Arabidopsis miR827 mediates post‐transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. (26th August 2016)

• Record Type: Journal Article
• Authors: Hewezi, Tarek; Piya, Sarbottam; Qi, Mingsheng; Balasubramaniam, Muthukumar; Rice, J. Hollis; Baum, Thomas J.
• Is Part Of: Plant journal. Volume 88:Number 2(2016:Oct.)
• Page Start: 179
• Page End: 192
• Publication Date: 2016-08-26
• Subjects: miR827 -- Arabidopsis -- cyst nematodes -- Heterodera schachtii -- post‐transcriptional gene silencing -- syncytium -- immune responses -- ubiquitin E3 ligases -- yeast two‐hybrid; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.13238
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: MicroRNAs (miRNAs) are a major class of small non‐coding RNAs with emerging functions in biotic and abiotic interactions. Here, we report on a new functional role of Arabidopsis miR827 and its NITROGEN LIMITATION ADAPTATION ( NLA ) target gene in mediating plant susceptibility to the beet cyst nematode Heterodera schachtii . Cyst nematodes are sedentary endoparasites that induce the formation of multinucleated feeding structures termed syncytia in the roots of host plants. Using promoter:GUS fusion assays we established that miR827 was activated in the initial feeding cells and this activation was maintained in the syncytium during all sedentary stages of nematode development. Meanwhile, the NLA target gene, which encodes an ubiquitin E3 ligase enzyme, was post‐transcriptionally silenced in the syncytium to permanently suppress its activity during all nematode parasitic stages. Overexpression of miR827 in Arabidopsis resulted in hyper‐susceptibility to H. schachtii . In contrast, inactivation of miR827 activity through target mimicry or by overexpression a miR827‐resistant cDNA of NLA produced the opposite phenotype of reduced plant susceptibility to H. schachtii . Gene expression analysis of several pathogenesis‐related genes together with Agrobacterium ‐mediated transient expression in Nicotiana benthamiana provided strong evidence that miR827‐mediated downregulation of NLA to suppress basal defense pathways. In addition, using yeast two‐hybrid screens we identified several candidates of NLA‐interacting proteins that are involved in a wide range of biological processes and molecular functions, including three pathogenesis‐related proteins. Taken together, we conclude that nematode‐activated miR827 in the syncytium is necessary to suppress immune responses in order to establish infection and cause disease. Significance Statement: Cyst nematodes engage in sophisticated and prolonged periods of biotrophic interaction with host plants; suppression of basal defenses is vital for successful parasitism, but how these nematodes suppress plant basal defenses remain largely unknown. Here we show that post‐transcriptional gene silencing of an Arabidopsis ubiquitin E3 ligase gene by miR827 in nematode feeding sites inactivated basal defenses and enhanced plant susceptibility, while inactivating miR827 activity reduced plant susceptibility.