MicroRNA regulation of plant innate immune receptors

Abstract

Plant genomes contain large numbers of cell surface leucine-rich repeat (LRR) and intracellular nucleotide binding (NB)-LRR immune receptors encoded by resistance (R) genes that recognize specific pathogen effectors and trigger resistance responses. The unregulated expression of NB-LRR genes can trigger autoimmunity in the absence of pathogen infection and inhibit plant growth. Despite the potential serious consequence on agricultural production, the mechanisms regulating R-gene expression are not well understood. We identified microRNA (miRNA) progenitor genes precursor transcripts, and two miRNAs [nta-miR6019 (22-nt) and ntamiR6020 (21-nt)] that guide cleavage of transcripts of the Toll and Interleukin-1 receptor-NB-LRR immune receptor N from tobacco that confers resistance to tobacco mosaic virus (TMV). We further showed that cleavage by nta-miR6019 triggers RNA-dependent RNA polymerase 6-and ribonuclease Dicer-like 4-dependent biogenesis of 21-nt secondary siRNAs "in phase" with the 22-nt miR6019 cleavage site. Furthermore, we found that processing of the 22-nt nta-miR6019 depended on an asymmetric bulge caused by mismatch in the nta-miR6019 precursor. Interestingly, coexpression of N with nta-miR6019 and nta-miR6020 resulted in attenuation of N-mediated resistance to TMV, indicating that these miRNAs have functional roles in NB-LRR regulation. Using a bioinformatics approach, we identified six additional 22-nt miRNA and two 21-nt miRNA families from three Solanaceae species-tobacco, tomato, and potato. We show that members of these miRNA families cleave transcripts of predicted functional R genes and trigger production of phased secondary 21-nt siRNAs. Our results demonstrate a conserved role for miRNAs and secondary siRNAs in NB-LRR/LRR immune receptor gene regulation and pathogen resistance in Solanaceae.

CRT1 is a nuclear-translocated MORC endonuclease that participates in multiple levels of plant immunity

“…Many viruses, including TCV, encode proteins that disrupt this defense 48 . In plants, the small RNAs involved in RNA silencing have critical roles in reprogramming host gene expression following infection with various pathogens [49][50][51][52] . Thus, CRT1-mediated RNA silencing may be responsible for at least some of these host responses although most of the defence genes tested were not affected by CRT1/CRH1 (Supplementary Fig.…”

An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication

“…recognition whereas NLR activity levels above a certain threshold can trigger autoimmunity and spontaneous cell death (25)(26)(27)(28)(29). We found levels of RPP7-coding transcripts to be well-correlated with levels of immunity conferred by this disease resistance gene, indicating that proper control of these transcripts is critical for RPP7 function (30) (Fig.…”

Virus-Based MicroRNA Silencing in Plants

“…In Nicotiana sylvestris, the ortholog of the HD-ZIP III transcription factor PHAVOLUTA was shown to be regulated by miR165/166-directed cleavage of its mRNA (McHale and Koning, 2004). miR165/166 also have been predicted and detected in N. benthamiana (Li et al, 2012). However, their exact function has not been characterized.…”