Plants encode numerous intracellular receptors known as nucleotide-binding leucine-rich repeat receptors (NLRs) that recognize pathogen-derived effectors or their activity to activate defenses. MiRNA regulate NLR genes in many species, often triggering the production of phasiRNAs. Most such examples involve genes encoding NLR carrying coiled-coil domains, although a few include genes encoding NLRs carrying a Toll/interleukin-1 domain (TNL). Here, we characterize the role of miR825-5p in Arabidopsis, using a combination of bioinformatics, transgenic plants with altered miRNA levels and/or reporters, small RNA and virulence assays. We demonstrate that miR825-5p downregulates TNL MIST1 by targeting for endonucleolytic cleavage the sequence coding for TIR2, a highly conserved amino acid motif, linked to a catalytic residue essential for immune function. MiR825-5p acts as a negative regulator of basal resistance against Pseudomonas syringae. MiR825-5p triggers the production from MIST1 of a large number of phased siRNAs that can mediate cleavage of both MIST1 and additional TNL gene transcripts, potentially acting as a regulatory hub. MiR825-5p is expressed in unchallenged leaves and transcriptionally downregulated in response to PAMPs. Our results show that miR825-5p, which is required for full expression of PTI, establishes a link between PAMP perception and expression of uncharacterized TNL genes.
Plants encode large numbers of intracellular immune receptors known as resistance (R) proteins or nucleotide-binding (NB) leucine-rich repeat (LRR) receptors (NLRs), involved in perception of pathogen-derived effectors and activation of immunity.Here, we report a two-tiered regulatory network mediated by microRNA and secondary phased small RNAs (phasiRNA) that targets the silencing of dozens of NLR genes encoding yet uncharacterized members of the Toll/interleukin-1 (TIR)-NBS-LRR (TNLs) subfamily in Arabidopsis. We show that miR825-5p downregulates expression of Arabidopsis AT5G38850 gene (renamed as microRNA-silenced TNL 1 or MIST1) by targeting the sequence coding for a highly conserved functional amino acid motif (TIR2) within the TIR domain of the receptor. Further, we show that MIST1 functions as a regulatory hub, since miRNA825-5p triggers RDR6-mediated processing of MIST1 transcripts, to generate trans-acting phasiRNAs that in turn target, a wide network of TNL genes for gene silencing. Regulation through MIST1 affects disease resistance against the model bacterial pathogen Pseudomonas syringae, since altered levels of miRNA825-5p lead to changes in Arabidopsis ability to establish basal defenses against this pathogen. MiR825-5p is expressed in unchallenged adult leaves and its production is down regulated in response to PAMPs such as bacterial flagellin but also fungal chitin.
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