Trehalose phosphate synthase 5-dependent trehalose metabolism modulates basal defense responses in Arabidopsis thaliana
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摘要
Despite the recent discovery that trehalose synthesis is important for plant development and abiotic stress tolerance, the effects of trehalose on biotic stress responses remain relatively unknown. In this study, we demonstrate that TREHALOSE PHOSPHATE SYNTHASE 5(TPS5)-dependent trehalose metabolism regulates Arabidopsis thaliana defenses against pathogens(necrotrophic Botrytis cinerea and biotrophic Pseudomonas syringae).Pathogen infection increased trehalose levels and upregulated TPS5 expression. Application of exogenous trehalose significantly improved plant defenses against B. cinerea, but increased the susceptibility of plants to P. syringae. We demonstrate that elevated trehalose biosynthesis, in transgenic plants over-expressing TPS5, also increased the susceptibility to P. syringae, but decreased the disease elcit r symptoms caused by B. cinerea. The knockout of TPS5 prevented the accumulation of trehalose and enhanced defense responses against P. syringae. Additionally, we observed that a TPS5-interacting protein(multiprotein bridging factor 1c) was required for induced expression of TPS5 during pathogen infections. Furthermore, we show that trehalose promotes P. syringae growth and disease development, via a mechanism involving suppression of the plant defense gene, Pathogenesis-Related Protein 1. These findings provide insight into the function of TPS5-dependent trehalose metabolism in plant basal defense responses.
Despite the recent discovery that trehalose synthesis is important for plant development and abiotic stress tolerance, the effects of trehalose on biotic stress responses remain relatively unknown. In this study, we demonstrate that TREHALOSE PHOSPHATE SYNTHASE 5(TPS5)-dependent trehalose metabolism regulates Arabidopsis thaliana defenses against pathogens(necrotrophic Botrytis cinerea and biotrophic Pseudomonas syringae).Pathogen infection increased trehalose levels and upregulated TPS5 expression. Application of exogenous trehalose significantly improved plant defenses against B. cinerea, but increased the susceptibility of plants to P. syringae. We demonstrate that elevated trehalose biosynthesis, in transgenic plants over-expressing TPS5, also increased the susceptibility to P. syringae, but decreased the disease elcit r symptoms caused by B. cinerea. The knockout of TPS5 prevented the accumulation of trehalose and enhanced defense responses against P. syringae. Additionally, we observed that a TPS5-interacting protein(multiprotein bridging factor 1c) was required for induced expression of TPS5 during pathogen infections. Furthermore, we show that trehalose promotes P. syringae growth and disease development, via a mechanism involving suppression of the plant defense gene, Pathogenesis-Related Protein 1. These findings provide insight into the function of TPS5-dependent trehalose metabolism in plant basal defense responses.
Despite the recent discovery that trehalose synthesis is important for plant development and abiotic stress tolerance, the effects of trehalose on biotic stress responses remain relatively unknown. In this study, we demonstrate that TREHALOSE PHOSPHATE SYNTHASE 5(TPS5)-dependent trehalose metabolism regulates Arabidopsis thaliana defenses against pathogens(necrotrophic Botrytis cinerea and biotrophic Pseudomonas syringae).Pathogen infection increased trehalose levels and upregulated TPS5 expression. Application of exogenous trehalose significantly improved plant defenses against B. cinerea, but increased the susceptibility of plants to P. syringae. We demonstrate that elevated trehalose biosynthesis, in transgenic plants over-expressing TPS5, also increased the susceptibility to P. syringae, but decreased the disease elcit r symptoms caused by B. cinerea. The knockout of TPS5 prevented the accumulation of trehalose and enhanced defense responses against P. syringae. Additionally, we observed that a TPS5-interacting protein(multiprotein bridging factor 1c) was required for induced expression of TPS5 during pathogen infections. Furthermore, we show that trehalose promotes P. syringae growth and disease development, via a mechanism involving suppression of the plant defense gene, Pathogenesis-Related Protein 1. These findings provide insight into the function of TPS5-dependent trehalose metabolism in plant basal defense responses.
引文
Argueso CT,Ferreira FJ,Epple P,To JP,Hutchison CE,Schaller GE,Dangl JL,Kieber JJ(2012)Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity.PLoS Genet 8:e1002448
Avonce N,Leyman B,Mascorro-Gallardo JO,Van Dijck P,Thevelein JM,Iturriaga G(2004)The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose,abscisic acid,and stress signaling.Plant Physiol 136:3649-3659
Avonce N,Mendoza-Vargas A,Morett E,Iturriaga G(2006)Insights on the evolution of trehalose biosynthesis.BMCEvol Biol 6:109
Bae H,Herman E,Bailey B,Bae HJ,Sicher R(2005)Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification,abiotic stress,nitrogen metabolism,and plant defense.Physiol Plant 125:114-126
Berrocal-Lobo M,Molina A(2004)Ethylene response factor 1mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum.Mol Plant Microbe Interact 17:763-770
Brodmann A,Schuller A,Ludwig-M€uller J,Aeschbacher RA,Wiemken A,Boller T,Wingler A(2002)Induction of trehalase in Arabidopsis plants infected with the trehaloseproducing pathogen Plasmodiophora brassicae.Mol Plant Microbe Interact 15:693-700
Chary SN,Hicks GR,Choi YG,Carter D,Raikhel NV(2008)Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis.Plant Physiol 146:97-107
Clough SJ,Bent AF(1998)Floral dip:A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Plant J 16:735-743
Cui F,Wu S,Sun W,Coaker G,Kunkel B,He P,Shan L(2013)The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover.Plant Physiol 162:1018-1029
Dean R,Van Kan JA,Pretorius ZA,Hammond-Kosack KE,Di Pietro A,Spanu PD,Rudd JJ,Dickman M,Kahmann R,Ellis J(2012)The Top 10 fungal pathogens in molecular plant pathology.Mol Plant Pathol 13:414-430
Djonovic S,Urbach JM,Drenkard E,Bush J,Feinbaum R,Ausubel JL,Traficante D,Risech M,Kocks C,Fischbach MA(2013)Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants.PLoS Pathog 9:e1003217
Eastmond PJ,Graham IA(2003)Trehalose metabolism:Aregulatory role for trehalose-6-phosphate?Curr Opin Plant Biol 6:231-235
Eastmond PJ,Van Dijken AJ,Spielman M,Kerr A,Tissier AF,Dickinson HG,Jones JD,Smeekens SC,Graham IA(2002)Trehalose-6-phosphate synthase 1,which catalyses the first step in trehalose synthesis,is essential for Arabidopsis embryo maturation.Plant J 29:225-235
Fernandez O,Bethencourt L,Quero A,Sangwan RS,Clement C(2010)Trehalose and plant stress responses:Friend or foe?Trends Plant Sci 15:409-417
Foster AJ,Jenkinson JM,Talbot NJ(2003)Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea.EMBO J 22:225-235
Fritzius T,Aeschbacher R,Wiemken A,Wingler A(2001)Induction of ApL3 expression by trehalose complements the starch-deficient Arabidopsis mutantadg2-1 lacking ApL1,the large subunit of ADP-glucose pyrophosphorylase.Plant Physiol 126:883-889
Gomez-Ariza J,Campo S,Rufat M,Estopa M,Messeguer J,Segundo BS,Coca M(2007)Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesisrelated PRms protein in rice plants.Mol Plant Microbe Interact 20:832-842
Gimenez-Ibanez S,Solano R(2013)Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens.Front Plant Sci 4:72
Govind SR,Jogaiah S,Abdelrahman M,Shetty HS,Tran L-SP(2016)Exogenous trehalose treatment enhances the activities of defense-related enzymes and triggers resistance against downy mildew disease of pearl millet.Front Plant Sci 7:1593
Gravot A,Grillet L,Wagner G,Jubault M,Lariagon C,Baron C,Deleu C,Delourme R,Bouchereau A,Manzanares-Dauleux MJ(2011)Genetic and physiological analysis of the relationship between partial resistance to clubroot and tolerance to trehalose in Arabidopsis thaliana.New Phytol191:1083-1094
Henry C,Bledsoe SW,Griffiths CA,Kollman A,Paul MJ,Sakr S,Lagrimini LM(2015)Differential role for trehalose metabolism in salt-stressed maize.Plant Physiol 169:1072-1089
Hu Y,Jiang L,Wang F,Yu D(2013)Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DREbinding factor1 cascade and freezing tolerance in Arabidopsis.Plant Cell 25:2907-2924
Jiang Y,Liang G,Yang S,Yu D(2014)Arabidopsis WRKY57functions as a node of convergence for jasmonic acid-and auxin-mediated signaling in jasmonic acid-induced leaf senescence.Plant Cell 26:230-245
Kazan K,Manners JM(2013)MYC2:The master in action.Mol Plant 6:686-703
Kim MJ,Lim GH,Kim ES,Ko CB,Yang KY,Jeong JA,Lee MC,Kim CS(2007)Abiotic and biotic stress tolerance in Arabidopsis overexpressing the Multiprotein bridging factor 1a(MBF1a)transcriptional coactivator gene.Biochem Biophys Res Commun 354:440-446
Koch E,Slusarenko A(1990)Arabidopsis is susceptible to infection by a downy mildew fungus.Plant Cell 2:437-445
Kolbe A,Tiessen A,Schluepmann H,Paul M,Ulrich S,Geigenberger P(2005)Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase.Proc Natl Acad Sci USA102:11118-11123
Leyman B,Van Dijck P,Thevelein JM(2001)An unexpected plethora oftrehalose biosynthesis genes in Arabidopsis thaliana.Trends Plant Sci 6:510-513
Li HW,Zang BS,Deng XW,Wang XP(2011)Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice.Planta 234:1007-1018
Liu QX,Jindra M,Ueda H,Hiromi Y,Hirose S(2003)Drosophila MBF1 is a co-activator for tracheae defective and contributes to the formation of tracheal and nervous systems.Development 130:719-728
Lorenzo O,Piqueras R,Sanchez-Serrano JJ,Solano R(2003)ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense.Plant Cell 15:165-178
Mengiste T,Chen X,Salmeron J,Dietrich R(2003)The BOTRYTISSUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis.Plant Cell 15:2551-2565
Moghaddam MRB,Van den Ende W(2012)Sugars and plant innate immunity.J Exp Bot 63:3989-3998
Mukhopadhyay A,Deplancke B,Walhout AJ,Tissenbaum HA(2008)Chromatin immunoprecipitation(ChIP)coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans.Nat Protoc 3:698-709
Nakata M,Mitsuda N,Herde M,Koo AJ,Moreno JE,Suzuki K,Howe GA,Ohme-Takagi M(2013)A bHLH-Type Transcription Factor,ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTIONFACTOR/JA-ASSOCIATED MYC2-LIKE1,acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis.Plant Cell 25:1641-1656
Naseem M,Dandekar T(2012)The role of auxin-cytokinin antagonism in plant-pathogen interactions.PLoS Pathog8:e1003026
Paul MJ,Primavesi LF,Jhurreea D,Zhang Y(2008)Trehalose metabolism and signaling.Annu Rev Plant Biol 59:417-441
Pre M,Atallah M,Champion A,De Vos M,Pieterse CM,Memelink J(2008)The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense.Plant Physiol 147:1347-1357
Reignault P,Cogan A,Muchembled J,Lounes-Hadj Sahraoui A,Durand R,Sancholle M(2001)Trehalose induces resistance to powdery mildew in wheat.New Phytol 149:519-529
Saleh A,Alvarez-Venegas R,Avramova Z(2008)An efficient chromatin immunoprecipitation(ChIP)protocol for studying histone modifications in Arabidopsis plants.Nat Protoc3:1018-1025
Satoh-Nagasawa N,Nagasawa N,Malcomber S,Sakai H,Jackson D(2006)A trehalose metabolic enzyme controls inflorescence architecture in maize.Nature 441:227-230
Schluepmann H,Berke L,Sanchez-Perez GF(2012)Metabolism control over growth:A case for trehalose-6-phosphate in plants.J Exp Bot 63:3379-3390
Schluepmann H,Paul M(2009)Trehalose metabolites in Arabidopsis-elusive,active and central.The Arabidopsis book/American Society of Plant Biologists 7:e0122
Schluepmann H,van Dijken A,Aghdasi M,Wobbes B,Paul M,Smeekens S(2004)Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation.Plant Physiol 135:879-890
Seo HS,Song JT,Cheong JJ,Lee YH,Lee YW,Hwang I,Lee JS,Choi YD(2001)Jasmonic acid carboxyl methyltransferase:A key enzyme for jasmonate-regulated plant responses.Proc Natl Acad Sci USA 98:4788-4793
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Avonce N,Leyman B,Mascorro-Gallardo JO,Van Dijck P,Thevelein JM,Iturriaga G(2004)The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose,abscisic acid,and stress signaling.Plant Physiol 136:3649-3659
Avonce N,Mendoza-Vargas A,Morett E,Iturriaga G(2006)Insights on the evolution of trehalose biosynthesis.BMCEvol Biol 6:109
Bae H,Herman E,Bailey B,Bae HJ,Sicher R(2005)Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification,abiotic stress,nitrogen metabolism,and plant defense.Physiol Plant 125:114-126
Berrocal-Lobo M,Molina A(2004)Ethylene response factor 1mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum.Mol Plant Microbe Interact 17:763-770
Brodmann A,Schuller A,Ludwig-M€uller J,Aeschbacher RA,Wiemken A,Boller T,Wingler A(2002)Induction of trehalase in Arabidopsis plants infected with the trehaloseproducing pathogen Plasmodiophora brassicae.Mol Plant Microbe Interact 15:693-700
Chary SN,Hicks GR,Choi YG,Carter D,Raikhel NV(2008)Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis.Plant Physiol 146:97-107
Clough SJ,Bent AF(1998)Floral dip:A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Plant J 16:735-743
Cui F,Wu S,Sun W,Coaker G,Kunkel B,He P,Shan L(2013)The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover.Plant Physiol 162:1018-1029
Dean R,Van Kan JA,Pretorius ZA,Hammond-Kosack KE,Di Pietro A,Spanu PD,Rudd JJ,Dickman M,Kahmann R,Ellis J(2012)The Top 10 fungal pathogens in molecular plant pathology.Mol Plant Pathol 13:414-430
Djonovic S,Urbach JM,Drenkard E,Bush J,Feinbaum R,Ausubel JL,Traficante D,Risech M,Kocks C,Fischbach MA(2013)Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants.PLoS Pathog 9:e1003217
Eastmond PJ,Graham IA(2003)Trehalose metabolism:Aregulatory role for trehalose-6-phosphate?Curr Opin Plant Biol 6:231-235
Eastmond PJ,Van Dijken AJ,Spielman M,Kerr A,Tissier AF,Dickinson HG,Jones JD,Smeekens SC,Graham IA(2002)Trehalose-6-phosphate synthase 1,which catalyses the first step in trehalose synthesis,is essential for Arabidopsis embryo maturation.Plant J 29:225-235
Fernandez O,Bethencourt L,Quero A,Sangwan RS,Clement C(2010)Trehalose and plant stress responses:Friend or foe?Trends Plant Sci 15:409-417
Foster AJ,Jenkinson JM,Talbot NJ(2003)Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea.EMBO J 22:225-235
Fritzius T,Aeschbacher R,Wiemken A,Wingler A(2001)Induction of ApL3 expression by trehalose complements the starch-deficient Arabidopsis mutantadg2-1 lacking ApL1,the large subunit of ADP-glucose pyrophosphorylase.Plant Physiol 126:883-889
Gomez-Ariza J,Campo S,Rufat M,Estopa M,Messeguer J,Segundo BS,Coca M(2007)Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesisrelated PRms protein in rice plants.Mol Plant Microbe Interact 20:832-842
Gimenez-Ibanez S,Solano R(2013)Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens.Front Plant Sci 4:72
Govind SR,Jogaiah S,Abdelrahman M,Shetty HS,Tran L-SP(2016)Exogenous trehalose treatment enhances the activities of defense-related enzymes and triggers resistance against downy mildew disease of pearl millet.Front Plant Sci 7:1593
Gravot A,Grillet L,Wagner G,Jubault M,Lariagon C,Baron C,Deleu C,Delourme R,Bouchereau A,Manzanares-Dauleux MJ(2011)Genetic and physiological analysis of the relationship between partial resistance to clubroot and tolerance to trehalose in Arabidopsis thaliana.New Phytol191:1083-1094
Henry C,Bledsoe SW,Griffiths CA,Kollman A,Paul MJ,Sakr S,Lagrimini LM(2015)Differential role for trehalose metabolism in salt-stressed maize.Plant Physiol 169:1072-1089
Hu Y,Jiang L,Wang F,Yu D(2013)Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DREbinding factor1 cascade and freezing tolerance in Arabidopsis.Plant Cell 25:2907-2924
Jiang Y,Liang G,Yang S,Yu D(2014)Arabidopsis WRKY57functions as a node of convergence for jasmonic acid-and auxin-mediated signaling in jasmonic acid-induced leaf senescence.Plant Cell 26:230-245
Kazan K,Manners JM(2013)MYC2:The master in action.Mol Plant 6:686-703
Kim MJ,Lim GH,Kim ES,Ko CB,Yang KY,Jeong JA,Lee MC,Kim CS(2007)Abiotic and biotic stress tolerance in Arabidopsis overexpressing the Multiprotein bridging factor 1a(MBF1a)transcriptional coactivator gene.Biochem Biophys Res Commun 354:440-446
Koch E,Slusarenko A(1990)Arabidopsis is susceptible to infection by a downy mildew fungus.Plant Cell 2:437-445
Kolbe A,Tiessen A,Schluepmann H,Paul M,Ulrich S,Geigenberger P(2005)Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase.Proc Natl Acad Sci USA102:11118-11123
Leyman B,Van Dijck P,Thevelein JM(2001)An unexpected plethora oftrehalose biosynthesis genes in Arabidopsis thaliana.Trends Plant Sci 6:510-513
Li HW,Zang BS,Deng XW,Wang XP(2011)Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice.Planta 234:1007-1018
Liu QX,Jindra M,Ueda H,Hiromi Y,Hirose S(2003)Drosophila MBF1 is a co-activator for tracheae defective and contributes to the formation of tracheal and nervous systems.Development 130:719-728
Lorenzo O,Piqueras R,Sanchez-Serrano JJ,Solano R(2003)ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense.Plant Cell 15:165-178
Mengiste T,Chen X,Salmeron J,Dietrich R(2003)The BOTRYTISSUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis.Plant Cell 15:2551-2565
Moghaddam MRB,Van den Ende W(2012)Sugars and plant innate immunity.J Exp Bot 63:3989-3998
Mukhopadhyay A,Deplancke B,Walhout AJ,Tissenbaum HA(2008)Chromatin immunoprecipitation(ChIP)coupled to detection by quantitative real-time PCR to study transcription factor binding to DNA in Caenorhabditis elegans.Nat Protoc 3:698-709
Nakata M,Mitsuda N,Herde M,Koo AJ,Moreno JE,Suzuki K,Howe GA,Ohme-Takagi M(2013)A bHLH-Type Transcription Factor,ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTIONFACTOR/JA-ASSOCIATED MYC2-LIKE1,acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis.Plant Cell 25:1641-1656
Naseem M,Dandekar T(2012)The role of auxin-cytokinin antagonism in plant-pathogen interactions.PLoS Pathog8:e1003026
Paul MJ,Primavesi LF,Jhurreea D,Zhang Y(2008)Trehalose metabolism and signaling.Annu Rev Plant Biol 59:417-441
Pre M,Atallah M,Champion A,De Vos M,Pieterse CM,Memelink J(2008)The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense.Plant Physiol 147:1347-1357
Reignault P,Cogan A,Muchembled J,Lounes-Hadj Sahraoui A,Durand R,Sancholle M(2001)Trehalose induces resistance to powdery mildew in wheat.New Phytol 149:519-529
Saleh A,Alvarez-Venegas R,Avramova Z(2008)An efficient chromatin immunoprecipitation(ChIP)protocol for studying histone modifications in Arabidopsis plants.Nat Protoc3:1018-1025
Satoh-Nagasawa N,Nagasawa N,Malcomber S,Sakai H,Jackson D(2006)A trehalose metabolic enzyme controls inflorescence architecture in maize.Nature 441:227-230
Schluepmann H,Berke L,Sanchez-Perez GF(2012)Metabolism control over growth:A case for trehalose-6-phosphate in plants.J Exp Bot 63:3379-3390
Schluepmann H,Paul M(2009)Trehalose metabolites in Arabidopsis-elusive,active and central.The Arabidopsis book/American Society of Plant Biologists 7:e0122
Schluepmann H,van Dijken A,Aghdasi M,Wobbes B,Paul M,Smeekens S(2004)Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation.Plant Physiol 135:879-890
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