title: Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis.
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.
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Li-Juan
authors.initials: LJ
authors.lastname: Xie
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Qin-Fang
authors.initials: QF
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, China.
authors.forename: Mo-Xian
authors.initials: MX
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Lu-Jun
authors.initials: LJ
authors.lastname: Yu
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Li
authors.initials: L
authors.lastname: Huang
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Liang
authors.initials: L
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Feng-Zhu
authors.initials: FZ
authors.lastname: Wang
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Fan-Nv
authors.initials: FN
authors.lastname: Xia
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Tian-Ren
authors.initials: TR
authors.lastname: Zhu
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Jian-Xin
authors.initials: JX
authors.lastname: Wu
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Jian
authors.initials: J
authors.lastname: Yin
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Bin
authors.initials: B
authors.lastname: Liao
authors.affiliation: School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
authors.forename: Jianxin
authors.initials: J
authors.lastname: Shi
authors.affiliation: State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, China.
authors.forename: Jian-Hua
authors.initials: JH
authors.lastname: Zhang
authors.affiliation: Department of Plant Sciences, Weizmann Institute of Science, Rehovot, Israel.
authors.forename: Asaph
authors.initials: A
authors.lastname: Aharoni
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Nan
authors.initials: N
authors.lastname: Yao
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Wensheng
authors.initials: W
authors.lastname: Shu
authors.affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
authors.forename: Shi
authors.initials: S
authors.lastname: Xiao
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D002518:Ceramides / Q000235:genetics* / Q000378:metabolism; D005030:Ethylenes / Q000378:metabolism; D000860:Hypoxia / Q000235:genetics; D050356:Lipid Metabolism / Q000235:genetics; D008081:Liposomes / Q000378:metabolism; D010712:Phosphatidic Acids / Q000378:metabolism; D010713:Phosphatidylcholines / Q000378:metabolism; D010714:Phosphatidylethanolamines / Q000378:metabolism; D010718:Phosphatidylserines / Q000235:genetics / Q000378:metabolism; D017440:Photoperiod; D011494:Protein Kinases / Q000235:genetics* / Q000378:metabolism; D036226:Seedlings / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D015398:Signal Transduction; D051049:Sphingosine N-Acyltransferase / Q000235:genetics*
chemical_list: D002518:Ceramides; D005030:Ethylenes; D008081:Liposomes; D010712:Phosphatidic Acids; D010713:Phosphatidylcholines; D010714:Phosphatidylethanolamines; D010718:Phosphatidylserines; C483858:phosphatidylethanolamine; C036216:ethylene; D051049:Sphingosine N-Acyltransferase; D011494:Protein Kinases; C477753:CTR1 protein, Arabidopsis
references.citation: Biochim Biophys Acta. 2003 May 2;1612(1):98-106
references.pmid: 12729935
references.citation: Curr Opin Plant Biol. 2013 Oct;16(5):647-53
references.pmid: 23830867
references.citation: Rapid Commun Mass Spectrom. 2007;21(7):1304-14
references.pmid: 17340572
references.citation: Plant Cell. 2011 Jun;23(6):2362-78
references.pmid: 21666002
references.citation: Science. 2009 Apr 17;324(5925):343-4
references.pmid: 19372418
references.citation: Plant Sci. 2013 Sep;210:93-107
references.pmid: 23849117
references.citation: J Lipid Res. 2012 Aug;53(8):1513-21
references.pmid: 22615346
references.citation: Cell. 1993 Feb 12;72(3):427-41
references.pmid: 8431946
references.citation: Plant Mol Biol. 1995 Nov;29(3):599-609
references.pmid: 8534855
references.citation: Plant J. 2009 Apr;58(1):122-34
references.pmid: 19054355
references.citation: Cell. 1997 Apr 4;89(1):63-72
references.pmid: 9094715
references.citation: Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16475-80
references.pmid: 21930922
references.citation: J Biol Chem. 1996 Apr 5;271(14):8472-80
references.pmid: 8626548
references.citation: Plant Physiol. 2014 Apr 21;165(2):774-790
references.pmid: 24753539
references.citation: Plant Physiol. 1989 Sep;91(1):401-8
references.pmid: 16667033
references.citation: New Phytol. 2012 Dec;196(4):1086-1097
references.pmid: 23025549
references.citation: Curr Opin Plant Biol. 2003 Jun;6(3):247-56
references.pmid: 12753974
references.citation: New Phytol. 2004 Mar;161(3):677-702
references.pmid: 33873728
references.citation: Science. 2002 Jun 14;296(5575):2026-8
references.pmid: 12065837
references.citation: J Biol Chem. 2009 May 22;284(21):14469-75
references.pmid: 19304661
references.citation: J Exp Bot. 2007;58(14):3905-14
references.pmid: 18000017
references.citation: Biotechnol Lett. 2008 Jun;30(6):967-77
references.pmid: 18227974
references.citation: Nature. 2011 Oct 23;479(7373):419-22
references.pmid: 22020282
references.citation: Trends Plant Sci. 2003 Jul;8(7):317-20
references.pmid: 12878015
references.citation: Plant Cell. 2013 Dec;25(12):5030-42
references.pmid: 24368785
references.citation: Trends Plant Sci. 2004 Sep;9(9):449-56
references.pmid: 15337495
references.citation: Plant J. 2005 Nov;44(3):361-71
references.pmid: 16236147
references.citation: Plant J. 2015 Jan;81(1):53-67
references.pmid: 25284079
references.citation: Plant Physiol. 1997 Nov;115(3):875-879
references.pmid: 12223851
references.citation: Plant Biol (Stuttg). 2013 May;15(3):426-35
references.pmid: 23574304
references.citation: Science. 2012 Oct 19;338(6105):390-3
references.pmid: 22936567
references.citation: J Biol Chem. 1999 Jul 16;274(29):20313-7
references.pmid: 10400653
references.citation: Arabidopsis Book. 2013;11:e0161
references.pmid: 23505340
references.citation: New Phytol. 2011 Apr;190(2):457-71
references.pmid: 21231933
references.citation: J Biol Chem. 2010 Mar 12;285(11):7964-76
references.pmid: 20068046
references.citation: Plant Physiol. 2005 Mar;137(3):1115-29
references.pmid: 15734912
references.citation: Cell Res. 2012 Nov;22(11):1613-6
references.pmid: 23070300
references.citation: Ann Bot. 2005 Sep;96(4):661-8
references.pmid: 16033780
references.citation: Plant Physiol. 2011 Aug;156(4):2069-81
references.pmid: 21670223
references.citation: Science. 2000 Jan 21;287(5452):476-9
references.pmid: 10642547
references.citation: Science. 2009 Apr 17;324(5925):381-4
references.pmid: 19372430
references.citation: Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):6959-63
references.pmid: 8692926
references.citation: Curr Opin Plant Biol. 2004 Jun;7(3):329-36
references.pmid: 15134755
references.citation: Plant Physiol. 2013 Jan;161(1):81-96
references.pmid: 23175755
references.citation: Methods Mol Biol. 2013;1009:93-101
references.pmid: 23681527
references.citation: Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19486-91
references.pmid: 23132950
references.citation: Phytochemistry. 2006 Sep;67(17):1907-24
references.pmid: 16843506
references.citation: Plant Cell. 2013 Sep;25(9):3186-211
references.pmid: 24014546
references.citation: Prog Lipid Res. 2011 Apr;50(2):141-51
references.pmid: 21144863
references.citation: Plant Physiol. 2005 Mar;137(3):1130-8
references.pmid: 15734908
references.citation: Plant Cell. 2011 Nov;23(11):3944-60
references.pmid: 22108404
references.citation: Plant Physiol. 2011 May;156(1):202-12
references.pmid: 21398256
references.citation: Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5401-6
references.pmid: 9560288
references.citation: Plant Cell. 2010 May;22(5):1463-82
references.pmid: 20442372
references.citation: New Phytol. 2010 Jun;186(4):781-783
references.pmid: 20569412
references.citation: J Biol Chem. 2002 Aug 30;277(35):31994-2002
references.pmid: 12077151
references.citation: J Biol Chem. 2006 Aug 11;281(32):22684-94
references.pmid: 16772288
references.citation: Plant Physiol. 2007 Aug;144(4):1968-77
references.pmid: 17600137
references.citation: New Phytol. 2011 Dec;192(4):841-854
references.pmid: 21883234
references.citation: Plant Cell. 2010 Feb;22(2):364-75
references.pmid: 20145257
references.citation: Genes Dev. 2003 Nov 1;17(21):2636-41
references.pmid: 14563678
references.citation: Ann Bot. 2005 Sep;96(4):647-60
references.pmid: 16081496
references.citation: Plant Cell. 2011 Dec;23(12):4173-83
references.pmid: 22207573
references.citation: J Biol Chem. 2007 Apr 27;282(17):12450-7
references.pmid: 17308302
references.citation: Plant Cell. 2009 Aug;21(8):2357-77
references.pmid: 19690149
references.citation: Plant J. 2008 Dec;56(5):743-55
references.pmid: 18665916
references.citation: New Phytol. 2011 Apr;190(2):442-56
references.pmid: 20840511
references.citation: Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9814-9
references.pmid: 16782814
references.citation: PLoS One. 2012;7(1):e30355
references.pmid: 22279586
references.citation: Biochim Biophys Acta. 2003 Jun 10;1632(1-3):1-15
references.pmid: 12782146
references.citation: Trends Plant Sci. 2012 Mar;17(3):129-38
references.pmid: 22280796
references.citation: J Biol Chem. 2011 Nov 4;286(44):38069-38078
references.pmid: 21914808
references.citation: Front Plant Sci. 2012 Apr 10;3:68
references.pmid: 22639658
references.citation: Plant Cell. 2008 Jul;20(7):1862-78
references.pmid: 18612100
references.citation: Nature. 2011 Oct 23;479(7373):415-8
references.pmid: 22020279
references.citation: Plant Physiol. 2014 Feb;164(2):570-83
references.pmid: 24368335
references.citation: Curr Opin Plant Biol. 2013 Jun;16(3):350-7
references.pmid: 23499054
references.citation: New Phytol. 2014 Jul;203(1):310-22
references.pmid: 24684726
references.citation: Plant Cell. 2008 Nov;20(11):3163-79
references.pmid: 19001565
references.citation: EMBO J. 1998 Feb 2;17(3):732-42
references.pmid: 9450998
references.citation: Prog Lipid Res. 2003 Nov;42(6):527-43
references.pmid: 14559070
references.citation: Cell Signal. 2010 Apr;22(4):610-8
references.pmid: 19932170
references.citation: Plant J. 2012 Mar;69(5):769-81
references.pmid: 22023480
references.citation: Proc Natl Acad Sci U S A. 2013 May 28;110(22):8882-7
references.pmid: 23671091
references.citation: Plant Cell. 2013 Apr;25(4):1430-44
references.pmid: 23585650
references.citation: BMC Plant Biol. 2004 Sep 17;4:17
references.pmid: 15377388