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

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 i...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 117; no. 16; pp. 9112 - 9121
Main Authors Zhang, Hehong, Li, Lulu, He, Yuqing, Qin, Qingqing, Chen, Changhai, Wei, Zhongyan, Tan, Xiaoxiang, Xie, Kaili, Zhang, Ruifang, Hong, Gaojie, Li, Jing, Li, Junmin, Yan, Chengqi, Yan, Fei, Li, Yi, Chen, Jianping, Sun, Zongtao
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 21.04.2020
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Abstract 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 (doublestranded 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.
AbstractList 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.
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.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.
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 (doublestranded 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.
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.
Author Zhang, Ruifang
Hong, Gaojie
Tan, Xiaoxiang
Li, Junmin
Yan, Fei
Li, Lulu
Wei, Zhongyan
Xie, Kaili
Li, Jing
Yan, Chengqi
Qin, Qingqing
Li, Yi
Zhang, Hehong
Chen, Changhai
He, Yuqing
Sun, Zongtao
Chen, Jianping
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Keywords OsARF17
auxin response factor
rice virus
viral proteins
auxin signaling
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Edited by Mark Estelle, University of California San Diego, La Jolla, CA, and approved March 11, 2020 (received for review October 17, 2019)
1H.Z. and L.L. contributed equally to this work.
Author contributions: H.Z., J.C., and Z.S. designed research; H.Z., L.L., Y.H., Q.Q., C.C., Z.W., X.T., K.X., R.Z., and Z.S. performed research; G.H., Jing Li, Junmin Li, C.Y., F.Y., Y.L., J.C., and Z.S. analyzed data; and H.Z. and Z.S. wrote the paper.
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Snippet Plant auxin response factor (ARF) transcription factors are an important class of key transcriptional modulators in auxin signaling. Despite the well-studied...
Auxin signaling plays essential roles in almost every aspect of plant growth and development. Auxin response factors (ARFs) are key transcriptional regulators...
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SubjectTerms Biological Sciences
Deoxyribonucleic acid
Dimerization
Disease Resistance - genetics
DNA
Double-stranded RNA
Gene Expression Regulation, Plant - immunology
Host-Pathogen Interactions - genetics
Host-Pathogen Interactions - immunology
Indoleacetic Acids - metabolism
Modulators
Mutation
Nicotiana - genetics
Nicotiana - metabolism
Nicotiana - virology
Oryza - genetics
Oryza - immunology
Oryza - virology
Plant Diseases - genetics
Plant Diseases - immunology
Plant Diseases - virology
Plant growth
Plant Leaves - metabolism
Plant Proteins - genetics
Plant Proteins - metabolism
Plant resistance
Plant viruses
Plant Viruses - immunology
Plant Viruses - metabolism
Plants, Genetically Modified
Protein Multimerization - immunology
Proteins
Recombinant Proteins - genetics
Recombinant Proteins - metabolism
Ribonucleic acid
RNA
RNA viruses
RNA Viruses - immunology
RNA Viruses - metabolism
Signal Transduction - immunology
Signaling
Transcription activation
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Viral Proteins - immunology
Viral Proteins - metabolism
Viruses
Title Distinct modes of manipulation of rice auxin response factor OsARF17 by different plant RNA viruses for infection
URI https://www.jstor.org/stable/26929681
https://www.ncbi.nlm.nih.gov/pubmed/32253321
https://www.proquest.com/docview/2394262645
https://www.proquest.com/docview/2387256662
https://pubmed.ncbi.nlm.nih.gov/PMC7183187
Volume 117
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