Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis
Lipid remodeling is crucial for hypoxic tolerance in animals, whilst little is known about the hypoxia-induced lipid dynamics in plants. Here we performed a mass spectrometry-based analysis to survey the lipid profiles of Arabidopsis rosettes under various hypoxic conditions. We observed that hypoxi...
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creator | Xie, Li-Juan Chen, Qin-Fang Chen, Mo-Xian Yu, Lu-Jun Huang, Li Chen, Liang Wang, Feng-Zhu Xia, Fan-Nv Zhu, Tian-Ren Wu, Jian-Xin Yin, Jian Liao, Bin Shi, Jianxin Zhang, Jian-Hua Aharoni, Asaph Yao, Nan Shu, Wensheng Xiao, Shi |
description | Lipid remodeling is crucial for hypoxic tolerance in animals, whilst little is known about the hypoxia-induced lipid dynamics in plants. Here we performed a mass spectrometry-based analysis to survey the lipid profiles of Arabidopsis rosettes under various hypoxic conditions. We observed that hypoxia caused a significant increase in total amounts of phosphatidylserine, phosphatidic acid and oxidized lipids, but a decrease in phosphatidylcholine (PC) and phosphatidylethanolamine (PE). Particularly, significant gains in the polyunsaturated species of PC, PE and phosphatidylinositol, and losses in their saturated and mono-unsaturated species were evident during hypoxia. Moreover, hypoxia led to a remarkable elevation of ceramides and hydroxyceramides. Disruption of ceramide synthases LOH1, LOH2 and LOH3 enhanced plant sensitivity to dark submergence, but displayed more resistance to submergence under light than wild type. Consistently, levels of unsaturated very-long-chain (VLC) ceramide species (22:1, 24:1 and 26:1) predominantly declined in the loh1, loh2 and loh3 mutants under dark submergence. In contrast, significant reduction of VLC ceramides in the loh1-1 loh3-1 knockdown double mutant and lacking of VLC unsaturated ceramides in the ads2 mutants impaired plant tolerance to both dark and light submergences. Evidence that C24:1-ceramide interacted with recombinant CTR1 protein and inhibited its kinase activity in vitro, enhanced ER-to-nucleus translocation of EIN2-GFP and stabilization of EIN3-GFP in vivo, suggests a role of ceramides in modulating CTR1-mediated ethylene signaling. The dark submergence-sensitive phenotypes of loh mutants were rescued by a ctr1-1 mutation. Thus, our findings demonstrate that unsaturation of VLC ceramides is a protective strategy for hypoxic tolerance in Arabidopsis. |
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Here we performed a mass spectrometry-based analysis to survey the lipid profiles of Arabidopsis rosettes under various hypoxic conditions. We observed that hypoxia caused a significant increase in total amounts of phosphatidylserine, phosphatidic acid and oxidized lipids, but a decrease in phosphatidylcholine (PC) and phosphatidylethanolamine (PE). Particularly, significant gains in the polyunsaturated species of PC, PE and phosphatidylinositol, and losses in their saturated and mono-unsaturated species were evident during hypoxia. Moreover, hypoxia led to a remarkable elevation of ceramides and hydroxyceramides. Disruption of ceramide synthases LOH1, LOH2 and LOH3 enhanced plant sensitivity to dark submergence, but displayed more resistance to submergence under light than wild type. Consistently, levels of unsaturated very-long-chain (VLC) ceramide species (22:1, 24:1 and 26:1) predominantly declined in the loh1, loh2 and loh3 mutants under dark submergence. In contrast, significant reduction of VLC ceramides in the loh1-1 loh3-1 knockdown double mutant and lacking of VLC unsaturated ceramides in the ads2 mutants impaired plant tolerance to both dark and light submergences. Evidence that C24:1-ceramide interacted with recombinant CTR1 protein and inhibited its kinase activity in vitro, enhanced ER-to-nucleus translocation of EIN2-GFP and stabilization of EIN3-GFP in vivo, suggests a role of ceramides in modulating CTR1-mediated ethylene signaling. The dark submergence-sensitive phenotypes of loh mutants were rescued by a ctr1-1 mutation. Thus, our findings demonstrate that unsaturation of VLC ceramides is a protective strategy for hypoxic tolerance in Arabidopsis.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005143</identifier><identifier>PMID: 25822663</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis thaliana ; Cellular signal transduction ; Ceramides - genetics ; Ceramides - metabolism ; Ethylenes - metabolism ; Fatty acids ; Gene expression ; Genetic aspects ; Hypoxia - genetics ; Identification and classification ; Kinases ; Lipid Metabolism - genetics ; Lipids ; Liposomes - metabolism ; Phosphatidic Acids - metabolism ; Phosphatidylcholines - metabolism ; Phosphatidylethanolamines - metabolism ; Phosphatidylserines - genetics ; Phosphatidylserines - metabolism ; Photoperiod ; Protein Kinases - genetics ; Protein Kinases - metabolism ; Seedlings - genetics ; Seedlings - growth & development ; Seedlings - metabolism ; Seeds ; Signal Transduction ; Sphingosine N-Acyltransferase - genetics</subject><ispartof>PLoS genetics, 2015-03, Vol.11 (3), p.e1005143-e1005143</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Xie et al 2015 Xie et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 11(3): e1005143. doi:10.1371/journal.pgen.1005143</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c764t-5ac8ea44627392696b9e6ecd4592812ea7d5f06af9c085a0edd2298d21dbcea53</citedby><cites>FETCH-LOGICAL-c764t-5ac8ea44627392696b9e6ecd4592812ea7d5f06af9c085a0edd2298d21dbcea53</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/PMC4379176/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4379176/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25822663$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Yu, Hao</contributor><creatorcontrib>Xie, Li-Juan</creatorcontrib><creatorcontrib>Chen, Qin-Fang</creatorcontrib><creatorcontrib>Chen, Mo-Xian</creatorcontrib><creatorcontrib>Yu, Lu-Jun</creatorcontrib><creatorcontrib>Huang, Li</creatorcontrib><creatorcontrib>Chen, Liang</creatorcontrib><creatorcontrib>Wang, Feng-Zhu</creatorcontrib><creatorcontrib>Xia, Fan-Nv</creatorcontrib><creatorcontrib>Zhu, Tian-Ren</creatorcontrib><creatorcontrib>Wu, Jian-Xin</creatorcontrib><creatorcontrib>Yin, Jian</creatorcontrib><creatorcontrib>Liao, Bin</creatorcontrib><creatorcontrib>Shi, Jianxin</creatorcontrib><creatorcontrib>Zhang, Jian-Hua</creatorcontrib><creatorcontrib>Aharoni, Asaph</creatorcontrib><creatorcontrib>Yao, Nan</creatorcontrib><creatorcontrib>Shu, Wensheng</creatorcontrib><creatorcontrib>Xiao, Shi</creatorcontrib><title>Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Lipid remodeling is crucial for hypoxic tolerance in animals, whilst little is known about the hypoxia-induced lipid dynamics in plants. Here we performed a mass spectrometry-based analysis to survey the lipid profiles of Arabidopsis rosettes under various hypoxic conditions. We observed that hypoxia caused a significant increase in total amounts of phosphatidylserine, phosphatidic acid and oxidized lipids, but a decrease in phosphatidylcholine (PC) and phosphatidylethanolamine (PE). Particularly, significant gains in the polyunsaturated species of PC, PE and phosphatidylinositol, and losses in their saturated and mono-unsaturated species were evident during hypoxia. Moreover, hypoxia led to a remarkable elevation of ceramides and hydroxyceramides. Disruption of ceramide synthases LOH1, LOH2 and LOH3 enhanced plant sensitivity to dark submergence, but displayed more resistance to submergence under light than wild type. Consistently, levels of unsaturated very-long-chain (VLC) ceramide species (22:1, 24:1 and 26:1) predominantly declined in the loh1, loh2 and loh3 mutants under dark submergence. In contrast, significant reduction of VLC ceramides in the loh1-1 loh3-1 knockdown double mutant and lacking of VLC unsaturated ceramides in the ads2 mutants impaired plant tolerance to both dark and light submergences. Evidence that C24:1-ceramide interacted with recombinant CTR1 protein and inhibited its kinase activity in vitro, enhanced ER-to-nucleus translocation of EIN2-GFP and stabilization of EIN3-GFP in vivo, suggests a role of ceramides in modulating CTR1-mediated ethylene signaling. The dark submergence-sensitive phenotypes of loh mutants were rescued by a ctr1-1 mutation. Thus, our findings demonstrate that unsaturation of VLC ceramides is a protective strategy for hypoxic tolerance in Arabidopsis.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Cellular signal transduction</subject><subject>Ceramides - genetics</subject><subject>Ceramides - metabolism</subject><subject>Ethylenes - metabolism</subject><subject>Fatty acids</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Hypoxia - genetics</subject><subject>Identification and classification</subject><subject>Kinases</subject><subject>Lipid Metabolism - genetics</subject><subject>Lipids</subject><subject>Liposomes - metabolism</subject><subject>Phosphatidic Acids - metabolism</subject><subject>Phosphatidylcholines - metabolism</subject><subject>Phosphatidylethanolamines - metabolism</subject><subject>Phosphatidylserines - genetics</subject><subject>Phosphatidylserines - metabolism</subject><subject>Photoperiod</subject><subject>Protein Kinases - genetics</subject><subject>Protein Kinases - metabolism</subject><subject>Seedlings - genetics</subject><subject>Seedlings - growth & development</subject><subject>Seedlings - metabolism</subject><subject>Seeds</subject><subject>Signal Transduction</subject><subject>Sphingosine N-Acyltransferase - genetics</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11rFDEUhgdRbK3-A9EBQfRi1snnzNwIS_GjUCyo9TacSc7MpswkazJTuj_A_23W3ZYueKHkIuHkOW8O78nJsuekXBBWkXdXfg4OhsW6R7cgZSkIZw-yYyIEKype8of3zkfZkxivypKJuqkeZ0dU1JRKyY6zX5cuwjQHmKx3ue_yawybYvCuL_QKrMs1BhitwZivg59QT-kwgJvyLvgxX23W_sZCYZ2ZNZrcwAh9YttNPnozD0nW9TlOq82ADvNo-1TyNpSUlwFaa_w62vg0e9TBEPHZfj_JLj9--H76uTi_-HR2ujwvdCX5VAjQNQLnklasobKRbYMSteGioTWhCJURXSmha3RZCyjRGEqb2lBiWo0g2En2cqe7HnxUewejIrJO7pVckESc7Qjj4Uqtgx0hbJQHq_4EfOgVhMnqARUQrCTjrSSk48LwFqjAVkAnmQRSm6T1fv_a3I5oNLopwHAgenjj7Er1_lpxVjUkaZ9kb_YCwf-cMU5qtFHjkPxHP2_rljVlVU23db_aoT2k0qzrfFLUW1wtOam5FJSxRC3-QqVlcLTaO-xsih8kvD1ISMyEN1MPc4zq7NvX_2C__Dt78eOQfX2PXSEM0yr6Yd7-2HgI8h2og48xYHdnNSnVdmZuO662M6P2M5PSXtxv013S7ZCw33BjFFQ</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Xie, Li-Juan</creator><creator>Chen, Qin-Fang</creator><creator>Chen, Mo-Xian</creator><creator>Yu, Lu-Jun</creator><creator>Huang, Li</creator><creator>Chen, Liang</creator><creator>Wang, Feng-Zhu</creator><creator>Xia, Fan-Nv</creator><creator>Zhu, Tian-Ren</creator><creator>Wu, Jian-Xin</creator><creator>Yin, Jian</creator><creator>Liao, Bin</creator><creator>Shi, Jianxin</creator><creator>Zhang, Jian-Hua</creator><creator>Aharoni, Asaph</creator><creator>Yao, Nan</creator><creator>Shu, Wensheng</creator><creator>Xiao, Shi</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150301</creationdate><title>Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis</title><author>Xie, Li-Juan ; Chen, Qin-Fang ; Chen, Mo-Xian ; Yu, Lu-Jun ; Huang, Li ; Chen, Liang ; Wang, Feng-Zhu ; Xia, Fan-Nv ; Zhu, Tian-Ren ; Wu, Jian-Xin ; Yin, Jian ; Liao, Bin ; Shi, Jianxin ; Zhang, Jian-Hua ; Aharoni, Asaph ; Yao, Nan ; Shu, Wensheng ; Xiao, Shi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c764t-5ac8ea44627392696b9e6ecd4592812ea7d5f06af9c085a0edd2298d21dbcea53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Cellular signal transduction</topic><topic>Ceramides - genetics</topic><topic>Ceramides - metabolism</topic><topic>Ethylenes - metabolism</topic><topic>Fatty acids</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Hypoxia - genetics</topic><topic>Identification and classification</topic><topic>Kinases</topic><topic>Lipid Metabolism - genetics</topic><topic>Lipids</topic><topic>Liposomes - metabolism</topic><topic>Phosphatidic Acids - metabolism</topic><topic>Phosphatidylcholines - metabolism</topic><topic>Phosphatidylethanolamines - metabolism</topic><topic>Phosphatidylserines - genetics</topic><topic>Phosphatidylserines - metabolism</topic><topic>Photoperiod</topic><topic>Protein Kinases - genetics</topic><topic>Protein Kinases - metabolism</topic><topic>Seedlings - genetics</topic><topic>Seedlings - growth & development</topic><topic>Seedlings - metabolism</topic><topic>Seeds</topic><topic>Signal Transduction</topic><topic>Sphingosine N-Acyltransferase - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xie, Li-Juan</creatorcontrib><creatorcontrib>Chen, Qin-Fang</creatorcontrib><creatorcontrib>Chen, Mo-Xian</creatorcontrib><creatorcontrib>Yu, Lu-Jun</creatorcontrib><creatorcontrib>Huang, Li</creatorcontrib><creatorcontrib>Chen, Liang</creatorcontrib><creatorcontrib>Wang, Feng-Zhu</creatorcontrib><creatorcontrib>Xia, Fan-Nv</creatorcontrib><creatorcontrib>Zhu, Tian-Ren</creatorcontrib><creatorcontrib>Wu, Jian-Xin</creatorcontrib><creatorcontrib>Yin, Jian</creatorcontrib><creatorcontrib>Liao, Bin</creatorcontrib><creatorcontrib>Shi, Jianxin</creatorcontrib><creatorcontrib>Zhang, Jian-Hua</creatorcontrib><creatorcontrib>Aharoni, Asaph</creatorcontrib><creatorcontrib>Yao, Nan</creatorcontrib><creatorcontrib>Shu, Wensheng</creatorcontrib><creatorcontrib>Xiao, Shi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xie, Li-Juan</au><au>Chen, Qin-Fang</au><au>Chen, Mo-Xian</au><au>Yu, Lu-Jun</au><au>Huang, Li</au><au>Chen, Liang</au><au>Wang, Feng-Zhu</au><au>Xia, Fan-Nv</au><au>Zhu, Tian-Ren</au><au>Wu, Jian-Xin</au><au>Yin, Jian</au><au>Liao, Bin</au><au>Shi, Jianxin</au><au>Zhang, Jian-Hua</au><au>Aharoni, Asaph</au><au>Yao, Nan</au><au>Shu, Wensheng</au><au>Xiao, Shi</au><au>Yu, Hao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2015-03-01</date><risdate>2015</risdate><volume>11</volume><issue>3</issue><spage>e1005143</spage><epage>e1005143</epage><pages>e1005143-e1005143</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Lipid remodeling is crucial for hypoxic tolerance in animals, whilst little is known about the hypoxia-induced lipid dynamics in plants. Here we performed a mass spectrometry-based analysis to survey the lipid profiles of Arabidopsis rosettes under various hypoxic conditions. We observed that hypoxia caused a significant increase in total amounts of phosphatidylserine, phosphatidic acid and oxidized lipids, but a decrease in phosphatidylcholine (PC) and phosphatidylethanolamine (PE). Particularly, significant gains in the polyunsaturated species of PC, PE and phosphatidylinositol, and losses in their saturated and mono-unsaturated species were evident during hypoxia. Moreover, hypoxia led to a remarkable elevation of ceramides and hydroxyceramides. Disruption of ceramide synthases LOH1, LOH2 and LOH3 enhanced plant sensitivity to dark submergence, but displayed more resistance to submergence under light than wild type. Consistently, levels of unsaturated very-long-chain (VLC) ceramide species (22:1, 24:1 and 26:1) predominantly declined in the loh1, loh2 and loh3 mutants under dark submergence. In contrast, significant reduction of VLC ceramides in the loh1-1 loh3-1 knockdown double mutant and lacking of VLC unsaturated ceramides in the ads2 mutants impaired plant tolerance to both dark and light submergences. Evidence that C24:1-ceramide interacted with recombinant CTR1 protein and inhibited its kinase activity in vitro, enhanced ER-to-nucleus translocation of EIN2-GFP and stabilization of EIN3-GFP in vivo, suggests a role of ceramides in modulating CTR1-mediated ethylene signaling. The dark submergence-sensitive phenotypes of loh mutants were rescued by a ctr1-1 mutation. Thus, our findings demonstrate that unsaturation of VLC ceramides is a protective strategy for hypoxic tolerance in Arabidopsis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25822663</pmid><doi>10.1371/journal.pgen.1005143</doi><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis thaliana Cellular signal transduction Ceramides - genetics Ceramides - metabolism Ethylenes - metabolism Fatty acids Gene expression Genetic aspects Hypoxia - genetics Identification and classification Kinases Lipid Metabolism - genetics Lipids Liposomes - metabolism Phosphatidic Acids - metabolism Phosphatidylcholines - metabolism Phosphatidylethanolamines - metabolism Phosphatidylserines - genetics Phosphatidylserines - metabolism Photoperiod Protein Kinases - genetics Protein Kinases - metabolism Seedlings - genetics Seedlings - growth & development Seedlings - metabolism Seeds Signal Transduction Sphingosine N-Acyltransferase - genetics |
title | Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis |
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