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ARS Home » Midwest Area » Ames, Iowa » Corn Insects and Crop Genetics Research » Research » Publications at this Location » Publication #304122
Title: The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling

Author
item LIU, JIE - Chinese Academy Of Sciences
item CHENG, XILIU - Chinese Academy Of Sciences
item LIU, DA - Chinese Academy Of Sciences
item XU, WEIHUI - Iowa State University
item Wise, Roger
item SHEN, QIAN-HUA - Chinese Academy Of Sciences

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/15/2014
Publication Date: 12/11/2014
Citation: Liu, J., Cheng, X., Liu, D., Xu, W., Wise, R.P., Shen, Q. 2014. The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling. PLoS Genetics. 10(12):e1004755. DOI:10.1371/journal.pgen.1004755.

Interpretive Summary: Crop loss caused by disease remains one of the greatest challenges in agriculture in both developed and developing countries. Pathogenic fungi, viruses, bacteria, insects, and nematodes parasitize agronomic and horticultural crops, as well as commercial and recreational forests. Epidemics can be accelerated during shifting climate conditions. Thus, basic research on plant disease resistance, and translation of new technologies, are needed to offset pathogen-induced yield loss and enhance food security. Powdery mildew is a devastating fungal disease, but also an ideal system to explore the interactions of fungal pathogens with their host plants. This report describes novel and timely research on microRNA regulatory elements and their control of resistance-gene mediated immunity. The barley Mla gene confers disease resistance against the powdery mildew fungus, yet how this important gene is regulated to carry out its tasks is less clear. MicroRNAs (miRNAs) are 21-24 nucleotide small RNAs that repress gene expression in plants and animals. We show that specific members of the miR2009 family target distinct Mla variants to trigger Mla-dependent resistance responses. Overexpression of miR2009 members attenuates Mla-mediated powdery mildew disease resistance and cell-death, indicating an important role of the miR2009 family in immune signaling. This discovery establishes a new role for microRNAs as regulators of plant defense. Because common themes govern all plant-pathogen interactions, this finding provides new knowledge of broad significance to plant scientists, and to growers who utilize disease resistance to protect their crops.

Technical Abstract: Barley Mla alleles encode coiled-coil (CC), nucleotide binding and leucine-rich repeat (NB-LRR) intracellular receptors that trigger isolate-specific immune responses against the powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). How Mla or NB-LRR genes in grass species are regulated at posttranscriptional level is not clear. The microRNA family, miR2009, comprise four members that differentially regulate distinct Mla alleles in barley. We show that miR2009 members guide the cleavage of Mla1 transcripts in barley, and block or reduce the accumulation of MLA1 protein in Nicotiana benthamiana. Regulation specificity is determined by variation in a unique single-nucleotide-polymorphism (SNP) in mature miR2009 family members and two SNPs in the Mla miR2009-binding site that separates these alleles into three groups. Further, we demonstrate in barley and N. benthamiana that 22-nt miR2009s trigger the biogenesis of 21-nt phased siRNAs (phasiRNAs) and together form a feed-forward regulation loop for controlling group III Mla genes in an AGO1-dependent manner, in which transcript cleavage and translation suppression are both involved. Overexpression of miR2009 members specifically attenuates MLA1 but not MLA10-triggered disease resistance and cell-death signaling. We propose an important role of miR2009 family in dampening of immune response signaling triggered by a group of MLA immune receptors.