MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs
- Jixian Zhai1,2,
- Dong-Hoon Jeong1,2,
- Emanuele De Paoli1,2,7,
- Sunhee Park1,2,
- Benjamin D. Rosen3,
- Yupeng Li4,
- Alvaro J. González2,
- Zhe Yan5,
- Sherry L. Kitto1,
- Michael A. Grusak6,
- Scott A. Jackson4,
- Gary Stacey5,
- Douglas R. Cook3,
- Pamela J. Green1,2,
- D. Janine Sherrier1,2 and
- Blake C. Meyers1,2,8
- 1Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware 19717, USA;
- 2Delaware Biotechnology Institute, University of Delaware, Newark, Delaware 19711, USA;
- 3Department of Plant Pathology, University of California at Davis, Davis, California 95616, USA;
- 4Institute for Plant Breeding, Genetics, and Genomics, University of Georgia, Athens, Georgia 30602, USA;
- 5Department of Plant Microbiology and Pathology, University of Missouri, Columbia, Missouri 65211, USA;
- 6USDA-ARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030, USA
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.
Keywords
Footnotes
-
↵8 Corresponding author.
E-mail meyers{at}dbi.udel.edu
-
Supplemental material is available for this article.
-
Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.177527.111.
- Received August 26, 2011.
- Accepted October 20, 2011.
- Copyright © 2011 by Cold Spring Harbor Laboratory Press
