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Title: MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs

item ZHAI, JIXIAN - University Of Delaware
item JEONG, DONG-HOON - University Of Delaware
item DE PAOLI, EMANUELE - University Of Delaware
item PARK, SUNHEE - University Of Delaware
item ROSEN, BENJAMIN - University Of California
item LI, YUPENG - University Of Georgia
item GONZALEZ, ALVARO - University Of Delaware
item YAN, ZHE - University Of Missouri
item KITTO, SHERRY - University Of Delaware
item Grusak, Michael
item JACKSON, SCOTT - University Of Georgia
item STACEY, GARY - University Of Missouri
item COOK, DOUGLAS - University Of California
item GREEN, PAMELA - University Of Delaware
item SHERRIER, D - University Of Delaware
item MEYERS, BLAKE - University Of Delaware

Submitted to: Genes and Development
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/20/2011
Publication Date: 12/1/2011
Citation: Zhai, J., Jeong, D.-H., De Paoli, E., Park, S., Rosen, B.D., Li, Y., Gonzalez, A.J., Yan, Z., Kitto, S.L., Grusak, M.A., Jackson, S.A., Stacey, G., Cook, D.R., Green, P.J., Sherrier, D.J., Meyers, B.C. 2011. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes and Development. 25:2540-2553.

Interpretive Summary: Plants control various growth, nutrition-related, and pathogen defense traits by turning different genes on or off at the proper time, and in the proper tissue(s). One control mechanism involves the use of genetic material called micro ribonucleic acid, or miRNA. Certain types of miRNA can trigger the production of other RNA types; these are the so-called small interfering RNA’s, or siRNA. Thanks to new methods that have allowed us to identify and measure millions of copies of miRNA and siRNA in plant samples, we have been able to understand how these RNA fragments are used to control genes related to nitrogen nutrition in legume species. Nitrogen is important for general plant growth and yield, but proper nitrogen nutrition is also critical for the production of amino acids and protein in the plant and in its seeds. Thus, for agronomic legumes, such as bean, pea, and soybean, this new understanding about RNA types are important, because it will help lead to new strategies for the development of seed crop cultivars with elevated concentrations of proteins, as well as improved yield due to better disease resistance.

Technical Abstract: Legumes and many nonleguminous plants enter symbiotic interactions with microbes, and it is poorly understood how host plants respond to promote beneficial, symbiotic microbial interactions while suppressing those that are deleterious or pathogenic. Trans-acting siRNAs (tasiRNAs) negatively regulate target transcripts and are characterized by siRNAs spaced in 21-nucleotide (nt) "phased" intervals, a pattern formed by DICER-LIKE 4 (DCL4) processing. A search for phased siRNAs (phasiRNAs) found at least 114 Medicago loci, the majority of which were defense-related NB-LRR-encoding genes. We identified three highly abundant 22-nt microRNA (miRNA) families that target conserved domains in these NB-LRRs and trigger the production of trans-acting siRNAs. High levels of small RNAs were matched to >60% of all ~540 encoded Medicago NB-LRRs; in the potato, a model for mycorrhizal interactions, phasiRNAs were also produced from NB-LRRs. DCL2 and SGS3 transcripts were also cleaved by these 22-nt miRNAs, generating phasiRNAs, suggesting synchronization between silencing and pathogen defense pathways. In addition, a new example of apparent "two-hit" phasiRNA processing was identified. Our data reveal complex tasiRNA-based regulation of NB-LRRs that potentially evolved to facilitate symbiotic interactions and demonstrate miRNAs as master regulators of a large gene family via the targeting of highly conserved, protein-coding motifs, a new paradigm for miRNA function.