The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability

The post-translational addition of SUMO plays essential roles in numerous eukaryotic processes including cell division, transcription, chromatin organization, DNA repair, and stress defense through its selective conjugation to numerous targets. One prominent plant SUMO ligase is METHYL METHANESULFON...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Junya Zhang, Robert C. Augustine, Masaharu Suzuki, Juanjuan Feng, Si Nian Char, Bing Yang, Donald R. McCarty, Richard D. Vierstra
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2021
Materias:
Acceso en línea:https://doaj.org/article/15d0429b6f1e4b57affa4ca76f9c0656
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:15d0429b6f1e4b57affa4ca76f9c0656
record_format dspace
spelling oai:doaj.org-article:15d0429b6f1e4b57affa4ca76f9c06562021-11-11T06:16:25ZThe SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability1553-73901553-7404https://doaj.org/article/15d0429b6f1e4b57affa4ca76f9c06562021-10-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8568144/?tool=EBIhttps://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404The post-translational addition of SUMO plays essential roles in numerous eukaryotic processes including cell division, transcription, chromatin organization, DNA repair, and stress defense through its selective conjugation to numerous targets. One prominent plant SUMO ligase is METHYL METHANESULFONATE-SENSITIVE (MMS)-21/HIGH-PLOIDY (HPY)-2/NON-SMC-ELEMENT (NSE)-2, which has been connected genetically to development and endoreduplication. Here, we describe the potential functions of MMS21 through a collection of UniformMu and CRISPR/Cas9 mutants in maize (Zea mays) that display either seed lethality or substantially compromised pollen germination and seed/vegetative development. RNA-seq analyses of leaves, embryos, and endosperm from mms21 plants revealed a substantial dysregulation of the maize transcriptome, including the ectopic expression of seed storage protein mRNAs in leaves and altered accumulation of mRNAs associated with DNA repair and chromatin dynamics. Interaction studies demonstrated that MMS21 associates in the nucleus with the NSE4 and STRUCTURAL MAINTENANCE OF CHROMOSOMES (SMC)-5 components of the chromatin organizer SMC5/6 complex, with in vitro assays confirming that MMS21 will SUMOylate SMC5. Comet assays measuring genome integrity, sensitivity to DNA-damaging agents, and protein versus mRNA abundance comparisons implicated MMS21 in chromatin stability and transcriptional controls on proteome balance. Taken together, we propose that MMS21-directed SUMOylation of the SMC5/6 complex and other targets enables proper gene expression by influencing chromatin structure. Author summary The post-translational addition of SUMO to other proteins by the MMS21 SUMO ligase has been implicated in a plethora of biological processes in plants but the identit(ies) of its targets and the biological consequences of their modification remain poorly resolved. Here, we address this issue by characterizing a collection of maize mms21 mutants using genetic, biochemical, transcriptomic and proteomic approaches. Our results revealed that mms21 mutations substantially compromise pollen germination and seed/vegetative development, dysregulate the maize transcriptome, including the ectopic expression of seed storage protein mRNAs in leaves, increase DNA damage, and alter the proteome/transcriptome balance. Interaction studies showed that MMS21 associates in the nucleus with the NON-SMC-ELEMENT (NSE)-4 and STRUCTURAL MAINTENANCE OF CHROMOSOMES (SMC)-5 components of the chromatin organizer SMC5/6 complex responsible for DNA-damage repair and chromatin accessibility. Our data demonstrate that MMS21 is crucial for plant development likely through its maintenance of DNA repair, balanced transcription, and genome stability.Junya ZhangRobert C. AugustineMasaharu SuzukiJuanjuan FengSi Nian CharBing YangDonald R. McCartyRichard D. VierstraPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Junya Zhang
Robert C. Augustine
Masaharu Suzuki
Juanjuan Feng
Si Nian Char
Bing Yang
Donald R. McCarty
Richard D. Vierstra
The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability
description The post-translational addition of SUMO plays essential roles in numerous eukaryotic processes including cell division, transcription, chromatin organization, DNA repair, and stress defense through its selective conjugation to numerous targets. One prominent plant SUMO ligase is METHYL METHANESULFONATE-SENSITIVE (MMS)-21/HIGH-PLOIDY (HPY)-2/NON-SMC-ELEMENT (NSE)-2, which has been connected genetically to development and endoreduplication. Here, we describe the potential functions of MMS21 through a collection of UniformMu and CRISPR/Cas9 mutants in maize (Zea mays) that display either seed lethality or substantially compromised pollen germination and seed/vegetative development. RNA-seq analyses of leaves, embryos, and endosperm from mms21 plants revealed a substantial dysregulation of the maize transcriptome, including the ectopic expression of seed storage protein mRNAs in leaves and altered accumulation of mRNAs associated with DNA repair and chromatin dynamics. Interaction studies demonstrated that MMS21 associates in the nucleus with the NSE4 and STRUCTURAL MAINTENANCE OF CHROMOSOMES (SMC)-5 components of the chromatin organizer SMC5/6 complex, with in vitro assays confirming that MMS21 will SUMOylate SMC5. Comet assays measuring genome integrity, sensitivity to DNA-damaging agents, and protein versus mRNA abundance comparisons implicated MMS21 in chromatin stability and transcriptional controls on proteome balance. Taken together, we propose that MMS21-directed SUMOylation of the SMC5/6 complex and other targets enables proper gene expression by influencing chromatin structure. Author summary The post-translational addition of SUMO to other proteins by the MMS21 SUMO ligase has been implicated in a plethora of biological processes in plants but the identit(ies) of its targets and the biological consequences of their modification remain poorly resolved. Here, we address this issue by characterizing a collection of maize mms21 mutants using genetic, biochemical, transcriptomic and proteomic approaches. Our results revealed that mms21 mutations substantially compromise pollen germination and seed/vegetative development, dysregulate the maize transcriptome, including the ectopic expression of seed storage protein mRNAs in leaves, increase DNA damage, and alter the proteome/transcriptome balance. Interaction studies showed that MMS21 associates in the nucleus with the NON-SMC-ELEMENT (NSE)-4 and STRUCTURAL MAINTENANCE OF CHROMOSOMES (SMC)-5 components of the chromatin organizer SMC5/6 complex responsible for DNA-damage repair and chromatin accessibility. Our data demonstrate that MMS21 is crucial for plant development likely through its maintenance of DNA repair, balanced transcription, and genome stability.
format article
author Junya Zhang
Robert C. Augustine
Masaharu Suzuki
Juanjuan Feng
Si Nian Char
Bing Yang
Donald R. McCarty
Richard D. Vierstra
author_facet Junya Zhang
Robert C. Augustine
Masaharu Suzuki
Juanjuan Feng
Si Nian Char
Bing Yang
Donald R. McCarty
Richard D. Vierstra
author_sort Junya Zhang
title The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability
title_short The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability
title_full The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability
title_fullStr The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability
title_full_unstemmed The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability
title_sort sumo ligase mms21 profoundly influences maize development through its impact on genome activity and stability
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/15d0429b6f1e4b57affa4ca76f9c0656
work_keys_str_mv AT junyazhang thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT robertcaugustine thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT masaharusuzuki thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT juanjuanfeng thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT sinianchar thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT bingyang thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT donaldrmccarty thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT richarddvierstra thesumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT junyazhang sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT robertcaugustine sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT masaharusuzuki sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT juanjuanfeng sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT sinianchar sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT bingyang sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT donaldrmccarty sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
AT richarddvierstra sumoligasemms21profoundlyinfluencesmaizedevelopmentthroughitsimpactongenomeactivityandstability
_version_ 1718439467516166144