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...
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2021
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oai:doaj.org-article:6951897b4ab34774950a37ff21db7b802021-12-02T20:03:29ZThe SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability.1553-73901553-740410.1371/journal.pgen.1009830https://doaj.org/article/6951897b4ab34774950a37ff21db7b802021-10-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009830https://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.Junya ZhangRobert C AugustineMasaharu SuzukiJuanjuan FengSi Nian CharBing YangDonald R McCartyRichard D VierstraPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 10, p e1009830 (2021) |
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Genetics QH426-470 |
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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. |
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/6951897b4ab34774950a37ff21db7b80 |
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