Dissecting the temporal genetic networks programming soybean embryo development from embryonic morphogenesis to post-germination

Key message Desiccation-stage transcription factors perform similar functions, with early ones focused on desiccation tolerance and later ones on development. Gene networks governing late embryo development diverge between soybean and Arabidopsis . To understand gene activities programming seed embr...

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Veröffentlicht in:Plant cell reports 2024-11, Vol.43 (11), p.266, Article 266
Hauptverfasser: Wang, Yen-Ching, Hsieh, Wei-Hsun, Lin, Liang-Peng, He, Meng-Hsun, Jhan, Ya-Ting, Huang, Chu-Jun, Zhan, Junpeng, Chang, Ching-Chun, Hsieh, Tzung-Fu, Lin, Jer-Young
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container_title Plant cell reports
container_volume 43
creator Wang, Yen-Ching
Hsieh, Wei-Hsun
Lin, Liang-Peng
He, Meng-Hsun
Jhan, Ya-Ting
Huang, Chu-Jun
Zhan, Junpeng
Chang, Ching-Chun
Hsieh, Tzung-Fu
Lin, Jer-Young
description Key message Desiccation-stage transcription factors perform similar functions, with early ones focused on desiccation tolerance and later ones on development. Gene networks governing late embryo development diverge between soybean and Arabidopsis . To understand gene activities programming seed embryo development, we profiled the soybean embryo transcriptome across embryonic morphogenesis through post-germination. Transcriptomic landscapes across embryo development feature highly prevalent transcripts, categorized into early and late groups, with shared and distinct functions. During the mid-storage reserve accumulation stage, the upregulated genes are enriched with regulatory tasks at both the transcriptional and chromatin levels, including DNA methylation and chromatin remodeling. The epigenetic-related functions also dominate in the upregulated genes during germination, involving core histone variants and histone chaperones. Gene network analysis reveals both stage-specific modules and modules active across multiple stages. The desiccation-associated gene module integrates diverse transcription factors (TFs) that are sequentially active during different desiccation stages, transitioning from abiotic stress functions early on to developmental functions later. Two TFs, active during the early and mid-desiccation stages were functionally assessed in Arabidopsis overexpression lines to uncover their potential roles in desiccation processes. Interestingly, nearly half of the Arabidopsis orthologs of soybean TFs active in the desiccation-associated module are inactive during Arabidopsis desiccation. Our results reveal that chromatin and transcriptional regulation coordinate during mid-storage reserve accumulation, while distinct epigenetic mechanisms drive germination. Additionally, gene modules either perform stage-specific functions or are required across multiple stages, and gene networks during late embryogenesis diverge between soybean and Arabidopsis . Our studies provide new information on the biological processes and gene networks underlying development from embryonic morphogenesis to post-germination.
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Gene networks governing late embryo development diverge between soybean and Arabidopsis . To understand gene activities programming seed embryo development, we profiled the soybean embryo transcriptome across embryonic morphogenesis through post-germination. Transcriptomic landscapes across embryo development feature highly prevalent transcripts, categorized into early and late groups, with shared and distinct functions. During the mid-storage reserve accumulation stage, the upregulated genes are enriched with regulatory tasks at both the transcriptional and chromatin levels, including DNA methylation and chromatin remodeling. The epigenetic-related functions also dominate in the upregulated genes during germination, involving core histone variants and histone chaperones. Gene network analysis reveals both stage-specific modules and modules active across multiple stages. The desiccation-associated gene module integrates diverse transcription factors (TFs) that are sequentially active during different desiccation stages, transitioning from abiotic stress functions early on to developmental functions later. Two TFs, active during the early and mid-desiccation stages were functionally assessed in Arabidopsis overexpression lines to uncover their potential roles in desiccation processes. Interestingly, nearly half of the Arabidopsis orthologs of soybean TFs active in the desiccation-associated module are inactive during Arabidopsis desiccation. Our results reveal that chromatin and transcriptional regulation coordinate during mid-storage reserve accumulation, while distinct epigenetic mechanisms drive germination. Additionally, gene modules either perform stage-specific functions or are required across multiple stages, and gene networks during late embryogenesis diverge between soybean and Arabidopsis . 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Gene networks governing late embryo development diverge between soybean and Arabidopsis . To understand gene activities programming seed embryo development, we profiled the soybean embryo transcriptome across embryonic morphogenesis through post-germination. Transcriptomic landscapes across embryo development feature highly prevalent transcripts, categorized into early and late groups, with shared and distinct functions. During the mid-storage reserve accumulation stage, the upregulated genes are enriched with regulatory tasks at both the transcriptional and chromatin levels, including DNA methylation and chromatin remodeling. The epigenetic-related functions also dominate in the upregulated genes during germination, involving core histone variants and histone chaperones. Gene network analysis reveals both stage-specific modules and modules active across multiple stages. The desiccation-associated gene module integrates diverse transcription factors (TFs) that are sequentially active during different desiccation stages, transitioning from abiotic stress functions early on to developmental functions later. Two TFs, active during the early and mid-desiccation stages were functionally assessed in Arabidopsis overexpression lines to uncover their potential roles in desiccation processes. Interestingly, nearly half of the Arabidopsis orthologs of soybean TFs active in the desiccation-associated module are inactive during Arabidopsis desiccation. Our results reveal that chromatin and transcriptional regulation coordinate during mid-storage reserve accumulation, while distinct epigenetic mechanisms drive germination. Additionally, gene modules either perform stage-specific functions or are required across multiple stages, and gene networks during late embryogenesis diverge between soybean and Arabidopsis . 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Hsieh, Wei-Hsun ; Lin, Liang-Peng ; He, Meng-Hsun ; Jhan, Ya-Ting ; Huang, Chu-Jun ; Zhan, Junpeng ; Chang, Ching-Chun ; Hsieh, Tzung-Fu ; Lin, Jer-Young</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c356t-8f18ddb7846a19dbc29c46beab09bbe5c35bb2ea471ec74dac9d9ae107ca439e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Accumulation</topic><topic>Arabidopsis</topic><topic>Arabidopsis - embryology</topic><topic>Arabidopsis - genetics</topic><topic>Biological activity</topic><topic>Biomedical and Life Sciences</topic><topic>Biotechnology</topic><topic>Cell Biology</topic><topic>Chromatin remodeling</topic><topic>Desiccation</topic><topic>Developmental stages</topic><topic>DNA methylation</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Embryos</topic><topic>Epigenetics</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene regulation</topic><topic>Gene Regulatory Networks</topic><topic>Genes</topic><topic>Germination</topic><topic>Germination - genetics</topic><topic>Glycine max - embryology</topic><topic>Glycine max - genetics</topic><topic>Histones</topic><topic>Information processing</topic><topic>Life Sciences</topic><topic>Modules</topic><topic>Morphogenesis</topic><topic>Morphogenesis - genetics</topic><topic>Network analysis</topic><topic>Original</topic><topic>Original Article</topic><topic>Plant Biochemistry</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Sciences</topic><topic>Seeds - genetics</topic><topic>Seeds - growth &amp; 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Gene networks governing late embryo development diverge between soybean and Arabidopsis . To understand gene activities programming seed embryo development, we profiled the soybean embryo transcriptome across embryonic morphogenesis through post-germination. Transcriptomic landscapes across embryo development feature highly prevalent transcripts, categorized into early and late groups, with shared and distinct functions. During the mid-storage reserve accumulation stage, the upregulated genes are enriched with regulatory tasks at both the transcriptional and chromatin levels, including DNA methylation and chromatin remodeling. The epigenetic-related functions also dominate in the upregulated genes during germination, involving core histone variants and histone chaperones. Gene network analysis reveals both stage-specific modules and modules active across multiple stages. The desiccation-associated gene module integrates diverse transcription factors (TFs) that are sequentially active during different desiccation stages, transitioning from abiotic stress functions early on to developmental functions later. Two TFs, active during the early and mid-desiccation stages were functionally assessed in Arabidopsis overexpression lines to uncover their potential roles in desiccation processes. Interestingly, nearly half of the Arabidopsis orthologs of soybean TFs active in the desiccation-associated module are inactive during Arabidopsis desiccation. Our results reveal that chromatin and transcriptional regulation coordinate during mid-storage reserve accumulation, while distinct epigenetic mechanisms drive germination. Additionally, gene modules either perform stage-specific functions or are required across multiple stages, and gene networks during late embryogenesis diverge between soybean and Arabidopsis . Our studies provide new information on the biological processes and gene networks underlying development from embryonic morphogenesis to post-germination.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>39422819</pmid><doi>10.1007/s00299-024-03354-0</doi><orcidid>https://orcid.org/0000-0003-3762-5445</orcidid><oa>free_for_read</oa></addata></record>
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subjects Accumulation
Arabidopsis
Arabidopsis - embryology
Arabidopsis - genetics
Biological activity
Biomedical and Life Sciences
Biotechnology
Cell Biology
Chromatin remodeling
Desiccation
Developmental stages
DNA methylation
Embryogenesis
Embryonic growth stage
Embryos
Epigenetics
Gene Expression Profiling
Gene Expression Regulation, Developmental
Gene Expression Regulation, Plant
Gene regulation
Gene Regulatory Networks
Genes
Germination
Germination - genetics
Glycine max - embryology
Glycine max - genetics
Histones
Information processing
Life Sciences
Modules
Morphogenesis
Morphogenesis - genetics
Network analysis
Original
Original Article
Plant Biochemistry
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Sciences
Seeds - genetics
Seeds - growth & development
Soybeans
Stress functions
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Transcriptome - genetics
Transcriptomes
Transcriptomics
title Dissecting the temporal genetic networks programming soybean embryo development from embryonic morphogenesis to post-germination
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