R genes are classified into at least five groups according to domain composition[5]. Among them, the NBS-LRR family containing a nucleotide binding site (NBS) and a C-terminal leucine rich repeat domain (LRR) is the largest. Repression of R gene expression by small RNAs is not limited to individual miRNA–R gene interactions and entails global effects mediated by phased siRNAs (phasiRNAs). PhasiRNA biogenesis is triggered by miRNA-guided cleavage of noncoding transcripts or certain protein coding transcripts. Emerging evidence indicates that plants utilize specific miRNAs to target some NBS-LRR genes and trigger the production of phasiRNAs from these transcripts. In Arabidopsis, miR472 and miR825* target two NBS-LRR genes and trigger the production of phasiRNAs from these transcripts[18,19,20]. We showed that nuclear SNC1 likely inhibited miRNA biogenesis by repressing the transcription of MIR genes together with its interacting protein TPR1, a transcriptional corepressor. This work revealed a mechanism whereby an activated R protein may relieve the global repression of R genes by small RNAs to enable defense. While the previously known miRNA–phasiRNA– R genes module represses R gene expression in the absence of pathogens, the R gene–miRNA–phasiRNA module discovered in this study likely enables R gene expression during defense
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