鞘脂在植物-真菌互作中的分子调控机制研究进展
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摘要
鞘脂是细胞生物膜结构的重要组分,鞘脂及其代谢产物参与许多重要的信号转导过程。在植物-真菌互作中,植物鞘脂的主要作用是诱导细胞发生程序性死亡;真菌鞘脂既能引起植物死亡,也能诱导植物产生抗病性。该文总结了植物和真菌鞘脂的结构及代谢特点,综述了鞘脂参与调控植物-真菌互作的分子机制研究进展,并展望了植物-真菌共生关系中鞘脂作用的研究方向。
Sphingolipids are essential components of cell membranes and take part in many critical processes of signal transduction. In plant-fungus interactions, plant sphingolipids mainly induce programmed cell death, whereas fungus sphingolipids induce plant death or plant disease resistance. In this paper, we summarize the structure and metabolic characteristics of plant and fungus sphingolipids as well as advances in the molecular regulation of sphingolipids in plant-fungus interactions. Moreover, the research direction of the role of sphingolipids in plant-fungus symbiosis is also prospected.
Sphingolipids are essential components of cell membranes and take part in many critical processes of signal transduction. In plant-fungus interactions, plant sphingolipids mainly induce programmed cell death, whereas fungus sphingolipids induce plant death or plant disease resistance. In this paper, we summarize the structure and metabolic characteristics of plant and fungus sphingolipids as well as advances in the molecular regulation of sphingolipids in plant-fungus interactions. Moreover, the research direction of the role of sphingolipids in plant-fungus symbiosis is also prospected.
引文
郭顺星(2016).药用植物内生真菌生物学.北京:科学出版社.pp.190-191.
林久生,王根轩(2001).活性氧与植物细胞编程性死亡.植物生理学通讯37,551-555.
刘润华,江文波,余迪求(2009).植物鞘脂的结构、代谢途径及其功能.植物学报44,619-628.
田磊,李元敬,何兴元,田春杰(2016).丛枝菌根真菌脂类代谢对共生信号调控的响应和反馈.微生物学报56,26-34.
张海涵(2011).黄土高原枸杞根际微生态特征及其共生真菌调控宿主生长与耐旱响应机制.博士论文.杨凌:西北农林科技大学.pp.38-40.
Aerts AM,Fran?ois IEJA,Bammens L,Cammue BPA,Smets B,Winderickx J,Accardo S,De Vos DE,Thevissen K(2006).Level of M(IP)2C sphingolipid affects plant defensin sensitivity,oxidative stress resistance and chronological life-span in yeast.FEBS Lett 580,1903-1907.
Arora P,Porcelli SA(2008).A glycan shield for bacterial sphingolipids.Chem Biol 15,642-644.
Barreto-Bergter E,Sassaki GL,De Souza LM(2011).Structural analysis of fungal cerebrosides.Front Microbiol2,239.
Bi FC,Liu Z,Wu JX,Liang H,Xi XL,Fang C,Sun TJ,Yin J,Dai GY,Rong C,Greenberg JT,Su WW,Yao N(2014).Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts.Plant Cell 26,3449-3467.
Brandwagt BF,Kneppers TJA,Nijkamp HJJ,Hille J(2002).Overexpression of the tomato ASC-1 gene mediates high insensitivity to AAL toxins and fumonisin B1 in tomato hairy roots and confers resistance to Alternaria alternata f.sp.lycopersici in Nicotiana umbratica plants.Mol Plant Microbe Interact 15,35-42.
Chen M,Markham JE,Cahoon EB(2012).Sphingolipid?8unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis.Plant J 69,769-781.
De Zélicourt A,Montiel G,Pouvreau JB,Thoiron S,Delgrange S,Simier P,Delavault P(2009).Susceptibility of Phelipanche and Orobanche species to AAL-toxin.Planta230,1047-1055.
Deepak SA,Raj SN,Umemura K,Kono T,Shetty HS(2003).Cerebroside as an elicitor for induced resistance against the downy mildew pathogen in pearl millet.Ann Appl Biol 143,169-173.
Healey KR,Challa KK,Edlind TD,Katiyar SK(2015).Sphingolipids mediate differential echinocandin susceptibility in Candida albicans and Aspergillus nidulans.Anti microb Agents Chemother 59,3377-3384.
Hechtberger P,Zinser E,Saf R,Hummel K,Paltauf F,Daum G(1994).Characterization,quantification and subcellular localization of inositol-containing sphingolipids of the yeast,Saccharomyces cerevisiae.Eur J Biochem225,641-649.
Lachaud C,Silva DD,Cotelle V,Thuleau P,Xiong TC,Jauneau A,Brière C,Graziana A,Bellec Y,Faure JD,Ranjeva R,Mazars C(2010).Nuclear calcium controls the apoptotic-like cell death induced by D-erythro-sphinganine in tobacco cells.Cell Calcium 47,92-100.
Lindahl L,Santos AXS,Olsson H,Olsson L,Bettiga M(2017).Membrane engineering of S.cerevisiae targeting sphingolipid metabolism.Sci Rep 7,41868.
Magnin-Robert M,Le Bourse D,Markham J,Dorey S,Clément C,Baillieul F,Dhondt-Cordelier S(2015).Modifications of sphingolipid content affect tolerance to hemibiotrophic and necrotrophic pathogens by modulating plant defense responses in Arabidopsis.Plant Physiol169,2255-2274.
Maillet F,Poinsot V,AndréO,Puech-Pagès V,Haouy A,Gueunier M,Cromer L,Giraudet D,Formey D,Niebel A,Martinez EA,Driguez H,Bécard G,DénariéJ(2011).Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.Nature 469,58-63.
Markham JE,Lynch DV,Napier JA,Dunn TM,Cahoon EB(2013).Plant sphingolipids:function follows form.Curr Opin Plant Biol 16,350-357.
Michaelson LV,Napier JA,Molino D,Faure JD(2016).Plant sphingolipids:their importance in cellular organization and adaption.Biochim Biophys Acta 1861,1329-1335.
Mortimer JC,Yu X,Albrecht S,Sicilia F,Huichalaf M,Ampuero D,Michaelson LV,Murphy AM,Matsunaga T,Kurz S,Stephens E,Baldwin TC,Ishii T,Napier JA,Weber APM,Handford MG,Dupree P(2013).Abnormal glycosphingolipid mannosylation triggers salicylic acid mediated responses in Arabidopsis.Plant Cell 25,1881-1894.
Oguro Y,Yamazaki H,Takagi M,Takaku H(2014).Antifungal activity of plant defensin AFP1 in Brassica juncea involves the recognition of the methyl residue in glucosylceramide of target pathogen Candida albicans.Curr Genet 60,89-97.
Olsen I,Jantzen E(2001).Sphingolipids in bacteria and fungi.Anaerobe 7,103-112.
Peer M,Stegmann M,Mueller MJ,Waller F(2010).Pseudomonas syringae infection triggers de novo synthesis of phytosphingosine from sphinganine in Arabidopsis thaliana.FEBS Lett 584,4053-4056.
Ramamoorthy V,Cahoon EB,Li J,Thokala M,Minto RE,Shah DM(2007).Glucosylceramide synthase is essential for alfalfa defensin-mediated growth inhibition but not for pathogenicity of Fusarium graminearum.Mol Microbiol 66,771-786.
Ramamoorthy V,Cahoon EB,Thokala M,Kaur J,Li J,Shah DM(2009).Sphingolipid C-9 methyltransferases are important for growth and virulence but not for sensitivity to antifungal plant defensins in Fusarium graminearum.Eukaryot Cell 8,217-229.
Rittershaus PC,Kechichian TB,Allegood JC,Merrill AH,Hennig M,Luberto C,Del Poeta M(2006).Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans.J Clin Invest 116,1651-1659.
Rollin-Pinheiro R,Singh A,Barreto-Bergter E,Poeta MD(2016).Sphingolipids as targets for treatment of fungal infections.Future Med Chem 8,1469-1484.
Saucedo-García M,Guevara-García A,González-Solís A,Cruz-García F,Vázquez-Santana S,Markham JE,Guadalupe Lozano-Rosas M,Dietrich CR,Ramos-Vega M,Cahoon EB,Gavilanes-Ruíz M(2011).MPK6,sphinganine and the LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis.New Phytol 191,943-957.
Sharma L,Prakash H(2017).Sphingolipids are dual specific drug targets for the management of pulmonary infections:perspective.Front Immunol 8,378.
Shi LH,Bielawski J,Mu JY,Dong HL,Teng C,Zhang J,Yang XH,Tomishige N,Hanada K,Hannun YA,Zuo J(2007).Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis.Cell Res 17,1030-1040.
Siebers M,Brands M,Wewer V,Duan YJ,H?lzl G,D?rmann P(2016).Lipids in plant-microbe interactions.Biochim Biophys Acta 1861,1379-1395.
Spassieva SD,Markham JE,Hille J(2002).The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death.Plant J 32,561-572.
Tani Y,Amaishi Y,Funatsu T,Ito M,Itonor S,Hata Y,Ashida H,Yamamoto K(2014).Structural analysis of cerebrosides from Aspergillus fungi:the existence of galactosylceramide in A.oryzae.Biotechnol Lett 36,2507-2513.
Tartaglio V,Rennie EA,Cahoon R,Wang G,Baidoo E,Mortimer JC,Cahoon EB,Scheller HV(2017).Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidosis.Plant J 89,278-290.
Thevissen K,Fran?ois IEJA,Takemoto JY,Ferket KKA,Meert EMK,Cammue BPA(2003).Dm AMP1,an antifungal plant defensin from dahlia(Dahlia merckii),interacts with sphingolipids from Saccharomyces cerevisiae.FEMS Microbiol Lett 226,169-173.
Thevissen K,Warnecke DC,Fran?ois IEJA,Leipelt M,Heinz E,Ott C,Z?hringer U,Thomma BPHJ,Ferket KKA,Cammue BPA(2004).Defensins from insects and plants interact with fungal glucosylceramides.J Biol Chem279,3900-3905.
Townley HE,Mc Donald K,Jenkins GI,Knight MR,Leaver CJ(2005).Ceramides induce programmed cell death in Arabidopsis cells in a calcium-dependent manner.Biol Chem 386,161-166.
Ueda N(2017).Sphingolipids in genetic and acquired forms of chronic kidney diseases.Curr Med Chem 24,1238-1275.
Umemura K,Ogawa N,Koga J,Iwata M,Usami H(2002).Elicitor activity of cerebroside,a sphingolipid elicitor,in cell suspension cultures of rice.Plant Cell Physiol 43,778-784.
Umemura K,Ogawa N,Yamauchi T,Iwata M,Shimura M,Koga J(2000).Cerebroside elicitors found in diverse phytopathogens activate defense responses in rice plants.Plant Cell Physiol 41,676-683.
Virolainen E,Blokhina O,Fagerstedt K(2002).Ca2+-induced high amplitude swelling and cytochrome c release from wheat(Triticum aestivum L.)mitochondria under anoxic stress.Ann Bot 90,509-516.
Wang WM,Yang XH,Tangchaiburana S,Ndeh R,Markham JE,Tsegaye Y,Dun TM,Wang GL,Bellizzi M,Parsons JF,Morrissey D,Bravo JE,Lynch DV,Xiao SY(2008).An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis.Plant Cell 20,3163-3179.
Warnecke D,Heinz E(2003).Recently discovered functions of glucosylceramides in plants and fungi.Cell Mol Life Sci60,919-941.
Yanagawa D,Ishikawa T,Imai H(2017).Synthesis and degradation of long-chain base phosphates affect fumonisin B1-induced cell death in Arabidopsis thaliana.JPlant Res 130,571-585.
Zhu CY,Wang MS,Wang WL,Ruan RJ,Ma HJ,Mao CG,Li HY(2014).Glucosylceramides are required for mycelial growth and full virulence in Penicillium digitatum.Biochem Biophys Res Commun 455,165-171.
林久生,王根轩(2001).活性氧与植物细胞编程性死亡.植物生理学通讯37,551-555.
刘润华,江文波,余迪求(2009).植物鞘脂的结构、代谢途径及其功能.植物学报44,619-628.
田磊,李元敬,何兴元,田春杰(2016).丛枝菌根真菌脂类代谢对共生信号调控的响应和反馈.微生物学报56,26-34.
张海涵(2011).黄土高原枸杞根际微生态特征及其共生真菌调控宿主生长与耐旱响应机制.博士论文.杨凌:西北农林科技大学.pp.38-40.
Aerts AM,Fran?ois IEJA,Bammens L,Cammue BPA,Smets B,Winderickx J,Accardo S,De Vos DE,Thevissen K(2006).Level of M(IP)2C sphingolipid affects plant defensin sensitivity,oxidative stress resistance and chronological life-span in yeast.FEBS Lett 580,1903-1907.
Arora P,Porcelli SA(2008).A glycan shield for bacterial sphingolipids.Chem Biol 15,642-644.
Barreto-Bergter E,Sassaki GL,De Souza LM(2011).Structural analysis of fungal cerebrosides.Front Microbiol2,239.
Bi FC,Liu Z,Wu JX,Liang H,Xi XL,Fang C,Sun TJ,Yin J,Dai GY,Rong C,Greenberg JT,Su WW,Yao N(2014).Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts.Plant Cell 26,3449-3467.
Brandwagt BF,Kneppers TJA,Nijkamp HJJ,Hille J(2002).Overexpression of the tomato ASC-1 gene mediates high insensitivity to AAL toxins and fumonisin B1 in tomato hairy roots and confers resistance to Alternaria alternata f.sp.lycopersici in Nicotiana umbratica plants.Mol Plant Microbe Interact 15,35-42.
Chen M,Markham JE,Cahoon EB(2012).Sphingolipid?8unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis.Plant J 69,769-781.
De Zélicourt A,Montiel G,Pouvreau JB,Thoiron S,Delgrange S,Simier P,Delavault P(2009).Susceptibility of Phelipanche and Orobanche species to AAL-toxin.Planta230,1047-1055.
Deepak SA,Raj SN,Umemura K,Kono T,Shetty HS(2003).Cerebroside as an elicitor for induced resistance against the downy mildew pathogen in pearl millet.Ann Appl Biol 143,169-173.
Healey KR,Challa KK,Edlind TD,Katiyar SK(2015).Sphingolipids mediate differential echinocandin susceptibility in Candida albicans and Aspergillus nidulans.Anti microb Agents Chemother 59,3377-3384.
Hechtberger P,Zinser E,Saf R,Hummel K,Paltauf F,Daum G(1994).Characterization,quantification and subcellular localization of inositol-containing sphingolipids of the yeast,Saccharomyces cerevisiae.Eur J Biochem225,641-649.
Lachaud C,Silva DD,Cotelle V,Thuleau P,Xiong TC,Jauneau A,Brière C,Graziana A,Bellec Y,Faure JD,Ranjeva R,Mazars C(2010).Nuclear calcium controls the apoptotic-like cell death induced by D-erythro-sphinganine in tobacco cells.Cell Calcium 47,92-100.
Lindahl L,Santos AXS,Olsson H,Olsson L,Bettiga M(2017).Membrane engineering of S.cerevisiae targeting sphingolipid metabolism.Sci Rep 7,41868.
Magnin-Robert M,Le Bourse D,Markham J,Dorey S,Clément C,Baillieul F,Dhondt-Cordelier S(2015).Modifications of sphingolipid content affect tolerance to hemibiotrophic and necrotrophic pathogens by modulating plant defense responses in Arabidopsis.Plant Physiol169,2255-2274.
Maillet F,Poinsot V,AndréO,Puech-Pagès V,Haouy A,Gueunier M,Cromer L,Giraudet D,Formey D,Niebel A,Martinez EA,Driguez H,Bécard G,DénariéJ(2011).Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza.Nature 469,58-63.
Markham JE,Lynch DV,Napier JA,Dunn TM,Cahoon EB(2013).Plant sphingolipids:function follows form.Curr Opin Plant Biol 16,350-357.
Michaelson LV,Napier JA,Molino D,Faure JD(2016).Plant sphingolipids:their importance in cellular organization and adaption.Biochim Biophys Acta 1861,1329-1335.
Mortimer JC,Yu X,Albrecht S,Sicilia F,Huichalaf M,Ampuero D,Michaelson LV,Murphy AM,Matsunaga T,Kurz S,Stephens E,Baldwin TC,Ishii T,Napier JA,Weber APM,Handford MG,Dupree P(2013).Abnormal glycosphingolipid mannosylation triggers salicylic acid mediated responses in Arabidopsis.Plant Cell 25,1881-1894.
Oguro Y,Yamazaki H,Takagi M,Takaku H(2014).Antifungal activity of plant defensin AFP1 in Brassica juncea involves the recognition of the methyl residue in glucosylceramide of target pathogen Candida albicans.Curr Genet 60,89-97.
Olsen I,Jantzen E(2001).Sphingolipids in bacteria and fungi.Anaerobe 7,103-112.
Peer M,Stegmann M,Mueller MJ,Waller F(2010).Pseudomonas syringae infection triggers de novo synthesis of phytosphingosine from sphinganine in Arabidopsis thaliana.FEBS Lett 584,4053-4056.
Ramamoorthy V,Cahoon EB,Li J,Thokala M,Minto RE,Shah DM(2007).Glucosylceramide synthase is essential for alfalfa defensin-mediated growth inhibition but not for pathogenicity of Fusarium graminearum.Mol Microbiol 66,771-786.
Ramamoorthy V,Cahoon EB,Thokala M,Kaur J,Li J,Shah DM(2009).Sphingolipid C-9 methyltransferases are important for growth and virulence but not for sensitivity to antifungal plant defensins in Fusarium graminearum.Eukaryot Cell 8,217-229.
Rittershaus PC,Kechichian TB,Allegood JC,Merrill AH,Hennig M,Luberto C,Del Poeta M(2006).Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans.J Clin Invest 116,1651-1659.
Rollin-Pinheiro R,Singh A,Barreto-Bergter E,Poeta MD(2016).Sphingolipids as targets for treatment of fungal infections.Future Med Chem 8,1469-1484.
Saucedo-García M,Guevara-García A,González-Solís A,Cruz-García F,Vázquez-Santana S,Markham JE,Guadalupe Lozano-Rosas M,Dietrich CR,Ramos-Vega M,Cahoon EB,Gavilanes-Ruíz M(2011).MPK6,sphinganine and the LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis.New Phytol 191,943-957.
Sharma L,Prakash H(2017).Sphingolipids are dual specific drug targets for the management of pulmonary infections:perspective.Front Immunol 8,378.
Shi LH,Bielawski J,Mu JY,Dong HL,Teng C,Zhang J,Yang XH,Tomishige N,Hanada K,Hannun YA,Zuo J(2007).Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis.Cell Res 17,1030-1040.
Siebers M,Brands M,Wewer V,Duan YJ,H?lzl G,D?rmann P(2016).Lipids in plant-microbe interactions.Biochim Biophys Acta 1861,1379-1395.
Spassieva SD,Markham JE,Hille J(2002).The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death.Plant J 32,561-572.
Tani Y,Amaishi Y,Funatsu T,Ito M,Itonor S,Hata Y,Ashida H,Yamamoto K(2014).Structural analysis of cerebrosides from Aspergillus fungi:the existence of galactosylceramide in A.oryzae.Biotechnol Lett 36,2507-2513.
Tartaglio V,Rennie EA,Cahoon R,Wang G,Baidoo E,Mortimer JC,Cahoon EB,Scheller HV(2017).Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidosis.Plant J 89,278-290.
Thevissen K,Fran?ois IEJA,Takemoto JY,Ferket KKA,Meert EMK,Cammue BPA(2003).Dm AMP1,an antifungal plant defensin from dahlia(Dahlia merckii),interacts with sphingolipids from Saccharomyces cerevisiae.FEMS Microbiol Lett 226,169-173.
Thevissen K,Warnecke DC,Fran?ois IEJA,Leipelt M,Heinz E,Ott C,Z?hringer U,Thomma BPHJ,Ferket KKA,Cammue BPA(2004).Defensins from insects and plants interact with fungal glucosylceramides.J Biol Chem279,3900-3905.
Townley HE,Mc Donald K,Jenkins GI,Knight MR,Leaver CJ(2005).Ceramides induce programmed cell death in Arabidopsis cells in a calcium-dependent manner.Biol Chem 386,161-166.
Ueda N(2017).Sphingolipids in genetic and acquired forms of chronic kidney diseases.Curr Med Chem 24,1238-1275.
Umemura K,Ogawa N,Koga J,Iwata M,Usami H(2002).Elicitor activity of cerebroside,a sphingolipid elicitor,in cell suspension cultures of rice.Plant Cell Physiol 43,778-784.
Umemura K,Ogawa N,Yamauchi T,Iwata M,Shimura M,Koga J(2000).Cerebroside elicitors found in diverse phytopathogens activate defense responses in rice plants.Plant Cell Physiol 41,676-683.
Virolainen E,Blokhina O,Fagerstedt K(2002).Ca2+-induced high amplitude swelling and cytochrome c release from wheat(Triticum aestivum L.)mitochondria under anoxic stress.Ann Bot 90,509-516.
Wang WM,Yang XH,Tangchaiburana S,Ndeh R,Markham JE,Tsegaye Y,Dun TM,Wang GL,Bellizzi M,Parsons JF,Morrissey D,Bravo JE,Lynch DV,Xiao SY(2008).An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis.Plant Cell 20,3163-3179.
Warnecke D,Heinz E(2003).Recently discovered functions of glucosylceramides in plants and fungi.Cell Mol Life Sci60,919-941.
Yanagawa D,Ishikawa T,Imai H(2017).Synthesis and degradation of long-chain base phosphates affect fumonisin B1-induced cell death in Arabidopsis thaliana.JPlant Res 130,571-585.
Zhu CY,Wang MS,Wang WL,Ruan RJ,Ma HJ,Mao CG,Li HY(2014).Glucosylceramides are required for mycelial growth and full virulence in Penicillium digitatum.Biochem Biophys Res Commun 455,165-171.