A novel RAV transcription factor from pear interacts with viral RNA‐silencing suppressors to inhibit viral infection

• Published in: The Plant journal : for cell and molecular biology Vol. 120; no. 3; pp. 1079 - 1093
• Main Authors: Xie, Yin‐Shuai, Zeng, Qi, Huang, Wen‐Ting, Wang, Jin‐Ying, Li, Han‐Wei, Yu, Shang‐Zhen, Liu, Can, Zhang, Xue‐Qing, Feng, Chen‐Lu, Zhang, Wen‐Hao, Li, Tian‐Zhong, Cheng, Yu‐Qin
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.11.2024
• Subjects: Abscisic acid; apple stem grooving virus; apples; Binding; C-Terminus; Cytoplasm; DNA helicase; Fruit trees; Fruits; Gene silencing; Grapevine leafroll-associated virus 2; helicase; Host plants; Infections; Necrosis; p24; pears; Plant Diseases - genetics; Plant Diseases - virology; Plant Proteins - genetics; Plant Proteins - metabolism; Plant virus diseases; Plant viruses; Plant Viruses - genetics; Plant Viruses - physiology; Pyrus - genetics; Pyrus - metabolism; Pyrus - virology; Replicase; RNA; RNA Interference; RNA viruses; RNA, Small Interfering - genetics; RNA, Small Interfering - metabolism; RNA, Viral - genetics; RNA, Viral - metabolism; RNA-mediated interference; RNA‐silencing suppressor; siRNA; siRNA binding; Suppressors; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Viral infections; Viral Proteins - genetics; Viral Proteins - metabolism; Viruses; Vitis; siRNA binding; p24; apple stem grooving virus; helicase; RNA‐silencing suppressor; grapevine leafroll‐associated virus 2
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.17037

SUMMARY In plants, RNA silencing constitutes a strong defense against viral infection, which viruses counteract with RNA‐silencing suppressors (RSSs). Understanding the interactions between viral RSSs and host factors is crucial for elucidating the molecular arms race between viruses and host plants. We report that the helicase motif (Hel) of the replicase encoded by apple stem grooving virus (ASGV)—the main virus affecting pear trees in China—is an RSS that can inhibit both local and systemic RNA silencing, possibly by binding double‐stranded (ds) siRNA. The transcription factor related to ABSCISIC ACID INSENSITIVE3/VIVIPAROUS1 from pear (PbRAV1) enters the cytoplasm and binds Hel through its C terminus, thereby attenuating its RSS activity by reducing its binding affinity to 21‐ and 24‐nt ds siRNA, and suppressing ASGV infection. PbRAV1 can also target p24, an RSS encoded by grapevine leafroll‐associated virus 2 (GLRaV‐2), with similar negative effects on p24's suppressive function and inhibition of GLRaV‐2 infection. Moreover, like the positive role of the PbRAV1 homolog from grapevine (VvRAV1) in p24's previously reported RSS activity, ASGV Hel can also hijack VvRAV1 and employ the protein to sequester 21‐nt ds siRNA, thereby enhancing its own RSS activity and promoting ASGV infection. Furthermore, PbRAV1 neither interacts with CP, an RSS encoded by grapevine inner necrosis virus, nor has any obvious effect on CP's RSS activity. Our results identify an RSS encoded by ASGV and demonstrate that PbRAV1, representing a novel type of RAV transcription factor, plays a defensive role against viral infection by targeting viral RSSs. Significance Statement Our results demonstrate that the helicase motif (Hel) of the replicase encoded by apple stem grooving virus (ASGV) can suppress RNA silencing, and reveal that PbRAV1, a novel type of RAV transcription factor, targets two unrelated viral RSSs—ASGV Hel and GLRaV‐2 p24—to attenuate their RSS activity, thereby suppressing viral infection.