A WW domain-containing protein forms immune nuclear bodies against begomoviruses

Detalhes bibliográficos
Autor(a) principal: Calil, Iara P.
Data de Publicação: 2018
Outros Autores: Quadros, Iana P. S., Araújo, Thais C., Duarte, Christiane E. M., Gouveia-Mageste, Bianca C., Silva, José Cleydson F., Brustolini, Otávio J. B., Teixeira, Ruan M., Oliveira, Cauê N., Milagres, Rafael W. M. M., Martins, Gilberto S., Reis, Pedro A. B., Machado, Joao Paulo B., Fontes, Elizabeth P. B., Chory, Joanne
Tipo de documento: Artigo
Idioma: eng
Título da fonte: LOCUS Repositório Institucional da UFV
Texto Completo: https://doi.org/10.1016/j.molp.2018.09.009
http://www.locus.ufv.br/handle/123456789/24307
Resumo: The bipartite begomoviruses (Geminiviridae family), which are DNA viruses that replicate in the nucleus of infected cells, encode the nuclear shuttle protein (NSP) to facilitate the translocation of viral DNA from the nucleus to the cytoplasm via nuclear pores. This intracellular trafficking of NSP–DNA complexes is accessorized by the NSP-interacting guanosine triphosphatase (NIG) at the cytosolic side. Here, we report the nuclear redistribution of NIG by AtWWP1, a WW domain-containing protein that forms immune nuclear bodies (NBs) against begomoviruses. We demonstrated that AtWWP1 relocates NIG from the cytoplasm to the nucleus where it is confined to AtWWP1-NBs, suggesting that the NIG-AtWWP1 interaction may interfere with the NIG pro-viral function associated with its cytosolic localization. Consistent with this assumption, loss of AtWWP1 function cuased plants more susceptible to begomovirus infection, whereas overexpression of AtWWP1 enhanced plant resistance to begomovirus. Furthermore, we found that a mutant version of AtWWP1 defective for NB formation was no longer capable of interacting with and relocating NIG to the nucleus and lost its immune function against begomovirus. The antiviral function of AtWWP1-NBs, however, could be antagonized by viral infection that induced either the disruption or a decrease in the number of AtWWP1-NBs. Collectively, these results led us to propose that AtWWP1 organizes nuclear structures into nuclear foci, which provide intrinsic immunity against begomovirus infection.
id UFV_d30725cda5040da7e607770b25d45e08
oai_identifier_str oai:locus.ufv.br:123456789/24307
network_acronym_str UFV
network_name_str LOCUS Repositório Institucional da UFV
repository_id_str 2145
spelling Calil, Iara P.Quadros, Iana P. S.Araújo, Thais C.Duarte, Christiane E. M.Gouveia-Mageste, Bianca C.Silva, José Cleydson F.Brustolini, Otávio J. B.Teixeira, Ruan M.Oliveira, Cauê N.Milagres, Rafael W. M. M.Martins, Gilberto S.Reis, Pedro A. B.Machado, Joao Paulo B.Fontes, Elizabeth P. B.Chory, Joanne2019-04-04T17:38:08Z2019-04-04T17:38:08Z2018-12-031674-2052https://doi.org/10.1016/j.molp.2018.09.009http://www.locus.ufv.br/handle/123456789/24307The bipartite begomoviruses (Geminiviridae family), which are DNA viruses that replicate in the nucleus of infected cells, encode the nuclear shuttle protein (NSP) to facilitate the translocation of viral DNA from the nucleus to the cytoplasm via nuclear pores. This intracellular trafficking of NSP–DNA complexes is accessorized by the NSP-interacting guanosine triphosphatase (NIG) at the cytosolic side. Here, we report the nuclear redistribution of NIG by AtWWP1, a WW domain-containing protein that forms immune nuclear bodies (NBs) against begomoviruses. We demonstrated that AtWWP1 relocates NIG from the cytoplasm to the nucleus where it is confined to AtWWP1-NBs, suggesting that the NIG-AtWWP1 interaction may interfere with the NIG pro-viral function associated with its cytosolic localization. Consistent with this assumption, loss of AtWWP1 function cuased plants more susceptible to begomovirus infection, whereas overexpression of AtWWP1 enhanced plant resistance to begomovirus. Furthermore, we found that a mutant version of AtWWP1 defective for NB formation was no longer capable of interacting with and relocating NIG to the nucleus and lost its immune function against begomovirus. The antiviral function of AtWWP1-NBs, however, could be antagonized by viral infection that induced either the disruption or a decrease in the number of AtWWP1-NBs. Collectively, these results led us to propose that AtWWP1 organizes nuclear structures into nuclear foci, which provide intrinsic immunity against begomovirus infection.engMolecular PlantVolume 11, Issue 12, Pages 1449-1465, December 2018Elsevier B. V.info:eu-repo/semantics/openAccessNuclear bodiesAntiviral immunityBegomovirusNIGAtWWP1A WW domain-containing protein forms immune nuclear bodies against begomovirusesinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfreponame:LOCUS Repositório Institucional da UFVinstname:Universidade Federal de Viçosa (UFV)instacron:UFVORIGINALartigo.pdfartigo.pdfTexto completoapplication/pdf2959500https://locus.ufv.br//bitstream/123456789/24307/1/artigo.pdf1a90e6a7130ff20cea65f3af95d095c4MD51LICENSElicense.txtlicense.txttext/plain; charset=utf-81748https://locus.ufv.br//bitstream/123456789/24307/2/license.txt8a4605be74aa9ea9d79846c1fba20a33MD52123456789/243072019-04-04 14:39:08.739oai:locus.ufv.br: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Repositório InstitucionalPUBhttps://www.locus.ufv.br/oai/requestfabiojreis@ufv.bropendoar:21452019-04-04T17:39:08LOCUS Repositório Institucional da UFV - Universidade Federal de Viçosa (UFV)false
dc.title.en.fl_str_mv A WW domain-containing protein forms immune nuclear bodies against begomoviruses
title A WW domain-containing protein forms immune nuclear bodies against begomoviruses
spellingShingle A WW domain-containing protein forms immune nuclear bodies against begomoviruses
Calil, Iara P.
Nuclear bodies
Antiviral immunity
Begomovirus
NIG
AtWWP1
title_short A WW domain-containing protein forms immune nuclear bodies against begomoviruses
title_full A WW domain-containing protein forms immune nuclear bodies against begomoviruses
title_fullStr A WW domain-containing protein forms immune nuclear bodies against begomoviruses
title_full_unstemmed A WW domain-containing protein forms immune nuclear bodies against begomoviruses
title_sort A WW domain-containing protein forms immune nuclear bodies against begomoviruses
author Calil, Iara P.
author_facet Calil, Iara P.
Quadros, Iana P. S.
Araújo, Thais C.
Duarte, Christiane E. M.
Gouveia-Mageste, Bianca C.
Silva, José Cleydson F.
Brustolini, Otávio J. B.
Teixeira, Ruan M.
Oliveira, Cauê N.
Milagres, Rafael W. M. M.
Martins, Gilberto S.
Reis, Pedro A. B.
Machado, Joao Paulo B.
Fontes, Elizabeth P. B.
Chory, Joanne
author_role author
author2 Quadros, Iana P. S.
Araújo, Thais C.
Duarte, Christiane E. M.
Gouveia-Mageste, Bianca C.
Silva, José Cleydson F.
Brustolini, Otávio J. B.
Teixeira, Ruan M.
Oliveira, Cauê N.
Milagres, Rafael W. M. M.
Martins, Gilberto S.
Reis, Pedro A. B.
Machado, Joao Paulo B.
Fontes, Elizabeth P. B.
Chory, Joanne
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Calil, Iara P.
Quadros, Iana P. S.
Araújo, Thais C.
Duarte, Christiane E. M.
Gouveia-Mageste, Bianca C.
Silva, José Cleydson F.
Brustolini, Otávio J. B.
Teixeira, Ruan M.
Oliveira, Cauê N.
Milagres, Rafael W. M. M.
Martins, Gilberto S.
Reis, Pedro A. B.
Machado, Joao Paulo B.
Fontes, Elizabeth P. B.
Chory, Joanne
dc.subject.pt-BR.fl_str_mv Nuclear bodies
Antiviral immunity
Begomovirus
NIG
AtWWP1
topic Nuclear bodies
Antiviral immunity
Begomovirus
NIG
AtWWP1
description The bipartite begomoviruses (Geminiviridae family), which are DNA viruses that replicate in the nucleus of infected cells, encode the nuclear shuttle protein (NSP) to facilitate the translocation of viral DNA from the nucleus to the cytoplasm via nuclear pores. This intracellular trafficking of NSP–DNA complexes is accessorized by the NSP-interacting guanosine triphosphatase (NIG) at the cytosolic side. Here, we report the nuclear redistribution of NIG by AtWWP1, a WW domain-containing protein that forms immune nuclear bodies (NBs) against begomoviruses. We demonstrated that AtWWP1 relocates NIG from the cytoplasm to the nucleus where it is confined to AtWWP1-NBs, suggesting that the NIG-AtWWP1 interaction may interfere with the NIG pro-viral function associated with its cytosolic localization. Consistent with this assumption, loss of AtWWP1 function cuased plants more susceptible to begomovirus infection, whereas overexpression of AtWWP1 enhanced plant resistance to begomovirus. Furthermore, we found that a mutant version of AtWWP1 defective for NB formation was no longer capable of interacting with and relocating NIG to the nucleus and lost its immune function against begomovirus. The antiviral function of AtWWP1-NBs, however, could be antagonized by viral infection that induced either the disruption or a decrease in the number of AtWWP1-NBs. Collectively, these results led us to propose that AtWWP1 organizes nuclear structures into nuclear foci, which provide intrinsic immunity against begomovirus infection.
publishDate 2018
dc.date.issued.fl_str_mv 2018-12-03
dc.date.accessioned.fl_str_mv 2019-04-04T17:38:08Z
dc.date.available.fl_str_mv 2019-04-04T17:38:08Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv https://doi.org/10.1016/j.molp.2018.09.009
http://www.locus.ufv.br/handle/123456789/24307
dc.identifier.issn.none.fl_str_mv 1674-2052
identifier_str_mv 1674-2052
url https://doi.org/10.1016/j.molp.2018.09.009
http://www.locus.ufv.br/handle/123456789/24307
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartofseries.pt-BR.fl_str_mv Volume 11, Issue 12, Pages 1449-1465, December 2018
dc.rights.driver.fl_str_mv Elsevier B. V.
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Elsevier B. V.
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Molecular Plant
publisher.none.fl_str_mv Molecular Plant
dc.source.none.fl_str_mv reponame:LOCUS Repositório Institucional da UFV
instname:Universidade Federal de Viçosa (UFV)
instacron:UFV
instname_str Universidade Federal de Viçosa (UFV)
instacron_str UFV
institution UFV
reponame_str LOCUS Repositório Institucional da UFV
collection LOCUS Repositório Institucional da UFV
bitstream.url.fl_str_mv https://locus.ufv.br//bitstream/123456789/24307/1/artigo.pdf
https://locus.ufv.br//bitstream/123456789/24307/2/license.txt
bitstream.checksum.fl_str_mv 1a90e6a7130ff20cea65f3af95d095c4
8a4605be74aa9ea9d79846c1fba20a33
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
repository.name.fl_str_mv LOCUS Repositório Institucional da UFV - Universidade Federal de Viçosa (UFV)
repository.mail.fl_str_mv fabiojreis@ufv.br
_version_ 1801212986520502272