The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling

PLoS Genet. 2014 Dec 11;10(12):e1004755. doi: 10.1371/journal.pgen.1004755. eCollection 2014 Dec.

Abstract

Barley (Hordeum vulgare L.) Mla alleles encode coiled-coil (CC), nucleotide binding, leucine-rich repeat (NB-LRR) receptors that trigger isolate-specific immune responses against the powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). How Mla or NB-LRR genes in grass species are regulated at post-transcriptional level is not clear. The microRNA family, miR9863, comprises four members that differentially regulate distinct Mla alleles in barley. We show that miR9863 members guide the cleavage of Mla1 transcripts in barley, and block or reduce the accumulation of MLA1 protein in the heterologous Nicotiana benthamiana expression system. Regulation specificity is determined by variation in a unique single-nucleotide-polymorphism (SNP) in mature miR9863 family members and two SNPs in the Mla miR9863-binding site that separates these alleles into three groups. Further, we demonstrate that 22-nt miR9863s trigger the biogenesis of 21-nt phased siRNAs (phasiRNAs) and together these sRNAs form a feed-forward regulation network for repressing the expression of group I Mla alleles. Overexpression of miR9863 members specifically attenuates MLA1, but not MLA10-triggered disease resistance and cell-death signaling. We propose a key role of the miR9863 family in dampening immune response signaling triggered by a group of MLA immune receptors in barley.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alleles
  • Ascomycota
  • Base Sequence
  • Cell Death
  • Disease Resistance*
  • Epigenetic Repression
  • Gene Expression Regulation, Plant
  • Gene Silencing
  • Hordeum / genetics*
  • Hordeum / microbiology
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Molecular Sequence Data
  • Nucleic Acid Conformation
  • Plant Diseases / microbiology
  • Plant Immunity / genetics*
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Polymorphism, Single Nucleotide
  • RNA, Plant / genetics*
  • RNA, Plant / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Signal Transduction
  • Transcription, Genetic
  • Translations
  • Triticum / genetics

Substances

  • MLA1 protein, Hordeum vulgare
  • MicroRNAs
  • Plant Proteins
  • RNA, Plant
  • RNA, Small Interfering

Grants and funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDB11020400), the National Basic Research Program of China (2011CB100700), the Ministry of Agriculture of China (2014ZX08009-003-001), the National Natural Science Foundation of China (31030007 and 31270300) to QHS, and in part by National Science Foundation (USA) Plant Genome Program grant 09-22746 to RW. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture and/or the National Science Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.