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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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. |
doi_str_mv | 10.1007/s00299-024-03354-0 |
format | Article |
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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.</description><identifier>ISSN: 0721-7714</identifier><identifier>ISSN: 1432-203X</identifier><identifier>EISSN: 1432-203X</identifier><identifier>DOI: 10.1007/s00299-024-03354-0</identifier><identifier>PMID: 39422819</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>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</subject><ispartof>Plant cell reports, 2024-11, Vol.43 (11), p.266, Article 266</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2024 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c356t-8f18ddb7846a19dbc29c46beab09bbe5c35bb2ea471ec74dac9d9ae107ca439e3</cites><orcidid>0000-0003-3762-5445</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00299-024-03354-0$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00299-024-03354-0$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,27922,27923,41486,42555,51317</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39422819$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Yen-Ching</creatorcontrib><creatorcontrib>Hsieh, Wei-Hsun</creatorcontrib><creatorcontrib>Lin, Liang-Peng</creatorcontrib><creatorcontrib>He, Meng-Hsun</creatorcontrib><creatorcontrib>Jhan, Ya-Ting</creatorcontrib><creatorcontrib>Huang, Chu-Jun</creatorcontrib><creatorcontrib>Zhan, Junpeng</creatorcontrib><creatorcontrib>Chang, Ching-Chun</creatorcontrib><creatorcontrib>Hsieh, Tzung-Fu</creatorcontrib><creatorcontrib>Lin, Jer-Young</creatorcontrib><title>Dissecting the temporal genetic networks programming soybean embryo development from embryonic morphogenesis to post-germination</title><title>Plant cell reports</title><addtitle>Plant Cell Rep</addtitle><addtitle>Plant Cell Rep</addtitle><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.</description><subject>Accumulation</subject><subject>Arabidopsis</subject><subject>Arabidopsis - embryology</subject><subject>Arabidopsis - genetics</subject><subject>Biological activity</subject><subject>Biomedical and Life Sciences</subject><subject>Biotechnology</subject><subject>Cell Biology</subject><subject>Chromatin remodeling</subject><subject>Desiccation</subject><subject>Developmental stages</subject><subject>DNA methylation</subject><subject>Embryogenesis</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Epigenetics</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene regulation</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Germination</subject><subject>Germination - genetics</subject><subject>Glycine max - embryology</subject><subject>Glycine max - genetics</subject><subject>Histones</subject><subject>Information processing</subject><subject>Life Sciences</subject><subject>Modules</subject><subject>Morphogenesis</subject><subject>Morphogenesis - genetics</subject><subject>Network analysis</subject><subject>Original</subject><subject>Original Article</subject><subject>Plant Biochemistry</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Sciences</subject><subject>Seeds - genetics</subject><subject>Seeds - growth & development</subject><subject>Soybeans</subject><subject>Stress functions</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcriptome - genetics</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><issn>0721-7714</issn><issn>1432-203X</issn><issn>1432-203X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNp9kUuPFCEUhYnROG3rH3BhSNy4KeVVRbEyZsZRk0ncaOKOAHW7usYCSqDH9M6fPrTdjo-Fm0vC-e7hXg5CTyl5SQmRrzIhTKmGMNEQztta76EVFZw1jPAv99GKSEYbKak4Q49yviakirJ7iM64Eoz1VK3Qj4spZ3BlCiMuW8AF_BKTmfEIAcrkcK3fY_qa8ZLimIz3BzLHvQUTMHib9hEPcANzXDyEgjcp-tN9qO0-pmUbD2Z5yrhEvMRcmhFS9TFliuExerAxc4Ynp3ONPl--_XT-vrn6-O7D-ZurxvG2K02_of0wWNmLzlA1WMeUE10dwhJlLbSVspaBEZKCk2IwTg3KACXSGcEV8DV6ffRddtbD4OqsdU29pMmbtNfRTPpvJUxbPcYbTanoFVNddXhxckjx2w5y0X7KDubZBIi7rDmlUqlOtrSiz_9Br-Muhbrfgeop5aJllWJHyqWYc4LN3TSU6EPC-piwrgnrnwnXukbP_tzjruVXpBXgRyBXKdSf_v32f2xvARhat1o</recordid><startdate>20241101</startdate><enddate>20241101</enddate><creator>Wang, Yen-Ching</creator><creator>Hsieh, Wei-Hsun</creator><creator>Lin, Liang-Peng</creator><creator>He, Meng-Hsun</creator><creator>Jhan, Ya-Ting</creator><creator>Huang, Chu-Jun</creator><creator>Zhan, Junpeng</creator><creator>Chang, Ching-Chun</creator><creator>Hsieh, Tzung-Fu</creator><creator>Lin, Jer-Young</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T5</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3762-5445</orcidid></search><sort><creationdate>20241101</creationdate><title>Dissecting the temporal genetic networks programming soybean embryo development from embryonic morphogenesis to post-germination</title><author>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</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 & development</topic><topic>Soybeans</topic><topic>Stress functions</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Transcriptome - genetics</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Yen-Ching</creatorcontrib><creatorcontrib>Hsieh, Wei-Hsun</creatorcontrib><creatorcontrib>Lin, Liang-Peng</creatorcontrib><creatorcontrib>He, Meng-Hsun</creatorcontrib><creatorcontrib>Jhan, Ya-Ting</creatorcontrib><creatorcontrib>Huang, Chu-Jun</creatorcontrib><creatorcontrib>Zhan, Junpeng</creatorcontrib><creatorcontrib>Chang, Ching-Chun</creatorcontrib><creatorcontrib>Hsieh, Tzung-Fu</creatorcontrib><creatorcontrib>Lin, Jer-Young</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant cell reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Yen-Ching</au><au>Hsieh, Wei-Hsun</au><au>Lin, Liang-Peng</au><au>He, Meng-Hsun</au><au>Jhan, Ya-Ting</au><au>Huang, Chu-Jun</au><au>Zhan, Junpeng</au><au>Chang, Ching-Chun</au><au>Hsieh, Tzung-Fu</au><au>Lin, Jer-Young</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dissecting the temporal genetic networks programming soybean embryo development from embryonic morphogenesis to post-germination</atitle><jtitle>Plant cell reports</jtitle><stitle>Plant Cell Rep</stitle><addtitle>Plant Cell Rep</addtitle><date>2024-11-01</date><risdate>2024</risdate><volume>43</volume><issue>11</issue><spage>266</spage><pages>266-</pages><artnum>266</artnum><issn>0721-7714</issn><issn>1432-203X</issn><eissn>1432-203X</eissn><abstract>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.</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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