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Plant Physiol. 2018 May;177(1):352-368. doi: 10.1104/pp.17.01665. Epub 2018 Mar 16.

Magnaporthe oryzae Induces the Expression of a MicroRNA to Suppress the Immune Response in Rice.

Zhang X1,2,3, Bao Y1,2, Shan D1,2, Wang Z1,2, Song X1,2, Wang Z1,2, Wang J1,2, He L4, Wu L5, Zhang Z1,2, Niu D1,2, Jin H6, Zhao H7,2.

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College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.
Key Laboratory of Integrated Management of Crop Diseases and Pests, Nanjing Agricultural University, Ministry of Education, Nanjing 210095, China.
Institute of Industrial Crops, Shanxi Academy of Agricultural Sciences, Taiyuan 030000, Shanxi, China.
State Key Laboratory of Crop Genetics and Germplasm Enhancement, Cytogenetics Institute, Nanjing Agricultural University, Nanjing 210095, China.
Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China.
Department of Plant Pathology and Microbiology, University of California, Riverside, California 92521
College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China


MicroRNAs play crucial roles in plant responses to pathogen infections. The rice blast disease, caused by the fungus Magnaporthe oryzae, is the most important disease of rice (Oryza sativa). To explore the microRNA species that participate in rice immunity against the rice blast disease, we compared the expression of small RNAs between mock- and M. oryzae-treated rice. We found that infection by M. oryzae strain Guy11 specifically induced the expression of rice miR319 and, consequently, suppressed its target gene TEOSINTE BRANCHED/CYCLOIDEA/PROLIFERATING CELL FACTOR1 (OsTCP21), which encodes a transcription factor. Using transgenic rice that overexpresses miR319b (OE) or expresses OsTCP21-Res (which is resistant to miR319-mediated silencing), we found that OsTCP21 is a positive regulator of the rice defense response against the blast disease. When wild-type and miR319b-OE rice were infected by Guy11, multiple jasmonic acid (JA) synthetic and signaling components were suppressed, indicating that Guy11 suppresses JA signaling through inducing miR319. In particular, we found that LIPOXYGENASE2 (LOX2) and LOX5 were specifically suppressed by miR319 overexpression or by Guy11 infection. LOXs are the key enzymes of JA synthesis, which catalyze the conversion of α-linoleic acid to hydroperoxy-octadecadienoic acid. The application of α-linoleic acid rescued disease symptoms on the OsTCP21-Res rice but not wild-type rice, supporting our hypothesis that OsLOX2 and OsLOX5 are the key JA synthesis genes hijacked by Guy11 to subvert host immunity and facilitate pathogenicity. We propose that induced expression of OsLOX2/5 may improve resistance to the rice blast disease.

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