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

Autor: Robert C. Augustine, Masaharu Suzuki, Richard D. Vierstra, Juanjuan Feng, Si Nian Char, Junya Zhang, Donald R. McCarty, Bing Yang
Jazyk: angličtina
Rok vydání: 2021
Předmět:
Cancer Research
Fruit and Seed Anatomy
Cell division
Proteome
Transcription
Genetic
SUMO protein
Plant Science
QH426-470
Biochemistry
Transcriptome
Ligases
Gene expression
Genetics (clinical)
Plant Anatomy
Messenger RNA
Eukaryota
Plants
Chromatin
Cell biology
Nucleic acids
Experimental Organism Systems
Seeds
Post-translational modification
Genome
Plant
Research Article
DNA repair
Arabidopsis Thaliana
Ubiquitin-Protein Ligases
SUMO-1 Protein
Brassica
Biology
Research and Analysis Methods
Zea mays
Chromosomes
Plant
Genomic Instability
Model Organisms
Plant and Algal Models
Genetics
Endoreduplication
Grasses
Molecular Biology
Ecology
Evolution
Behavior and Systematics
Biology and life sciences
Arabidopsis Proteins
Organisms
Proteins
Sumoylation
DNA
Endosperm
Maize
Seedlings
Animal Studies
RNA
Ectopic expression
Zdroj: PLoS Genetics, Vol 17, Iss 10, p e1009830 (2021)
PLoS Genetics
PLoS Genetics, Vol 17, Iss 10 (2021)
ISSN: 1553-7404
1553-7390
Popis: 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.
Databáze: OpenAIRE
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