Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development
Autor(a) principal: | |
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Data de Publicação: | 2018 |
Outros Autores: | , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/1822/73140 |
Resumo: | Post-translational modifiers such as the small ubiquitin-like modifier (SUMO) peptide act as fast and reversible protein regulators. Functional characterization of the sumoylation machinery has determined the key regulatory role that SUMO plays in plant development. Unlike components of the SUMO conjugation pathway, SUMO proteases (ULPs) are encoded by a relatively large gene family and are potential sources of specificity within the pathway. This study reports a thorough comparative genomics and phylogenetic characterization of plant ULPs, revealing the presence of one ULP1-like and three ULP2-like SUMO protease subgroups within plant genomes. As representatives of an under-studied subgroup, Arabidopsis SPF1 and SPF2 were subjected to functional characterization. Loss-of-function mutants implicated both proteins with vegetative growth, flowering time, and seed size and yield. Mutants constitutively accumulated SUMO conjugates, and yeast complementation assays associated these proteins with the function of ScUlp2 but not ScUlp1. Fluorescence imaging placed both proteins in the plant cell nucleoplasm. Transcriptomics analysis indicated strong regulatory involvement in secondary metabolism, cell wall remodelling, and nitrate assimilation. Furthermore, developmental defects of the spf1-1 spf2-2 (spf1/2) double-mutant opposed those of the major E3 ligase siz1 mutant and, most significantly, developmental and transcriptomic characterization of the siz1 spf1/2 triple-mutant placed SIZ1 as epistatic to SPF1 and SPF2. |
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Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant developmentPlant developmentPTMSIZ1sumoylationSUMO proteasestranscriptomeULP2Ciências Naturais::Ciências BiológicasScience & TechnologyPost-translational modifiers such as the small ubiquitin-like modifier (SUMO) peptide act as fast and reversible protein regulators. Functional characterization of the sumoylation machinery has determined the key regulatory role that SUMO plays in plant development. Unlike components of the SUMO conjugation pathway, SUMO proteases (ULPs) are encoded by a relatively large gene family and are potential sources of specificity within the pathway. This study reports a thorough comparative genomics and phylogenetic characterization of plant ULPs, revealing the presence of one ULP1-like and three ULP2-like SUMO protease subgroups within plant genomes. As representatives of an under-studied subgroup, Arabidopsis SPF1 and SPF2 were subjected to functional characterization. Loss-of-function mutants implicated both proteins with vegetative growth, flowering time, and seed size and yield. Mutants constitutively accumulated SUMO conjugates, and yeast complementation assays associated these proteins with the function of ScUlp2 but not ScUlp1. Fluorescence imaging placed both proteins in the plant cell nucleoplasm. Transcriptomics analysis indicated strong regulatory involvement in secondary metabolism, cell wall remodelling, and nitrate assimilation. Furthermore, developmental defects of the spf1-1 spf2-2 (spf1/2) double-mutant opposed those of the major E3 ligase siz1 mutant and, most significantly, developmental and transcriptomic characterization of the siz1 spf1/2 triple-mutant placed SIZ1 as epistatic to SPF1 and SPF2.We thank Mark Hochstrasser (Department of Molecular Biophysics & Biochemistry, Yale University, New Haven, CT, USA) for kindly providing the ulp1-ts yeast mutant strain. This research was funded by FEDER (through COMPETE), and by Fundacao para a Ciencia e Tecnologia (FCT), within the scope of project SUMOdulator (FCOMP-01-0124-FEDER-028459 and PTDC/BIA-PLA/3850/2012). PHC was supported by FCT (SFRH/BD/44484/2008). HA and FF were supported by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (FEDER) (NORTE-01-0145-FEDER-000007 and Norte-01-0145-FEDER-000008, respectively). The work was supported by FEDER through the COMPETE 2020-Operacional Programme for Competitiveness and Internationalisation (POCI), Portugal 2020, and by Portuguese funds through FCT, within the framework of projects 'Rede de Investigacao em Biodiversidade e Biologia Evolutiva' (POCI-01-0145-FEDER-006821) and 'Institute for Research and Innovation in Health Sciences' (POCI-01-0145-FEDER-007274). This research was also supported by a grant from the Spanish Ministerio de Ciencia y Tecnologia (AGL2016-75819-C2-1-R) and FEDER (PCQ, AGC, ERB).Oxford University PressUniversidade do MinhoHumberto Castro, PedroSantos, Miguel AngeloFreitas, SaraCana-Quijada, PepeLourenco, TiagoRodrigues, Mafalda A. A.Fonseca, FatimaRuiz-Albert, JavierAzevedo, Jorge E.Tavares, R. M.Castillo, Araceli G.Bejarano, Eduardo R.Azevedo, Herlander20182018-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/1822/73140engPedro Humberto Castro, Miguel Ângelo Santos, Sara Freitas, Pepe Cana-Quijada, Tiago Lourenço, Mafalda A A Rodrigues, Fátima Fonseca, Javier Ruiz-Albert, Jorge E Azevedo, Rui Manuel Tavares, Araceli G Castillo, Eduardo R Bejarano, Herlander Azevedo, Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development, Journal of Experimental Botany, Volume 69, Issue 19, 31 August 2018, Pages 4633–4649, https://doi.org/10.1093/jxb/ery2650022-09571460-243110.1093/jxb/ery26530053161https://academic.oup.com/jxb/article/69/19/4633/5058961info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-21T12:01:40Zoai:repositorium.sdum.uminho.pt:1822/73140Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T18:51:36.171931Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
title |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
spellingShingle |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development Humberto Castro, Pedro Plant development PTM SIZ1 sumoylation SUMO proteases transcriptome ULP2 Ciências Naturais::Ciências Biológicas Science & Technology |
title_short |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
title_full |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
title_fullStr |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
title_full_unstemmed |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
title_sort |
Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development |
author |
Humberto Castro, Pedro |
author_facet |
Humberto Castro, Pedro Santos, Miguel Angelo Freitas, Sara Cana-Quijada, Pepe Lourenco, Tiago Rodrigues, Mafalda A. A. Fonseca, Fatima Ruiz-Albert, Javier Azevedo, Jorge E. Tavares, R. M. Castillo, Araceli G. Bejarano, Eduardo R. Azevedo, Herlander |
author_role |
author |
author2 |
Santos, Miguel Angelo Freitas, Sara Cana-Quijada, Pepe Lourenco, Tiago Rodrigues, Mafalda A. A. Fonseca, Fatima Ruiz-Albert, Javier Azevedo, Jorge E. Tavares, R. M. Castillo, Araceli G. Bejarano, Eduardo R. Azevedo, Herlander |
author2_role |
author author author author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade do Minho |
dc.contributor.author.fl_str_mv |
Humberto Castro, Pedro Santos, Miguel Angelo Freitas, Sara Cana-Quijada, Pepe Lourenco, Tiago Rodrigues, Mafalda A. A. Fonseca, Fatima Ruiz-Albert, Javier Azevedo, Jorge E. Tavares, R. M. Castillo, Araceli G. Bejarano, Eduardo R. Azevedo, Herlander |
dc.subject.por.fl_str_mv |
Plant development PTM SIZ1 sumoylation SUMO proteases transcriptome ULP2 Ciências Naturais::Ciências Biológicas Science & Technology |
topic |
Plant development PTM SIZ1 sumoylation SUMO proteases transcriptome ULP2 Ciências Naturais::Ciências Biológicas Science & Technology |
description |
Post-translational modifiers such as the small ubiquitin-like modifier (SUMO) peptide act as fast and reversible protein regulators. Functional characterization of the sumoylation machinery has determined the key regulatory role that SUMO plays in plant development. Unlike components of the SUMO conjugation pathway, SUMO proteases (ULPs) are encoded by a relatively large gene family and are potential sources of specificity within the pathway. This study reports a thorough comparative genomics and phylogenetic characterization of plant ULPs, revealing the presence of one ULP1-like and three ULP2-like SUMO protease subgroups within plant genomes. As representatives of an under-studied subgroup, Arabidopsis SPF1 and SPF2 were subjected to functional characterization. Loss-of-function mutants implicated both proteins with vegetative growth, flowering time, and seed size and yield. Mutants constitutively accumulated SUMO conjugates, and yeast complementation assays associated these proteins with the function of ScUlp2 but not ScUlp1. Fluorescence imaging placed both proteins in the plant cell nucleoplasm. Transcriptomics analysis indicated strong regulatory involvement in secondary metabolism, cell wall remodelling, and nitrate assimilation. Furthermore, developmental defects of the spf1-1 spf2-2 (spf1/2) double-mutant opposed those of the major E3 ligase siz1 mutant and, most significantly, developmental and transcriptomic characterization of the siz1 spf1/2 triple-mutant placed SIZ1 as epistatic to SPF1 and SPF2. |
publishDate |
2018 |
dc.date.none.fl_str_mv |
2018 2018-01-01T00:00:00Z |
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 |
http://hdl.handle.net/1822/73140 |
url |
http://hdl.handle.net/1822/73140 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Pedro Humberto Castro, Miguel Ângelo Santos, Sara Freitas, Pepe Cana-Quijada, Tiago Lourenço, Mafalda A A Rodrigues, Fátima Fonseca, Javier Ruiz-Albert, Jorge E Azevedo, Rui Manuel Tavares, Araceli G Castillo, Eduardo R Bejarano, Herlander Azevedo, Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development, Journal of Experimental Botany, Volume 69, Issue 19, 31 August 2018, Pages 4633–4649, https://doi.org/10.1093/jxb/ery265 0022-0957 1460-2431 10.1093/jxb/ery265 30053161 https://academic.oup.com/jxb/article/69/19/4633/5058961 |
dc.rights.driver.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 |
Oxford University Press |
publisher.none.fl_str_mv |
Oxford University Press |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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