Cargando…

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

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,...

Descripción completa

Detalles Bibliográficos
Autores principales: Wang, Xin-Ru, Wang, Chao, Ban, Fei-Xue, Ghanim, Murad, Pan, Li-Long, Qian, Li-Xin, Liu, Yin-Quan, Wang, Xiao-Wei, Liu, Shu-Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7511215/
https://www.ncbi.nlm.nih.gov/pubmed/32963100
http://dx.doi.org/10.1128/mSystems.00433-20
_version_ 1783585919429771264
author Wang, Xin-Ru
Wang, Chao
Ban, Fei-Xue
Ghanim, Murad
Pan, Li-Long
Qian, Li-Xin
Liu, Yin-Quan
Wang, Xiao-Wei
Liu, Shu-Sheng
author_facet Wang, Xin-Ru
Wang, Chao
Ban, Fei-Xue
Ghanim, Murad
Pan, Li-Long
Qian, Li-Xin
Liu, Yin-Quan
Wang, Xiao-Wei
Liu, Shu-Sheng
author_sort Wang, Xin-Ru
collection PubMed
description 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 Online
Article
Text
id pubmed-7511215
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-75112152020-10-01 Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission Wang, Xin-Ru Wang, Chao Ban, Fei-Xue Ghanim, Murad Pan, Li-Long Qian, Li-Xin Liu, Yin-Quan Wang, Xiao-Wei Liu, Shu-Sheng mSystems Research Article 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. American Society for Microbiology 2020-09-22 /pmc/articles/PMC7511215/ /pubmed/32963100 http://dx.doi.org/10.1128/mSystems.00433-20 Text en Copyright © 2020 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wang, Xin-Ru
Wang, Chao
Ban, Fei-Xue
Ghanim, Murad
Pan, Li-Long
Qian, Li-Xin
Liu, Yin-Quan
Wang, Xiao-Wei
Liu, Shu-Sheng
Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission
title 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_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7511215/
https://www.ncbi.nlm.nih.gov/pubmed/32963100
http://dx.doi.org/10.1128/mSystems.00433-20
work_keys_str_mv AT wangxinru apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT wangchao apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT banfeixue apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT ghanimmurad apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT panlilong apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT qianlixin apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT liuyinquan apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT wangxiaowei apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission
AT liushusheng apoptosisinawhiteflyvectoractivatedbyabegomovirusenhancesviraltransmission