Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen.
Plant pathogenic fungi represent the largest group of disease-causing agents on crop plants, and are a constant and major threat to agriculture worldwide. Recent studies have shown that engineered production of RNA interference (RNAi)-inducing dsRNA in host plants can trigger specific fungal gene silencing and confer resistance to fungal pathogens1-7. Although these findings illustrate efficient uptake of host RNAi triggers by pathogenic fungi, it is unknown whether or not such an uptake mechanism has been evolved for a natural biological function in fungus-host interactions. Here, we show that in response to infection with Verticillium dahliae (a vascular fungal pathogen responsible for devastating wilt diseases in many crops) cotton plants increase production of microRNA 166 (miR166) and miR159 and export both to the fungal hyphae for specific silencing. We found that two V. dahliae genes encoding a Ca2+-dependent cysteine protease (Clp-1) and an isotrichodermin C-15 hydroxylase (HiC-15), and targeted by miR166 and miR159, respectively, are both essential for fungal virulence. Notably, V. dahliae strains expressing either Clp-1 or HiC-15 rendered resistant to the respective miRNA exhibited drastically enhanced virulence in cotton plants. Together, our findings identify a novel defence strategy of host plants by exporting specific miRNAs to induce cross-kingdom gene silencing in pathogenic fungi and confer disease resistance.
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.|College of Life Sciences, University of the Chinese Academy of Sciences, Beijing 100049, China.
Tao
T
Zhang
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.|College of Life Sciences, University of the Chinese Academy of Sciences, Beijing 100049, China.
Yun-Long
YL
Zhao
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Jian-Hua
0000-0003-2554-1930
JH
Zhao
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Sheng
S
Wang
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Yun
Y
Jin
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Zhong-Qi
0000-0003-2814-0243
ZQ
Chen
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Yuan-Yuan
YY
Fang
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.
Chen-Lei
0000-0002-6630-9049
CL
Hua
Department of Plant Pathology and Microbiology, Institute for Integrative Genome Biology, University of California, Riverside, California, 92521, USA.
Shou-Wei
SW
Ding
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China.|College of Life Sciences, University of the Chinese Academy of Sciences, Beijing 100049, China.
Hui-Shan
HS
Guo
D060467:Disease Resistance / Q000235:genetics*; D015966:Gene Expression Regulation, Fungal; D020868:Gene Silencing; D003368:Gossypium / Q000235:genetics* / Q000276:immunology / Q000382:microbiology; D025301:Hyphae; D035683:MicroRNAs / Q000378:metabolism*; D010935:Plant Diseases / Q000276:immunology* / Q000382:microbiology; D020172:Verticillium / Q000235:genetics / Q000472:pathogenicity*; D014774:Virulence / Q000235:genetics
D035683:MicroRNAs