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Oligogalactolipid production during cold challenge is conserved in early diverging lineages
Abstract Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), c...
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Published in: | Journal of experimental botany 2023-09, Vol.74 (17), p.5405-5417 |
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creator | Barnes, Allison C Myers, Jennifer L Surber, Samantha M Liang, Zhikai Mower, Jeffrey P Schnable, James C Roston, Rebecca L |
description | Abstract
Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), contributes to survival in severe cold. Here, we investigated oligogalactolipid production in species from bryophytes to angiosperms. Production of oligogalactolipids differed within each clade, suggesting multiple evolutionary origins of severe cold tolerance. We also observed greater oligogalactolipid production in control samples than in temperature-challenged samples of some species. Further examination of representative species revealed a tight association between temperature, damage, and oligogalactolipid production that scaled with the cold tolerance of each species. Based on oligogalactolipid production and transcript changes, multiple angiosperm species share a signal of oligogalactolipid production initially described in Arabidopsis, namely cytosolic acidification. Together, these data suggest that oligogalactolipid production is a severe cold response that originated from an ancestral damage response that remains in many land plant lineages and that cytosolic acidification may be a common signaling mechanism for its activation.
Oligogalactolipid production is a response to severe cold in many land plant lineages. It occurs during times of membrane damage and can be reproduced in multiple species by cytosolic acidification. |
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Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), contributes to survival in severe cold. Here, we investigated oligogalactolipid production in species from bryophytes to angiosperms. Production of oligogalactolipids differed within each clade, suggesting multiple evolutionary origins of severe cold tolerance. We also observed greater oligogalactolipid production in control samples than in temperature-challenged samples of some species. Further examination of representative species revealed a tight association between temperature, damage, and oligogalactolipid production that scaled with the cold tolerance of each species. Based on oligogalactolipid production and transcript changes, multiple angiosperm species share a signal of oligogalactolipid production initially described in Arabidopsis, namely cytosolic acidification. Together, these data suggest that oligogalactolipid production is a severe cold response that originated from an ancestral damage response that remains in many land plant lineages and that cytosolic acidification may be a common signaling mechanism for its activation.
Oligogalactolipid production is a response to severe cold in many land plant lineages. It occurs during times of membrane damage and can be reproduced in multiple species by cytosolic acidification.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erad241</identifier><identifier>PMID: 37357909</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Acclimatization - physiology ; Arabidopsis - metabolism ; Arabidopsis Proteins - metabolism ; Cold Temperature ; Editor's Choice ; Gene Expression Regulation, Plant ; Magnoliopsida - metabolism ; Research Papers ; Temperature</subject><ispartof>Journal of experimental botany, 2023-09, Vol.74 (17), p.5405-5417</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c413t-c135763695f6d7a45b437a6a47c9ef8b132b6e209f64ddd9cf083b5641926af63</citedby><cites>FETCH-LOGICAL-c413t-c135763695f6d7a45b437a6a47c9ef8b132b6e209f64ddd9cf083b5641926af63</cites><orcidid>0000-0002-3063-5002 ; 0000-0002-9963-8631 ; 0000-0001-6739-5527 ; 0000-0001-9539-3297</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37357909$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Nakamura, Yuki</contributor><creatorcontrib>Barnes, Allison C</creatorcontrib><creatorcontrib>Myers, Jennifer L</creatorcontrib><creatorcontrib>Surber, Samantha M</creatorcontrib><creatorcontrib>Liang, Zhikai</creatorcontrib><creatorcontrib>Mower, Jeffrey P</creatorcontrib><creatorcontrib>Schnable, James C</creatorcontrib><creatorcontrib>Roston, Rebecca L</creatorcontrib><title>Oligogalactolipid production during cold challenge is conserved in early diverging lineages</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Abstract
Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), contributes to survival in severe cold. Here, we investigated oligogalactolipid production in species from bryophytes to angiosperms. Production of oligogalactolipids differed within each clade, suggesting multiple evolutionary origins of severe cold tolerance. We also observed greater oligogalactolipid production in control samples than in temperature-challenged samples of some species. Further examination of representative species revealed a tight association between temperature, damage, and oligogalactolipid production that scaled with the cold tolerance of each species. Based on oligogalactolipid production and transcript changes, multiple angiosperm species share a signal of oligogalactolipid production initially described in Arabidopsis, namely cytosolic acidification. Together, these data suggest that oligogalactolipid production is a severe cold response that originated from an ancestral damage response that remains in many land plant lineages and that cytosolic acidification may be a common signaling mechanism for its activation.
Oligogalactolipid production is a response to severe cold in many land plant lineages. It occurs during times of membrane damage and can be reproduced in multiple species by cytosolic acidification.</description><subject>Acclimatization - physiology</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Cold Temperature</subject><subject>Editor's Choice</subject><subject>Gene Expression Regulation, Plant</subject><subject>Magnoliopsida - metabolism</subject><subject>Research Papers</subject><subject>Temperature</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp9kU1r3DAQhkVJSTZpT70Hn0IhuNGXZesUwtKkhYVc2lMPQpbGXi1ayZHsJfvv67Cb0Fx6Gph5eGeYB6EvBH8jWLKbzXN7A0lbyskHtCBc4JJyRk7QAmNKSyyr-gyd57zBGFe4qk7RGatZVUssF-jPo3d97LXXZozeDc4WQ4p2MqOLobBTcqEvTPS2MGvtPYQeCpfnTsiQdmALFwrQye8L63aQ-hfcuwC6h_wJfey0z_D5WC_Q7_vvv5Y_ytXjw8_l3ao0nLCxNGQ-RjAhq07YWvOq5azWQvPaSOialjDaCqBYdoJba6XpcMPaSnAiqdCdYBfo9pA7TO0WrIEwJu3VkNxWp72K2qn3k-DWqo87RXDDG8r4nPD1mJDi0wR5VFuXDXivA8QpK9pQWc-vw_WMXh9Qk2LOCbq3PQSrFx9q9qGOPmb68t_T3thXATNwdQDiNPw36S8f7pbd</recordid><startdate>20230913</startdate><enddate>20230913</enddate><creator>Barnes, Allison C</creator><creator>Myers, Jennifer L</creator><creator>Surber, Samantha M</creator><creator>Liang, Zhikai</creator><creator>Mower, Jeffrey P</creator><creator>Schnable, James C</creator><creator>Roston, Rebecca L</creator><general>Oxford University Press</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3063-5002</orcidid><orcidid>https://orcid.org/0000-0002-9963-8631</orcidid><orcidid>https://orcid.org/0000-0001-6739-5527</orcidid><orcidid>https://orcid.org/0000-0001-9539-3297</orcidid></search><sort><creationdate>20230913</creationdate><title>Oligogalactolipid production during cold challenge is conserved in early diverging lineages</title><author>Barnes, Allison C ; Myers, Jennifer L ; Surber, Samantha M ; Liang, Zhikai ; Mower, Jeffrey P ; Schnable, James C ; Roston, Rebecca L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c413t-c135763695f6d7a45b437a6a47c9ef8b132b6e209f64ddd9cf083b5641926af63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Acclimatization - physiology</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Cold Temperature</topic><topic>Editor's Choice</topic><topic>Gene Expression Regulation, Plant</topic><topic>Magnoliopsida - metabolism</topic><topic>Research Papers</topic><topic>Temperature</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barnes, Allison C</creatorcontrib><creatorcontrib>Myers, Jennifer L</creatorcontrib><creatorcontrib>Surber, Samantha M</creatorcontrib><creatorcontrib>Liang, Zhikai</creatorcontrib><creatorcontrib>Mower, Jeffrey P</creatorcontrib><creatorcontrib>Schnable, James C</creatorcontrib><creatorcontrib>Roston, Rebecca L</creatorcontrib><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>PubMed Central (Full Participant titles)</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barnes, Allison C</au><au>Myers, Jennifer L</au><au>Surber, Samantha M</au><au>Liang, Zhikai</au><au>Mower, Jeffrey P</au><au>Schnable, James C</au><au>Roston, Rebecca L</au><au>Nakamura, Yuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oligogalactolipid production during cold challenge is conserved in early diverging lineages</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2023-09-13</date><risdate>2023</risdate><volume>74</volume><issue>17</issue><spage>5405</spage><epage>5417</epage><pages>5405-5417</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Abstract
Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), contributes to survival in severe cold. Here, we investigated oligogalactolipid production in species from bryophytes to angiosperms. Production of oligogalactolipids differed within each clade, suggesting multiple evolutionary origins of severe cold tolerance. We also observed greater oligogalactolipid production in control samples than in temperature-challenged samples of some species. Further examination of representative species revealed a tight association between temperature, damage, and oligogalactolipid production that scaled with the cold tolerance of each species. Based on oligogalactolipid production and transcript changes, multiple angiosperm species share a signal of oligogalactolipid production initially described in Arabidopsis, namely cytosolic acidification. Together, these data suggest that oligogalactolipid production is a severe cold response that originated from an ancestral damage response that remains in many land plant lineages and that cytosolic acidification may be a common signaling mechanism for its activation.
Oligogalactolipid production is a response to severe cold in many land plant lineages. It occurs during times of membrane damage and can be reproduced in multiple species by cytosolic acidification.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>37357909</pmid><doi>10.1093/jxb/erad241</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-3063-5002</orcidid><orcidid>https://orcid.org/0000-0002-9963-8631</orcidid><orcidid>https://orcid.org/0000-0001-6739-5527</orcidid><orcidid>https://orcid.org/0000-0001-9539-3297</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acclimatization - physiology Arabidopsis - metabolism Arabidopsis Proteins - metabolism Cold Temperature Editor's Choice Gene Expression Regulation, Plant Magnoliopsida - metabolism Research Papers Temperature |
title | Oligogalactolipid production during cold challenge is conserved in early diverging lineages |
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