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Distinct modes of manipulation of rice auxin response factor OsARF17 by different plant RNA viruses for infection

Hehong Zhang,Lulu Li,Yuqing He,Qingqing Qin,Changhai Chen,Zhongyan Wei,Xiaoxiang Tan,Kaili Xie,Ruifang Zhang,G. Hong,Jing Li,Junmin Li,Chengqi Yan,Fei Yan,Yi Li,Jianping Chen,Zongtao Sun

Published 2020 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Auxin signaling plays essential roles in almost every aspect of plant growth and development. Auxin response factors (ARFs) are key transcriptional regulators of auxin signaling. However, it is not clear what roles ARF transcription factors may play in plant–pathogen, and specifically plant–virus, interactions. This study reveals that an ARF transcription factor is targeted by several independently evolved viral proteins of very different plant RNA viruses. These viral proteins impede the ARF activity in different ways, but in each case, these interactions benefit viral infection. These findings demonstrate that manipulation of the auxin signaling by viral proteins is a common pathogenicity strategy in plant RNA viruses. Plant auxin response factor (ARF) transcription factors are an important class of key transcriptional modulators in auxin signaling. Despite the well-studied roles of ARF transcription factors in plant growth and development, it is largely unknown whether, and how, ARF transcription factors may be involved in plant resistance to pathogens. We show here that two fijiviruses (double-stranded RNA viruses) utilize their proteins to disturb the dimerization of OsARF17 and repress its transcriptional activation ability, while a tenuivirus (negative-sense single-stranded RNA virus) directly interferes with the DNA binding activity of OsARF17. These interactions impair OsARF17-mediated antiviral defense. OsARF17 also confers resistance to a cytorhabdovirus and was directly targeted by one of the viral proteins. Thus, OsARF17 is the common target of several very different viruses. This suggests that OsARF17 plays a crucial role in plant defense against different types of plant viruses, and that these viruses use independently evolved viral proteins to target this key component of auxin signaling and facilitate infection.

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