Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture
Shaping of root architecture is a quintessential developmental response that involves the concerted action of many different cell types, is highly dynamic, and underpins root plasticity. To determine to what extent the environmental regulation of lateral root development is a product of cell-type pr...
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Veröffentlicht in: | The Plant cell 2017-10, Vol.29 (10), p.2393-2412 |
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creator | Walker, Liam Boddington, Clare Jenkins, Dafyd Wang, Ying Grønlund, Jesper T. Hulsmans, Jo Kumar, Sanjeev Patel, Dhaval Moore, Jonathan D. Carter, Anthony Samavedam, Siva Bonomo, Giovanni Hersh, David S. Coruzzi, Gloria M. Burroughs, Nigel J. Gifford, Miriam L. |
description | Shaping of root architecture is a quintessential developmental response that involves the concerted action of many different cell types, is highly dynamic, and underpins root plasticity. To determine to what extent the environmental regulation of lateral root development is a product of cell-type preferential activities, we tracked transcriptomic responses to two different treatments that both change root development in Arabidopsis thaliana at an unprecedented level of temporal detail. We found that individual transcripts are expressed with a very high degree of temporal and spatial specificity, yet biological processes are commonly regulated, in a mechanism we term response nonredundancy. Using causative gene network inference to compare the genes regulated in different cell types and during responses to nitrogen and a biotic interaction, we found that common transcriptional modules often regulate the same gene families but control different individual members of these families, specific to response and cell type. This reinforces that the activity of a gene cannot be defined simply as molecular function; rather, it is a consequence of spatial location, expression timing, and environmental responsiveness. |
doi_str_mv | 10.1105/tpc.16.00961 |
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To determine to what extent the environmental regulation of lateral root development is a product of cell-type preferential activities, we tracked transcriptomic responses to two different treatments that both change root development in Arabidopsis thaliana at an unprecedented level of temporal detail. We found that individual transcripts are expressed with a very high degree of temporal and spatial specificity, yet biological processes are commonly regulated, in a mechanism we term response nonredundancy. Using causative gene network inference to compare the genes regulated in different cell types and during responses to nitrogen and a biotic interaction, we found that common transcriptional modules often regulate the same gene families but control different individual members of these families, specific to response and cell type. This reinforces that the activity of a gene cannot be defined simply as molecular function; rather, it is a consequence of spatial location, expression timing, and environmental responsiveness.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.16.00961</identifier><identifier>PMID: 28893852</identifier><language>eng</language><publisher>England: American Society of Plant Biologists</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Architecture ; Biological activity ; Environmental regulations ; Gene expression ; Gene Expression Regulation, Plant - genetics ; Gene families ; Large-Scale Biology ; LARGE-SCALE BIOLOGY ARTICLE ; Molecular modelling ; Plant Roots - genetics ; Plant Roots - metabolism ; Root development ; Transcription</subject><ispartof>The Plant cell, 2017-10, Vol.29 (10), p.2393-2412</ispartof><rights>2017 American Society of Plant Biologists</rights><rights>2017 American Society of Plant Biologists. All rights reserved.</rights><rights>Copyright American Society of Plant Biologists Oct 2017</rights><rights>2017 American Society of Plant Biologists. All rights reserved. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c500t-72395133ce8e244e9f5325f945834ab2f292bc1ae6a716b8e958359ce7ede3e93</citedby><orcidid>0000-0002-5486-0407 ; 0000-0002-4005-2513 ; 0000-0002-2099-0596 ; 0000-0003-0875-1936 ; 0000-0003-2608-2166 ; 0000-0003-0261-0518 ; 0000-0002-3561-8180</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90015794$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90015794$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28893852$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Walker, Liam</creatorcontrib><creatorcontrib>Boddington, Clare</creatorcontrib><creatorcontrib>Jenkins, Dafyd</creatorcontrib><creatorcontrib>Wang, Ying</creatorcontrib><creatorcontrib>Grønlund, Jesper T.</creatorcontrib><creatorcontrib>Hulsmans, Jo</creatorcontrib><creatorcontrib>Kumar, Sanjeev</creatorcontrib><creatorcontrib>Patel, Dhaval</creatorcontrib><creatorcontrib>Moore, Jonathan D.</creatorcontrib><creatorcontrib>Carter, Anthony</creatorcontrib><creatorcontrib>Samavedam, Siva</creatorcontrib><creatorcontrib>Bonomo, Giovanni</creatorcontrib><creatorcontrib>Hersh, David S.</creatorcontrib><creatorcontrib>Coruzzi, Gloria M.</creatorcontrib><creatorcontrib>Burroughs, Nigel J.</creatorcontrib><creatorcontrib>Gifford, Miriam L.</creatorcontrib><title>Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Shaping of root architecture is a quintessential developmental response that involves the concerted action of many different cell types, is highly dynamic, and underpins root plasticity. To determine to what extent the environmental regulation of lateral root development is a product of cell-type preferential activities, we tracked transcriptomic responses to two different treatments that both change root development in Arabidopsis thaliana at an unprecedented level of temporal detail. We found that individual transcripts are expressed with a very high degree of temporal and spatial specificity, yet biological processes are commonly regulated, in a mechanism we term response nonredundancy. Using causative gene network inference to compare the genes regulated in different cell types and during responses to nitrogen and a biotic interaction, we found that common transcriptional modules often regulate the same gene families but control different individual members of these families, specific to response and cell type. This reinforces that the activity of a gene cannot be defined simply as molecular function; rather, it is a consequence of spatial location, expression timing, and environmental responsiveness.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Architecture</subject><subject>Biological activity</subject><subject>Environmental regulations</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene families</subject><subject>Large-Scale Biology</subject><subject>LARGE-SCALE BIOLOGY ARTICLE</subject><subject>Molecular modelling</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - metabolism</subject><subject>Root development</subject><subject>Transcription</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc9rFDEcxYMotlZvXpWAFw-dNT8mk8lFKEtthUrBVvAWspnv7GaZScYkU-x_b9ptF9tTwvd98vi-PITeU7KglIgvebIL2iwIUQ19gQ6p4Kxiqv39stxJTaq6EfQAvUlpSwihkqrX6IC1reKtYIfILzfGryFh5_EZeMCnf6cIKbng70ZXk7GAje_wtRsBX0a7gZSjyQX0Ny4GP4LPZhhu8Q_oXJl3-GpjJufXOPT4ZwgZn5RHLoPNc4S36FVvhgTvHs4j9Ovb6fXyvLq4PPu-PLmorCAkV5JxJSjnFlpgdQ2qL6lEr2rR8tqsWM8UW1lqoDGSNqsWVBGEsiChAw6KH6GvO99pXo3Q2bJkNIOeohtNvNXBOP1U8W6j1-FGCylr0ZBi8PnBIIY_c8msR5csDIPxEOakafk_RohkrKCfnqHbMEdf4ulCNIooqdpCHe8oG0NKEfr9MpTouyJ1KVLTRt8XWfCP_wfYw4_NFeDDDtimHOJeV6VjIVXN_wEy3qQJ</recordid><startdate>20171001</startdate><enddate>20171001</enddate><creator>Walker, Liam</creator><creator>Boddington, Clare</creator><creator>Jenkins, Dafyd</creator><creator>Wang, Ying</creator><creator>Grønlund, Jesper T.</creator><creator>Hulsmans, Jo</creator><creator>Kumar, Sanjeev</creator><creator>Patel, Dhaval</creator><creator>Moore, Jonathan D.</creator><creator>Carter, Anthony</creator><creator>Samavedam, Siva</creator><creator>Bonomo, Giovanni</creator><creator>Hersh, David S.</creator><creator>Coruzzi, Gloria M.</creator><creator>Burroughs, Nigel J.</creator><creator>Gifford, Miriam L.</creator><general>American Society of Plant Biologists</general><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>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5486-0407</orcidid><orcidid>https://orcid.org/0000-0002-4005-2513</orcidid><orcidid>https://orcid.org/0000-0002-2099-0596</orcidid><orcidid>https://orcid.org/0000-0003-0875-1936</orcidid><orcidid>https://orcid.org/0000-0003-2608-2166</orcidid><orcidid>https://orcid.org/0000-0003-0261-0518</orcidid><orcidid>https://orcid.org/0000-0002-3561-8180</orcidid></search><sort><creationdate>20171001</creationdate><title>Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture</title><author>Walker, Liam ; 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subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Architecture Biological activity Environmental regulations Gene expression Gene Expression Regulation, Plant - genetics Gene families Large-Scale Biology LARGE-SCALE BIOLOGY ARTICLE Molecular modelling Plant Roots - genetics Plant Roots - metabolism Root development Transcription |
title | Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture |
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