State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China
Hong Lu
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Corresponding author
Xiaoyue Fan
College of Plant Protection, Shandong Agricultural University, Tai’an 271018, China
Jiaming Zhu
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Jianfei Shi
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China
Wan Zhao
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Yan Xiao
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China
Yongyu Xu
College of Plant Protection, Shandong Agricultural University, Tai’an 271018, China
Jinfeng Chen
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Feng Cui
State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Corresponding author
Summary: Extracellular vesicle (EV)-mediated small RNA trafficking plays an important role in intercellular and interspecies communication. Plant arboviruses keep homeostasis in insect vectors, thus ensuring vector survival and viral transmission. How plant EV-mediated cross-kingdom RNA interference participates in viral infection in insect vectors remains unknown. Here, we successfully isolate rice EVs and identify a batch of microRNAs (miRNAs) encapsulated in EVs. Two EV-enriched rice miRNAs, Osa-miR159a.1-1 and Osa-miR167a, are transported into midgut epithelial cells of small brown planthopper, which is a competent vector of rice stripe virus (RSV). Osa-miR159a.1-1 elevates the expression of a phospholipase C by enhancing its mRNA stability, inducing the downstream CSL expression to inhibit apoptosis for the benefit of RSV replication. On the other hand, Osa-miR167a directly binds RSV RdRp to suppress viral replication. This differential regulation of EV-mediated cross-kingdom RNA interference contributes to arbovirus homeostasis in insect vectors and the following efficient transmission.