MicroRNA regulation of plant innate immune receptors

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 5; pp. 1790 - 1795
• Main Authors: Li, Feng, Pignatta, Daniela, Bendix, Claire, Brunkard, Jacob O, Cohn, Megan M, Tung, Jeffery, Sun, Haoyu, Kumar, Pavan, Baker, Barbara
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 31.01.2012; National Acad Sciences
• Subjects: Autoimmunity; Base Sequence; Bioinformatics; Biological Sciences; Cell surface; Disease resistance; DNA-directed RNA polymerase; Flowers & plants; Gene expression; Gene Expression Regulation, Plant; Gene regulation; Gene Silencing; Genes; Genomes; Immunity, Innate; Infection; Interleukin 1; Leaves; Lycopersicon esculentum; MicroRNA; MicroRNAs - genetics; MicroRNAs - physiology; miRNA; Molecular Sequence Data; Nicotiana - immunology; Nicotiana - physiology; Nucleotides; Pathogens; plant growth; potatoes; Receptors; Receptors, Immunologic - genetics; Receptors, Immunologic - physiology; Ribonuclease; RNA; RNA polymerase; RNA-directed RNA polymerase; Sensors; Sequence Homology, Nucleic Acid; siRNA; Small interfering RNA; Solanaceae; Solanum tuberosum; Stem cells; T cell receptors; Tobacco; Tobacco mosaic virus; tomatoes; Transcription; Typographic fonts
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1118282109

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 nta-miR6020 (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: