title: MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs.
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.
authors.affiliation: Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware 19717, USA.
authors.forename: Jixian
authors.initials: J
authors.lastname: Zhai
authors.forename: Dong-Hoon
authors.initials: DH
authors.lastname: Jeong
authors.forename: Emanuele
authors.initials: E
authors.lastname: De Paoli
authors.forename: Sunhee
authors.initials: S
authors.lastname: Park
authors.forename: Benjamin D
authors.initials: BD
authors.lastname: Rosen
authors.forename: Yupeng
authors.initials: Y
authors.lastname: Li
authors.forename: Alvaro J
authors.initials: AJ
authors.lastname: González
authors.forename: Zhe
authors.initials: Z
authors.lastname: Yan
authors.forename: Sherry L
authors.initials: SL
authors.lastname: Kitto
authors.forename: Michael A
authors.initials: MA
authors.lastname: Grusak
authors.forename: Scott A
authors.initials: SA
authors.lastname: Jackson
authors.forename: Gary
authors.initials: G
authors.lastname: Stacey
authors.forename: Douglas R
authors.initials: DR
authors.lastname: Cook
authors.forename: Pamela J
authors.initials: PJ
authors.lastname: Green
authors.forename: D Janine
authors.initials: DJ
authors.lastname: Sherrier
authors.forename: Blake C
authors.initials: BC
authors.lastname: Meyers
mesh_terms: D001483:Base Sequence; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D035683:MicroRNAs / Q000378:metabolism*; D008969:Molecular Sequence Data; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D010944:Plants / Q000235:genetics*; D034741:RNA, Small Interfering / Q000378:metabolism*
chemical_list: D035683:MicroRNAs; D010940:Plant Proteins; D034741:RNA, Small Interfering