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PMID: 22156213 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

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

Genes & development ·Vol. 25 ·No. 23 ·2011-12-01 ·Pages 2540-53

Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA, Jackson SA, Stacey G, Cook DR, Green PJ, Sherrier DJ, Meyers BC

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.

MeSH Terms
Base Sequence Gene Expression Regulation, Plant Genes, Plant MicroRNAs/metabolism Molecular Sequence Data Plant Proteins/genetics,metabolism Plants/genetics RNA, Small Interfering/metabolism
Chemicals
MicroRNAs Plant Proteins RNA, Small Interfering
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Zhai Jixian
Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware 19717, USA.
Jeong Dong-Hoon
De Paoli Emanuele
Park Sunhee
Rosen Benjamin D
Li Yupeng
González Alvaro J
Yan Zhe
Kitto Sherry L
Grusak Michael A
Jackson Scott A
Stacey Gary
Cook Douglas R
Green Pamela J
Sherrier D Janine
Meyers Blake C
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Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
1549-5477
DOI
10.1101/gad.177527.111
Published
2011-12-01
Pages
2540-53
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC3243063
Subset
IM
External Links
PubMed source DOI: 10.1101/gad.177527.111 PMC Full Text View journal details
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