A viral protein orchestrates rice ethylene signaling to coordinate viral infection and insect vector-mediated transmission

• Published in: Molecular plant Vol. 15; no. 4; pp. 689 - 705
• Main Authors: Zhao, Yaling, Cao, Xue, Zhong, Weihua, Zhou, Shunkang, Li, Zhanbiao, An, Hong, Liu, Xiahua, Wu, Ruifeng, Bohora, Surakshya, Wu, Yan, Liang, Zhenyi, Chen, Jiahao, Yang, Xin, Zhou, Guohui, Zhang, Tong
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 04.04.2022
• Subjects: Animals; arboviruses; ethylene signaling; Ethylenes; Hemiptera - metabolism; host-virus-vector interaction; Insect Vectors; Oryza - metabolism; OsEIL2; OsRTH2; Plant Diseases; SRBSDV; Viral Proteins - metabolism; Virus Diseases; OsRTH2; ethylene signaling; host-virus-vector interaction; OsEIL2; arboviruses; SRBSDV
• ISSN: 1674-2052; 1752-9867
• DOI: 10.1016/j.molp.2022.01.006

Arthropod-borne viruses cause serious threats to human health and global agriculture by rapidly spreading via insect vectors. Southern rice black-streaked dwarf virus (SRBSDV) is the most damaging rice-infecting virus that is frequently transmitted by planthoppers. However, the molecular mechanisms underlying its propagation in the host plants and epidemics in the field are largely unknown. Here, we showed that the SRBSDV-encoded P6 protein is a key effector that regulates rice ethylene signaling to coordinate viral infection and transmission. In early SRBSDV infection, P6 interacts with OsRTH2 in the cytoplasm to activate ethylene signaling and enhance SRBSDV proliferation; this also repels the insect vector to reduce infestation. In late infection, P6 enters the nucleus, where it interacts with OsEIL2, a key transcription factor of ethylene signaling. The P6-OsEIL2 interaction suppresses ethylene signaling by preventing the dimerization of OsEIL2, thereby facilitating viral transmission by attracting the insect vector. Collectively, these findings reveal a novel molecular mechanism by which an arbovirus modulates the host defense system to promote viral infection and transmission. This study reveals that the P6 effector encoded by Southern rice black-streaked dwarf virus modulates rice ethylene signaling to support viral infection and transmission. The P6 effector interacts with OsRTH2 in the cytoplasm and enhances ethylene signaling to favor viral accumulation in host plants at the early infection stage. In the late stage of virus infection, P6 gradually translocates to the nucleus, where it suppresses ethylene signaling to attract the insect vector and facilitate viral dissemination.