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PEBP regulates balance between apoptosis and autophagy, enabling coexistence of arbovirus and insect vector

View ORCID ProfileShifan Wang, View ORCID ProfileHuijuan Guo, View ORCID ProfileKeyan Zhu-Salzman, Feng Ge, View ORCID ProfileYucheng Sun
doi: https://doi.org/10.1101/2021.01.19.427364
Shifan Wang
aState Key Laboratory of Integrated Pest Management and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
bCAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China
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Huijuan Guo
aState Key Laboratory of Integrated Pest Management and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
bCAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China
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Keyan Zhu-Salzman
cDepartment of Entomology, Texas A&M University, College Station, TX 77843, USA
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Feng Ge
aState Key Laboratory of Integrated Pest Management and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
bCAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China
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  • For correspondence: sunyc@ioz.ac.cn gef@ioz.ac.cn
Yucheng Sun
aState Key Laboratory of Integrated Pest Management and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
bCAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China
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  • For correspondence: sunyc@ioz.ac.cn gef@ioz.ac.cn
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Abstract

Apoptosis and autophagy are two most prominent forms of programmed cell deaths (PCD) that have been implicated in antiviral immunity in vertebrate and plant hosts. Arboviruses are able to coexist with its arthropod vectors by coordinating the PCD immunity, but the regulatory mechanism involved is largely unknown. We found that the coat protein (CP) of an insect-borne plant virus TYLCV directly interacted with a phosphatidylethanolamine-binding protein (PEBP) of its insect vector whitefly to negatively influence the MAPK signaling cascade. As a result, the apoptosis was activated in whitefly which increased viral loading. Simultaneously, the PEBP4-CP interaction liberated ATG8, the hallmark of autophagy initiation, and eliminates arbovirus. Furthermore, apoptosis-promoted virus loading was compromised by agonist-induced autophagy, but autophagy-associated suppression on virus loading was unaffected by apoptosis agonist or inhibitor, suggesting that virus loading was predominantly determined by autophagy rather than by apoptosis. Our results demonstrated that maintaining a mild immune response by coordinating apoptosis and autophagy processes presumably could facilitate coexistence of the arbovirus and its insect vector. Taken together, immune homeostasis shaped by two types of PCD may facilitate the arbovirus preservation within the insect vector.

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Highlights

  • Interaction between whitefly PEBP4 and TYLCV CP suppresses phosphorylation of MAPK cascade, activating apoptosis

  • TYLCV CP liberates PEBP4-bound ATG8, resulting in lipidation of ATG8 and initiation of autophagy.

  • PEBP4 balances apoptosis and autophagy in viruliferous whitefly to optimize virus loading without obvious fitness cost.

Competing Interest Statement

The authors have declared no competing interest.

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Posted January 20, 2021.
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PEBP regulates balance between apoptosis and autophagy, enabling coexistence of arbovirus and insect vector
Shifan Wang, Huijuan Guo, Keyan Zhu-Salzman, Feng Ge, Yucheng Sun
bioRxiv 2021.01.19.427364; doi: https://doi.org/10.1101/2021.01.19.427364
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PEBP regulates balance between apoptosis and autophagy, enabling coexistence of arbovirus and insect vector
Shifan Wang, Huijuan Guo, Keyan Zhu-Salzman, Feng Ge, Yucheng Sun
bioRxiv 2021.01.19.427364; doi: https://doi.org/10.1101/2021.01.19.427364

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