Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

ABSTRACT Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Gemin...

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Autores principales:	Xin-Ru Wang, Chao Wang, Fei-Xue Ban, Murad Ghanim, Li-Long Pan, Li-Xin Qian, Yin-Quan Liu, Xiao-Wei Wang, Shu-Sheng Liu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	apoptosis DNA virus begomovirus insect vector transmission whitefly Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/463288d59b15404b9c8f89b7be9be332
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spelling	oai:doaj.org-article:463288d59b15404b9c8f89b7be9be3322021-12-02T19:47:33ZApoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission10.1128/mSystems.00433-202379-5077https://doaj.org/article/463288d59b15404b9c8f89b7be9be3322020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00433-20https://doaj.org/toc/2379-5077ABSTRACT Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci. Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo. Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission. IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.Xin-Ru WangChao WangFei-Xue BanMurad GhanimLi-Long PanLi-Xin QianYin-Quan LiuXiao-Wei WangShu-Sheng LiuAmerican Society for MicrobiologyarticleapoptosisDNA virusbegomovirusinsect vectortransmissionwhiteflyMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	apoptosis DNA virus begomovirus insect vector transmission whitefly Microbiology QR1-502
spellingShingle	apoptosis DNA virus begomovirus insect vector transmission whitefly Microbiology QR1-502 Xin-Ru Wang Chao Wang Fei-Xue Ban Murad Ghanim Li-Long Pan Li-Xin Qian Yin-Quan Liu Xiao-Wei Wang Shu-Sheng Liu Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
description	ABSTRACT Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci. Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo. Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission. IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.
format	article
author	Xin-Ru Wang Chao Wang Fei-Xue Ban Murad Ghanim Li-Long Pan Li-Xin Qian Yin-Quan Liu Xiao-Wei Wang Shu-Sheng Liu
author_facet	Xin-Ru Wang Chao Wang Fei-Xue Ban Murad Ghanim Li-Long Pan Li-Xin Qian Yin-Quan Liu Xiao-Wei Wang Shu-Sheng Liu
author_sort	Xin-Ru Wang
title	Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
title_short	Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
title_full	Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
title_fullStr	Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
title_full_unstemmed	Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
title_sort	apoptosis in a whitefly vector activated by a begomovirus enhances viral transmission
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/463288d59b15404b9c8f89b7be9be332
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Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

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