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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Veröffentlicht in:Annals of botany 2018-12, Vol.122 (7), p.1117-1129
Hauptverfasser: 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
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container_end_page 1129
container_issue 7
container_start_page 1117
container_title Annals of botany
container_volume 122
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
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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 &amp; 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. 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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. 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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 &amp; 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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