COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis
Abstract Background and Aims Cultured cell suspensions have been the preferred model to study the apoplast as well as to monitor metabolic and cell cycle-related changes. Previous work showed that methyl jasmonate (MeJA) inhibits leaf growth in a CORONATINE INSENSITIVE 1 (COI1)-dependent manner, wit...
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creator | Bömer, Moritz O’Brien, José A Pérez-Salamó, Imma Krasauskas, Jovaras Finch, Paul Briones, Andrea Daudi, Arsalan Souda, Puneet Tsui, Tjir-Li Whitelegge, Julian P Paul Bolwell, G Devoto, Alessandra |
description | Abstract
Background and Aims
Cultured cell suspensions have been the preferred model to study the apoplast as well as to monitor metabolic and cell cycle-related changes. Previous work showed that methyl jasmonate (MeJA) inhibits leaf growth in a CORONATINE INSENSITIVE 1 (COI1)-dependent manner, with COI1 being the jasmonate (JA) receptor. Here, the effect of COI1 overexpression on the growth of stably transformed arabidopsis cell cultures is described.
Methods
Time-course experiments were carried out to analyse gene expression, and protein and metabolite levels.
Key Results
Both MeJA treatment and the overexpression of COI1 modify growth, by altering cell proliferation and expansion. DNA content as well as transcript patterns of cell cycle and cell wall remodelling markers were altered. COI1 overexpression also increases the protein levels of OLIGOGALACTURONIDE OXIDASE 1, BETA-GLUCOSIDASE/ENDOGLUCANASES and POLYGALACTURONASE INHIBITING PROTEIN2, reinforcing the role of COI1 in mediating defence responses and highlighting a link between cell wall loosening and growth regulation. Moreover, changes in the levels of the primary metabolites alanine, serine and succinic acid of MeJA-treated Arabidopsis cell cultures were observed. In addition, COI1 overexpression positively affects the availability of metabolites such as β-alanine, threonic acid, putrescine, glucose and myo-inositol, thereby providing a connection between JA-inhibited growth and stress responses.
Conclusions
This study contributes to the understanding of the regulation of growth and the production of metabolic resources by JAs and COI1. This will have important implications in dissecting the complex relationships between hormonal and cell wall signalling in plants. The work also provides tools to uncover novel mechanisms co-ordinating cell division and post-mitotic cell expansion in the absence of organ developmental control. |
doi_str_mv | 10.1093/aob/mcy109 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6324744</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/aob/mcy109</oup_id><sourcerecordid>2057440562</sourcerecordid><originalsourceid>FETCH-LOGICAL-c441t-cb481207423b4306d0313be2cd55de402378e26b3a836590c9d9b8b439a7b0623</originalsourceid><addsrcrecordid>eNqFkU1LHTEYhUNR9Gq76Q-QbIQinfpOkvnIplAuthUEN3Ud8nWvkZlkTDKK_fXmelXsphLIB--TwzkchD7X8K0GTk9lUKejfij3D2hR9qbqCYcdtAAKTdXRlu2jg5RuAIC0vN5D-4RzwijQBfq7vDyvK2Mn6431Gd_INAYvs8XJrb0cBufXWK5WVueE1zHc5-uveLRZqjC4Qk0xmFlnFzyW3mBthwHfl2-bQbbOYx3GKST3RJSnjFI5E6bk0ke0u5JDsp-ez0N09fPsz_J3dXH563z546LSjNW50or1NYGOEaqK59YAramyRJumMZYBoV1vSauo7GnbcNDccNUXlMtOQUvoIfq-1Z1mNVqjS8woBzFFN8r4IIJ04t-Jd9diHe5ESwnrGCsCX54FYridbcpidGmTVHob5iSKA0agKet9FJqiCM2TrZMtqmNIKdrVq6MaxKZXUXoV214LfPQ2wyv6UmQBjrdAmKf_CT0CPLmt2A</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2057440562</pqid></control><display><type>article</type><title>COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis</title><source>MEDLINE</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Jstor Complete Legacy</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>PubMed Central</source><creator>Bömer, Moritz ; O’Brien, José A ; Pérez-Salamó, Imma ; Krasauskas, Jovaras ; Finch, Paul ; Briones, Andrea ; Daudi, Arsalan ; Souda, Puneet ; Tsui, Tjir-Li ; Whitelegge, Julian P ; Paul Bolwell, G ; Devoto, Alessandra</creator><creatorcontrib>Bömer, Moritz ; O’Brien, José A ; Pérez-Salamó, Imma ; Krasauskas, Jovaras ; Finch, Paul ; Briones, Andrea ; Daudi, Arsalan ; Souda, Puneet ; Tsui, Tjir-Li ; Whitelegge, Julian P ; Paul Bolwell, G ; Devoto, Alessandra</creatorcontrib><description>Abstract
Background and Aims
Cultured cell suspensions have been the preferred model to study the apoplast as well as to monitor metabolic and cell cycle-related changes. Previous work showed that methyl jasmonate (MeJA) inhibits leaf growth in a CORONATINE INSENSITIVE 1 (COI1)-dependent manner, with COI1 being the jasmonate (JA) receptor. Here, the effect of COI1 overexpression on the growth of stably transformed arabidopsis cell cultures is described.
Methods
Time-course experiments were carried out to analyse gene expression, and protein and metabolite levels.
Key Results
Both MeJA treatment and the overexpression of COI1 modify growth, by altering cell proliferation and expansion. DNA content as well as transcript patterns of cell cycle and cell wall remodelling markers were altered. COI1 overexpression also increases the protein levels of OLIGOGALACTURONIDE OXIDASE 1, BETA-GLUCOSIDASE/ENDOGLUCANASES and POLYGALACTURONASE INHIBITING PROTEIN2, reinforcing the role of COI1 in mediating defence responses and highlighting a link between cell wall loosening and growth regulation. Moreover, changes in the levels of the primary metabolites alanine, serine and succinic acid of MeJA-treated Arabidopsis cell cultures were observed. In addition, COI1 overexpression positively affects the availability of metabolites such as β-alanine, threonic acid, putrescine, glucose and myo-inositol, thereby providing a connection between JA-inhibited growth and stress responses.
Conclusions
This study contributes to the understanding of the regulation of growth and the production of metabolic resources by JAs and COI1. This will have important implications in dissecting the complex relationships between hormonal and cell wall signalling in plants. The work also provides tools to uncover novel mechanisms co-ordinating cell division and post-mitotic cell expansion in the absence of organ developmental control.</description><identifier>ISSN: 0305-7364</identifier><identifier>ISSN: 1095-8290</identifier><identifier>EISSN: 1095-8290</identifier><identifier>DOI: 10.1093/aob/mcy109</identifier><identifier>PMID: 29924303</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Acetates - metabolism ; alanine ; apoplast ; Arabidopsis ; Arabidopsis - chemistry ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; beta-alanine ; beta-glucosidase ; cell division ; Cell Division - genetics ; cell proliferation ; cell suspension culture ; Cell Wall - physiology ; cell walls ; cultured cells ; Cyclopentanes - metabolism ; DNA ; gene expression ; Gene Expression Regulation, Plant - physiology ; Genes, cdc - physiology ; glucose ; jasmonic acid ; leaves ; messenger RNA ; metabolites ; methyl jasmonate ; myo-inositol ; Original ; Oxylipins - metabolism ; Plant Proteins - metabolism ; polygalacturonase ; protein content ; putrescine ; serine ; Signal Transduction ; stress response ; structural proteins ; succinic acid</subject><ispartof>Annals of botany, 2018-12, Vol.122 (7), p.1117-1129</ispartof><rights>The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c441t-cb481207423b4306d0313be2cd55de402378e26b3a836590c9d9b8b439a7b0623</citedby><cites>FETCH-LOGICAL-c441t-cb481207423b4306d0313be2cd55de402378e26b3a836590c9d9b8b439a7b0623</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6324744/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6324744/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,725,778,782,883,1581,27907,27908,53774,53776</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29924303$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bömer, Moritz</creatorcontrib><creatorcontrib>O’Brien, José A</creatorcontrib><creatorcontrib>Pérez-Salamó, Imma</creatorcontrib><creatorcontrib>Krasauskas, Jovaras</creatorcontrib><creatorcontrib>Finch, Paul</creatorcontrib><creatorcontrib>Briones, Andrea</creatorcontrib><creatorcontrib>Daudi, Arsalan</creatorcontrib><creatorcontrib>Souda, Puneet</creatorcontrib><creatorcontrib>Tsui, Tjir-Li</creatorcontrib><creatorcontrib>Whitelegge, Julian P</creatorcontrib><creatorcontrib>Paul Bolwell, G</creatorcontrib><creatorcontrib>Devoto, Alessandra</creatorcontrib><title>COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis</title><title>Annals of botany</title><addtitle>Ann Bot</addtitle><description>Abstract
Background and Aims
Cultured cell suspensions have been the preferred model to study the apoplast as well as to monitor metabolic and cell cycle-related changes. Previous work showed that methyl jasmonate (MeJA) inhibits leaf growth in a CORONATINE INSENSITIVE 1 (COI1)-dependent manner, with COI1 being the jasmonate (JA) receptor. Here, the effect of COI1 overexpression on the growth of stably transformed arabidopsis cell cultures is described.
Methods
Time-course experiments were carried out to analyse gene expression, and protein and metabolite levels.
Key Results
Both MeJA treatment and the overexpression of COI1 modify growth, by altering cell proliferation and expansion. DNA content as well as transcript patterns of cell cycle and cell wall remodelling markers were altered. COI1 overexpression also increases the protein levels of OLIGOGALACTURONIDE OXIDASE 1, BETA-GLUCOSIDASE/ENDOGLUCANASES and POLYGALACTURONASE INHIBITING PROTEIN2, reinforcing the role of COI1 in mediating defence responses and highlighting a link between cell wall loosening and growth regulation. Moreover, changes in the levels of the primary metabolites alanine, serine and succinic acid of MeJA-treated Arabidopsis cell cultures were observed. In addition, COI1 overexpression positively affects the availability of metabolites such as β-alanine, threonic acid, putrescine, glucose and myo-inositol, thereby providing a connection between JA-inhibited growth and stress responses.
Conclusions
This study contributes to the understanding of the regulation of growth and the production of metabolic resources by JAs and COI1. This will have important implications in dissecting the complex relationships between hormonal and cell wall signalling in plants. The work also provides tools to uncover novel mechanisms co-ordinating cell division and post-mitotic cell expansion in the absence of organ developmental control.</description><subject>Acetates - metabolism</subject><subject>alanine</subject><subject>apoplast</subject><subject>Arabidopsis</subject><subject>Arabidopsis - chemistry</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>beta-alanine</subject><subject>beta-glucosidase</subject><subject>cell division</subject><subject>Cell Division - genetics</subject><subject>cell proliferation</subject><subject>cell suspension culture</subject><subject>Cell Wall - physiology</subject><subject>cell walls</subject><subject>cultured cells</subject><subject>Cyclopentanes - metabolism</subject><subject>DNA</subject><subject>gene expression</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Genes, cdc - physiology</subject><subject>glucose</subject><subject>jasmonic acid</subject><subject>leaves</subject><subject>messenger RNA</subject><subject>metabolites</subject><subject>methyl jasmonate</subject><subject>myo-inositol</subject><subject>Original</subject><subject>Oxylipins - metabolism</subject><subject>Plant Proteins - metabolism</subject><subject>polygalacturonase</subject><subject>protein content</subject><subject>putrescine</subject><subject>serine</subject><subject>Signal Transduction</subject><subject>stress response</subject><subject>structural proteins</subject><subject>succinic acid</subject><issn>0305-7364</issn><issn>1095-8290</issn><issn>1095-8290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqFkU1LHTEYhUNR9Gq76Q-QbIQinfpOkvnIplAuthUEN3Ud8nWvkZlkTDKK_fXmelXsphLIB--TwzkchD7X8K0GTk9lUKejfij3D2hR9qbqCYcdtAAKTdXRlu2jg5RuAIC0vN5D-4RzwijQBfq7vDyvK2Mn6431Gd_INAYvs8XJrb0cBufXWK5WVueE1zHc5-uveLRZqjC4Qk0xmFlnFzyW3mBthwHfl2-bQbbOYx3GKST3RJSnjFI5E6bk0ke0u5JDsp-ez0N09fPsz_J3dXH563z546LSjNW50or1NYGOEaqK59YAramyRJumMZYBoV1vSauo7GnbcNDccNUXlMtOQUvoIfq-1Z1mNVqjS8woBzFFN8r4IIJ04t-Jd9diHe5ESwnrGCsCX54FYridbcpidGmTVHob5iSKA0agKet9FJqiCM2TrZMtqmNIKdrVq6MaxKZXUXoV214LfPQ2wyv6UmQBjrdAmKf_CT0CPLmt2A</recordid><startdate>20181204</startdate><enddate>20181204</enddate><creator>Bömer, Moritz</creator><creator>O’Brien, José A</creator><creator>Pérez-Salamó, Imma</creator><creator>Krasauskas, Jovaras</creator><creator>Finch, Paul</creator><creator>Briones, Andrea</creator><creator>Daudi, Arsalan</creator><creator>Souda, Puneet</creator><creator>Tsui, Tjir-Li</creator><creator>Whitelegge, Julian P</creator><creator>Paul Bolwell, G</creator><creator>Devoto, Alessandra</creator><general>Oxford University Press</general><scope>TOX</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><scope>5PM</scope></search><sort><creationdate>20181204</creationdate><title>COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis</title><author>Bömer, Moritz ; O’Brien, José A ; Pérez-Salamó, Imma ; Krasauskas, Jovaras ; Finch, Paul ; Briones, Andrea ; Daudi, Arsalan ; Souda, Puneet ; Tsui, Tjir-Li ; Whitelegge, Julian P ; Paul Bolwell, G ; Devoto, Alessandra</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c441t-cb481207423b4306d0313be2cd55de402378e26b3a836590c9d9b8b439a7b0623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Acetates - metabolism</topic><topic>alanine</topic><topic>apoplast</topic><topic>Arabidopsis</topic><topic>Arabidopsis - chemistry</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>beta-alanine</topic><topic>beta-glucosidase</topic><topic>cell division</topic><topic>Cell Division - genetics</topic><topic>cell proliferation</topic><topic>cell suspension culture</topic><topic>Cell Wall - physiology</topic><topic>cell walls</topic><topic>cultured cells</topic><topic>Cyclopentanes - metabolism</topic><topic>DNA</topic><topic>gene expression</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Genes, cdc - physiology</topic><topic>glucose</topic><topic>jasmonic acid</topic><topic>leaves</topic><topic>messenger RNA</topic><topic>metabolites</topic><topic>methyl jasmonate</topic><topic>myo-inositol</topic><topic>Original</topic><topic>Oxylipins - metabolism</topic><topic>Plant Proteins - metabolism</topic><topic>polygalacturonase</topic><topic>protein content</topic><topic>putrescine</topic><topic>serine</topic><topic>Signal Transduction</topic><topic>stress response</topic><topic>structural proteins</topic><topic>succinic acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bömer, Moritz</creatorcontrib><creatorcontrib>O’Brien, José A</creatorcontrib><creatorcontrib>Pérez-Salamó, Imma</creatorcontrib><creatorcontrib>Krasauskas, Jovaras</creatorcontrib><creatorcontrib>Finch, Paul</creatorcontrib><creatorcontrib>Briones, Andrea</creatorcontrib><creatorcontrib>Daudi, Arsalan</creatorcontrib><creatorcontrib>Souda, Puneet</creatorcontrib><creatorcontrib>Tsui, Tjir-Li</creatorcontrib><creatorcontrib>Whitelegge, Julian P</creatorcontrib><creatorcontrib>Paul Bolwell, G</creatorcontrib><creatorcontrib>Devoto, Alessandra</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Annals of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bömer, Moritz</au><au>O’Brien, José A</au><au>Pérez-Salamó, Imma</au><au>Krasauskas, Jovaras</au><au>Finch, Paul</au><au>Briones, Andrea</au><au>Daudi, Arsalan</au><au>Souda, Puneet</au><au>Tsui, Tjir-Li</au><au>Whitelegge, Julian P</au><au>Paul Bolwell, G</au><au>Devoto, Alessandra</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis</atitle><jtitle>Annals of botany</jtitle><addtitle>Ann Bot</addtitle><date>2018-12-04</date><risdate>2018</risdate><volume>122</volume><issue>7</issue><spage>1117</spage><epage>1129</epage><pages>1117-1129</pages><issn>0305-7364</issn><issn>1095-8290</issn><eissn>1095-8290</eissn><abstract>Abstract
Background and Aims
Cultured cell suspensions have been the preferred model to study the apoplast as well as to monitor metabolic and cell cycle-related changes. Previous work showed that methyl jasmonate (MeJA) inhibits leaf growth in a CORONATINE INSENSITIVE 1 (COI1)-dependent manner, with COI1 being the jasmonate (JA) receptor. Here, the effect of COI1 overexpression on the growth of stably transformed arabidopsis cell cultures is described.
Methods
Time-course experiments were carried out to analyse gene expression, and protein and metabolite levels.
Key Results
Both MeJA treatment and the overexpression of COI1 modify growth, by altering cell proliferation and expansion. DNA content as well as transcript patterns of cell cycle and cell wall remodelling markers were altered. COI1 overexpression also increases the protein levels of OLIGOGALACTURONIDE OXIDASE 1, BETA-GLUCOSIDASE/ENDOGLUCANASES and POLYGALACTURONASE INHIBITING PROTEIN2, reinforcing the role of COI1 in mediating defence responses and highlighting a link between cell wall loosening and growth regulation. Moreover, changes in the levels of the primary metabolites alanine, serine and succinic acid of MeJA-treated Arabidopsis cell cultures were observed. In addition, COI1 overexpression positively affects the availability of metabolites such as β-alanine, threonic acid, putrescine, glucose and myo-inositol, thereby providing a connection between JA-inhibited growth and stress responses.
Conclusions
This study contributes to the understanding of the regulation of growth and the production of metabolic resources by JAs and COI1. This will have important implications in dissecting the complex relationships between hormonal and cell wall signalling in plants. The work also provides tools to uncover novel mechanisms co-ordinating cell division and post-mitotic cell expansion in the absence of organ developmental control.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>29924303</pmid><doi>10.1093/aob/mcy109</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current); PubMed Central |
subjects | Acetates - metabolism alanine apoplast Arabidopsis Arabidopsis - chemistry Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism beta-alanine beta-glucosidase cell division Cell Division - genetics cell proliferation cell suspension culture Cell Wall - physiology cell walls cultured cells Cyclopentanes - metabolism DNA gene expression Gene Expression Regulation, Plant - physiology Genes, cdc - physiology glucose jasmonic acid leaves messenger RNA metabolites methyl jasmonate myo-inositol Original Oxylipins - metabolism Plant Proteins - metabolism polygalacturonase protein content putrescine serine Signal Transduction stress response structural proteins succinic acid |
title | COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis |
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