Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites

Geminiviruses are DNA viruses that replicate in nuclei of infected plant cells using the plant DNA replication machinery, including PCNA (proliferating cellular nuclear antigen), a cofactor that orchestrates genome duplication and maintenance by recruiting crucial players to replication forks. These...

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Autores: Arroyo-Mateos, Manuel, Sabarit, Blanca, Maio, Francesca, Sánchez-Durán, Miguel A, Rosas-Díaz, Tabata, Prins, Marcel, Ruiz-Albert, Javier, Luna, Ana P, van den Burg, Harrold A, Bejarano, Eduardo R
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2018
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/345655
Acceso en línea:http://hdl.handle.net/10261/345655
https://api.elsevier.com/content/abstract/scopus_id/85053295453
Access Level:acceso abierto
Palabra clave:PCNA
sumoylation
geminivirus
homologous recombination
begomovirus
SUMO
Rep
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spelling Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor SitesArroyo-Mateos, ManuelSabarit, BlancaMaio, FrancescaSánchez-Durán, Miguel ARosas-Díaz, TabataPrins, MarcelRuiz-Albert, JavierLuna, Ana Pvan den Burg, Harrold ABejarano, Eduardo RPCNAsumoylationgeminivirushomologous recombinationbegomovirusSUMORepGeminiviruses are DNA viruses that replicate in nuclei of infected plant cells using the plant DNA replication machinery, including PCNA (proliferating cellular nuclear antigen), a cofactor that orchestrates genome duplication and maintenance by recruiting crucial players to replication forks. These viruses encode a multifunctional protein, Rep, which is essential for viral replication, induces the accumulation of the host replication machinery, and interacts with several host proteins, including PCNA and the SUMO E2 conjugation enzyme (SCE1). Posttranslational modification of PCNA by ubiquitin or SUMO plays an essential role in the switching of PCNA between interacting partners during DNA metabolism processes (e.g., replication, recombination, and repair, etc.). In yeast, PCNA sumoylation has been associated with DNA repair involving homologous recombination (HR). Previously, we reported that ectopic Rep expression results in very specific changes in the sumoylation pattern of plant cells. In this work, we show, using a reconstituted sumoylation system in Escherichia coli, that tomato PCNA is sumoylated at two residues, K254 and K164, and that coexpression of the geminivirus protein Rep suppresses sumoylation at these lysines. Finally, we confirm that PCNA is sumoylated in planta and that Rep also interferes with PCNA sumoylation in plant cells.IMPORTANCE SUMO adducts have a key role in regulating the activity of animal and yeast PCNA on DNA repair and replication. Our work demonstrates for the first time that sumoylation of plant PCNA occurs in plant cells and that a plant virus interferes with this modification. This work marks the importance of sumoylation in allowing viral infection and replication in plants. Moreover, it constitutes a prime example of how viral proteins interfere with posttranslational modifications of selected host factors to create a proper environment for infection.This research was supported by a grant from the Spanish Ministerio de Ciencia y Tecnología (AGL2016-75819-C2-1-R). M.A.S.-D. was awarded a predoctoral fellowship from the Junta de Andalucía and an EMBO short-term fellowship (ASTF no. 240-05). B.S. was awarded a predoctoral fellowship from the Spanish Ministerio de Educación y Cultura. The Topsector T&U program Better Plants for Demands (grant 1409-036 to H.A.V.D.B.), including the partnering breeding companies, supported this work. F.M. is financially supported by Keygene NV (The Netherlands)Peer reviewedAmerican Society for MicrobiologyMinisterio de Ciencia y Tecnología (España)0000-0002-4806-253XConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242018info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionapplication/pdfhttp://hdl.handle.net/10261/345655https://api.elsevier.com/content/abstract/scopus_id/85053295453reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésJournal of virologyhttps://journals.asm.org/doi/10.1128/jvi.00611-18Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3456552026-05-22T06:33:51Z
dc.title.none.fl_str_mv Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
title Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
spellingShingle Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
Arroyo-Mateos, Manuel
PCNA
sumoylation
geminivirus
homologous recombination
begomovirus
SUMO
Rep
title_short Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
title_full Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
title_fullStr Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
title_full_unstemmed Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
title_sort Geminivirus Replication Protein Impairs SUMO Conjugation of Proliferating Cellular Nuclear Antigen at Two Acceptor Sites
dc.creator.none.fl_str_mv Arroyo-Mateos, Manuel
Sabarit, Blanca
Maio, Francesca
Sánchez-Durán, Miguel A
Rosas-Díaz, Tabata
Prins, Marcel
Ruiz-Albert, Javier
Luna, Ana P
van den Burg, Harrold A
Bejarano, Eduardo R
author Arroyo-Mateos, Manuel
author_facet Arroyo-Mateos, Manuel
Sabarit, Blanca
Maio, Francesca
Sánchez-Durán, Miguel A
Rosas-Díaz, Tabata
Prins, Marcel
Ruiz-Albert, Javier
Luna, Ana P
van den Burg, Harrold A
Bejarano, Eduardo R
author_role author
author2 Sabarit, Blanca
Maio, Francesca
Sánchez-Durán, Miguel A
Rosas-Díaz, Tabata
Prins, Marcel
Ruiz-Albert, Javier
Luna, Ana P
van den Burg, Harrold A
Bejarano, Eduardo R
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia y Tecnología (España)
0000-0002-4806-253X
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv PCNA
sumoylation
geminivirus
homologous recombination
begomovirus
SUMO
Rep
topic PCNA
sumoylation
geminivirus
homologous recombination
begomovirus
SUMO
Rep
description Geminiviruses are DNA viruses that replicate in nuclei of infected plant cells using the plant DNA replication machinery, including PCNA (proliferating cellular nuclear antigen), a cofactor that orchestrates genome duplication and maintenance by recruiting crucial players to replication forks. These viruses encode a multifunctional protein, Rep, which is essential for viral replication, induces the accumulation of the host replication machinery, and interacts with several host proteins, including PCNA and the SUMO E2 conjugation enzyme (SCE1). Posttranslational modification of PCNA by ubiquitin or SUMO plays an essential role in the switching of PCNA between interacting partners during DNA metabolism processes (e.g., replication, recombination, and repair, etc.). In yeast, PCNA sumoylation has been associated with DNA repair involving homologous recombination (HR). Previously, we reported that ectopic Rep expression results in very specific changes in the sumoylation pattern of plant cells. In this work, we show, using a reconstituted sumoylation system in Escherichia coli, that tomato PCNA is sumoylated at two residues, K254 and K164, and that coexpression of the geminivirus protein Rep suppresses sumoylation at these lysines. Finally, we confirm that PCNA is sumoylated in planta and that Rep also interferes with PCNA sumoylation in plant cells.IMPORTANCE SUMO adducts have a key role in regulating the activity of animal and yeast PCNA on DNA repair and replication. Our work demonstrates for the first time that sumoylation of plant PCNA occurs in plant cells and that a plant virus interferes with this modification. This work marks the importance of sumoylation in allowing viral infection and replication in plants. Moreover, it constitutes a prime example of how viral proteins interfere with posttranslational modifications of selected host factors to create a proper environment for infection.
publishDate 2018
dc.date.none.fl_str_mv 2018
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/345655
https://api.elsevier.com/content/abstract/scopus_id/85053295453
url http://hdl.handle.net/10261/345655
https://api.elsevier.com/content/abstract/scopus_id/85053295453
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Journal of virology
https://journals.asm.org/doi/10.1128/jvi.00611-18
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.811543

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