Innovation, conservation, and repurposing of gene function in root cell type development
Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation,...
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| Veröffentlicht in: | Cell 2021-06, Vol.184 (12), p.3333-3348.e19 |
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| creator | Kajala, Kaisa Gouran, Mona Shaar-Moshe, Lidor Mason, G. Alex Rodriguez-Medina, Joel Kawa, Dorota Pauluzzi, Germain Reynoso, Mauricio Canto-Pastor, Alex Manzano, Concepcion Lau, Vincent Artur, Mariana A.S. West, Donnelly A. Gray, Sharon B. Borowsky, Alexander T. Moore, Bryshal P. Yao, Andrew I. Morimoto, Kevin W. Bajic, Marko Formentin, Elide Nirmal, Niba A. Rodriguez, Alan Pasha, Asher Deal, Roger B. Kliebenstein, Daniel J. Hvidsten, Torgeir R. Provart, Nicholas J. Sinha, Neelima R. Runcie, Daniel E. Bailey-Serres, Julia Brady, Siobhan M. |
| description | Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.
[Display omitted]
•Tomato cell type-resolution translatome atlas reveals cell type function•Conservation and repurposing in gene regulation between Arabidopsis and tomato•The tomato exodermis is lignified, suberized, and enriched for nitrogen regulation•The root meristem is molecularly homologous across plant species
The integration of pan-species cell type data reveals molecular signatures across growth conditions and sheds light on novelty, conservation, and repurposing of gene function relevant to crop engineering. |
| doi_str_mv | 10.1016/j.cell.2021.04.024 |
| format | Article |
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[Display omitted]
•Tomato cell type-resolution translatome atlas reveals cell type function•Conservation and repurposing in gene regulation between Arabidopsis and tomato•The tomato exodermis is lignified, suberized, and enriched for nitrogen regulation•The root meristem is molecularly homologous across plant species
The integration of pan-species cell type data reveals molecular signatures across growth conditions and sheds light on novelty, conservation, and repurposing of gene function relevant to crop engineering.</description><identifier>ISSN: 0092-8674</identifier><identifier>EISSN: 1097-4172</identifier><identifier>DOI: 10.1016/j.cell.2021.04.024</identifier><identifier>PMID: 34010619</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; cell types ; evolution ; exodermis ; gene expression ; Gene Expression Regulation, Plant ; gene regulation ; Gene Regulatory Networks ; genes ; Genes, Plant ; Green Fluorescent Proteins - metabolism ; Inventions ; Lycopersicon esculentum - cytology ; Lycopersicon esculentum - genetics ; Meristem - metabolism ; Plant Proteins - genetics ; Plant Proteins - metabolism ; plant root cells ; Plant Roots - cytology ; Plant Roots - genetics ; Plant Roots - growth & development ; Promoter Regions, Genetic - genetics ; Protein Biosynthesis ; rice ; root development ; root meristems ; Species Specificity ; tomato ; tomatoes ; Transcription Factors - metabolism ; translatomes ; xylem ; Xylem - genetics</subject><ispartof>Cell, 2021-06, Vol.184 (12), p.3333-3348.e19</ispartof><rights>2021 The Author(s)</rights><rights>Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c433t-ca1359595c4cf06409c2864d1feb6927d9d450d324ec920d0e8a24e302753fd73</citedby><cites>FETCH-LOGICAL-c433t-ca1359595c4cf06409c2864d1feb6927d9d450d324ec920d0e8a24e302753fd73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0092867421005043$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34010619$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kajala, Kaisa</creatorcontrib><creatorcontrib>Gouran, Mona</creatorcontrib><creatorcontrib>Shaar-Moshe, Lidor</creatorcontrib><creatorcontrib>Mason, G. Alex</creatorcontrib><creatorcontrib>Rodriguez-Medina, Joel</creatorcontrib><creatorcontrib>Kawa, Dorota</creatorcontrib><creatorcontrib>Pauluzzi, Germain</creatorcontrib><creatorcontrib>Reynoso, Mauricio</creatorcontrib><creatorcontrib>Canto-Pastor, Alex</creatorcontrib><creatorcontrib>Manzano, Concepcion</creatorcontrib><creatorcontrib>Lau, Vincent</creatorcontrib><creatorcontrib>Artur, Mariana A.S.</creatorcontrib><creatorcontrib>West, Donnelly A.</creatorcontrib><creatorcontrib>Gray, Sharon B.</creatorcontrib><creatorcontrib>Borowsky, Alexander T.</creatorcontrib><creatorcontrib>Moore, Bryshal P.</creatorcontrib><creatorcontrib>Yao, Andrew I.</creatorcontrib><creatorcontrib>Morimoto, Kevin W.</creatorcontrib><creatorcontrib>Bajic, Marko</creatorcontrib><creatorcontrib>Formentin, Elide</creatorcontrib><creatorcontrib>Nirmal, Niba A.</creatorcontrib><creatorcontrib>Rodriguez, Alan</creatorcontrib><creatorcontrib>Pasha, Asher</creatorcontrib><creatorcontrib>Deal, Roger B.</creatorcontrib><creatorcontrib>Kliebenstein, Daniel J.</creatorcontrib><creatorcontrib>Hvidsten, Torgeir R.</creatorcontrib><creatorcontrib>Provart, Nicholas J.</creatorcontrib><creatorcontrib>Sinha, Neelima R.</creatorcontrib><creatorcontrib>Runcie, Daniel E.</creatorcontrib><creatorcontrib>Bailey-Serres, Julia</creatorcontrib><creatorcontrib>Brady, Siobhan M.</creatorcontrib><title>Innovation, conservation, and repurposing of gene function in root cell type development</title><title>Cell</title><addtitle>Cell</addtitle><description>Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.
[Display omitted]
•Tomato cell type-resolution translatome atlas reveals cell type function•Conservation and repurposing in gene regulation between Arabidopsis and tomato•The tomato exodermis is lignified, suberized, and enriched for nitrogen regulation•The root meristem is molecularly homologous across plant species
The integration of pan-species cell type data reveals molecular signatures across growth conditions and sheds light on novelty, conservation, and repurposing of gene function relevant to crop engineering.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>cell types</subject><subject>evolution</subject><subject>exodermis</subject><subject>gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>gene regulation</subject><subject>Gene Regulatory Networks</subject><subject>genes</subject><subject>Genes, Plant</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Inventions</subject><subject>Lycopersicon esculentum - cytology</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Meristem - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>plant root cells</subject><subject>Plant Roots - cytology</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - growth & development</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Protein Biosynthesis</subject><subject>rice</subject><subject>root development</subject><subject>root meristems</subject><subject>Species Specificity</subject><subject>tomato</subject><subject>tomatoes</subject><subject>Transcription Factors - metabolism</subject><subject>translatomes</subject><subject>xylem</subject><subject>Xylem - genetics</subject><issn>0092-8674</issn><issn>1097-4172</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkMtKxDAUhoMoOo6-gAvJ0oWtJ5deAm5k8AaCGwV3oSankmEmqUk7MG9vy6hLkbPICXz_z-Ej5IxBzoCVV8vc4GqVc-AsB5kDl3tkxkBVmWQV3yczAMWzuqzkETlOaQkAdVEUh-RISGBQMjUjb4_eh03Tu-AvqQk-Yfz5Nd7SiN0Qu5Cc_6ChpR_okbaDNxNBnacxhJ5OV9B-2yG1uMFV6Nbo-xNy0DarhKff75y83t2-LB6yp-f7x8XNU2akEH1mGiYKNY6RpoVSgjK8LqVlLb6XildWWVmAFVyiURwsYN2MuwBeFaK1lZiTi11vF8PngKnXa5emixqPYUiaFwVTTJSs_gfKleIlr_iI8h1qYkgpYqu76NZN3GoGepKvl3pK6km-BqlH-WPo_Lt_eF-j_Y382B6B6x2Ao5CNw6iTcegNWhfR9NoG91f_F4f3lRg</recordid><startdate>20210610</startdate><enddate>20210610</enddate><creator>Kajala, Kaisa</creator><creator>Gouran, Mona</creator><creator>Shaar-Moshe, Lidor</creator><creator>Mason, G. Alex</creator><creator>Rodriguez-Medina, Joel</creator><creator>Kawa, Dorota</creator><creator>Pauluzzi, Germain</creator><creator>Reynoso, Mauricio</creator><creator>Canto-Pastor, Alex</creator><creator>Manzano, Concepcion</creator><creator>Lau, Vincent</creator><creator>Artur, Mariana A.S.</creator><creator>West, Donnelly A.</creator><creator>Gray, Sharon B.</creator><creator>Borowsky, Alexander T.</creator><creator>Moore, Bryshal P.</creator><creator>Yao, Andrew I.</creator><creator>Morimoto, Kevin W.</creator><creator>Bajic, Marko</creator><creator>Formentin, Elide</creator><creator>Nirmal, Niba A.</creator><creator>Rodriguez, Alan</creator><creator>Pasha, Asher</creator><creator>Deal, Roger B.</creator><creator>Kliebenstein, Daniel J.</creator><creator>Hvidsten, Torgeir R.</creator><creator>Provart, Nicholas J.</creator><creator>Sinha, Neelima R.</creator><creator>Runcie, Daniel E.</creator><creator>Bailey-Serres, Julia</creator><creator>Brady, Siobhan M.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20210610</creationdate><title>Innovation, conservation, and repurposing of gene function in root cell type development</title><author>Kajala, Kaisa ; Gouran, Mona ; Shaar-Moshe, Lidor ; Mason, G. Alex ; Rodriguez-Medina, Joel ; Kawa, Dorota ; Pauluzzi, Germain ; Reynoso, Mauricio ; Canto-Pastor, Alex ; Manzano, Concepcion ; Lau, Vincent ; Artur, Mariana A.S. ; West, Donnelly A. ; Gray, Sharon B. ; Borowsky, Alexander T. ; Moore, Bryshal P. ; Yao, Andrew I. ; Morimoto, Kevin W. ; Bajic, Marko ; Formentin, Elide ; Nirmal, Niba A. ; Rodriguez, Alan ; Pasha, Asher ; Deal, Roger B. ; Kliebenstein, Daniel J. ; Hvidsten, Torgeir R. ; Provart, Nicholas J. ; Sinha, Neelima R. ; Runcie, Daniel E. ; Bailey-Serres, Julia ; Brady, Siobhan M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c433t-ca1359595c4cf06409c2864d1feb6927d9d450d324ec920d0e8a24e302753fd73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>cell types</topic><topic>evolution</topic><topic>exodermis</topic><topic>gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>gene regulation</topic><topic>Gene Regulatory Networks</topic><topic>genes</topic><topic>Genes, Plant</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Inventions</topic><topic>Lycopersicon esculentum - cytology</topic><topic>Lycopersicon esculentum - genetics</topic><topic>Meristem - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>plant root cells</topic><topic>Plant Roots - cytology</topic><topic>Plant Roots - genetics</topic><topic>Plant Roots - growth & development</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Protein Biosynthesis</topic><topic>rice</topic><topic>root development</topic><topic>root meristems</topic><topic>Species Specificity</topic><topic>tomato</topic><topic>tomatoes</topic><topic>Transcription Factors - metabolism</topic><topic>translatomes</topic><topic>xylem</topic><topic>Xylem - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kajala, Kaisa</creatorcontrib><creatorcontrib>Gouran, Mona</creatorcontrib><creatorcontrib>Shaar-Moshe, Lidor</creatorcontrib><creatorcontrib>Mason, G. 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Alex</au><au>Rodriguez-Medina, Joel</au><au>Kawa, Dorota</au><au>Pauluzzi, Germain</au><au>Reynoso, Mauricio</au><au>Canto-Pastor, Alex</au><au>Manzano, Concepcion</au><au>Lau, Vincent</au><au>Artur, Mariana A.S.</au><au>West, Donnelly A.</au><au>Gray, Sharon B.</au><au>Borowsky, Alexander T.</au><au>Moore, Bryshal P.</au><au>Yao, Andrew I.</au><au>Morimoto, Kevin W.</au><au>Bajic, Marko</au><au>Formentin, Elide</au><au>Nirmal, Niba A.</au><au>Rodriguez, Alan</au><au>Pasha, Asher</au><au>Deal, Roger B.</au><au>Kliebenstein, Daniel J.</au><au>Hvidsten, Torgeir R.</au><au>Provart, Nicholas J.</au><au>Sinha, Neelima R.</au><au>Runcie, Daniel E.</au><au>Bailey-Serres, Julia</au><au>Brady, Siobhan M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Innovation, conservation, and repurposing of gene function in root cell type development</atitle><jtitle>Cell</jtitle><addtitle>Cell</addtitle><date>2021-06-10</date><risdate>2021</risdate><volume>184</volume><issue>12</issue><spage>3333</spage><epage>3348.e19</epage><pages>3333-3348.e19</pages><issn>0092-8674</issn><eissn>1097-4172</eissn><abstract>Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.
[Display omitted]
•Tomato cell type-resolution translatome atlas reveals cell type function•Conservation and repurposing in gene regulation between Arabidopsis and tomato•The tomato exodermis is lignified, suberized, and enriched for nitrogen regulation•The root meristem is molecularly homologous across plant species
The integration of pan-species cell type data reveals molecular signatures across growth conditions and sheds light on novelty, conservation, and repurposing of gene function relevant to crop engineering.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34010619</pmid><doi>10.1016/j.cell.2021.04.024</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Arabidopsis Arabidopsis - genetics cell types evolution exodermis gene expression Gene Expression Regulation, Plant gene regulation Gene Regulatory Networks genes Genes, Plant Green Fluorescent Proteins - metabolism Inventions Lycopersicon esculentum - cytology Lycopersicon esculentum - genetics Meristem - metabolism Plant Proteins - genetics Plant Proteins - metabolism plant root cells Plant Roots - cytology Plant Roots - genetics Plant Roots - growth & development Promoter Regions, Genetic - genetics Protein Biosynthesis rice root development root meristems Species Specificity tomato tomatoes Transcription Factors - metabolism translatomes xylem Xylem - genetics |
| title | Innovation, conservation, and repurposing of gene function in root cell type development |
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