Modifications of sphingolipid content affect tolerance to hemibiotrophic and necrotrophic pathogens by modulating plant defense responses in Arabidopsis

Plant Physiology

Volumn 169, Issue 3, 2015, Pages 2255-2274

  Magnin Robert, Maryline ^a   Le Bourse, Doriane ^b   Markham, Jonathan ^b   Dorey, Stéphan ^a   Clément, Christophe ^a   Baillieul, Fabienne ^a   Dhondt Cordelier, Sandrine ^a  

^a UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4-HYDROXY-8-SPHINGENINE; CYCLOPENTANE DERIVATIVE; DIHYDROSPHINGOSINE 1-PHOSPHATE; ISOLEUCINE; JASMONIC ACID; JASMONOYL-ISOLEUCINE; OXYLIPIN; PHYTOHORMONE; PHYTOSPHINGOSINE-1-PHOSPHATE; REACTIVE OXYGEN METABOLITE; SAFINGOL; SALICYLIC ACID; SPHINGOLIPID; SPHINGOSINE;

ANALOGS AND DERIVATIVES; ARABIDOPSIS; BOTRYTIS; CELL DEATH; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION;

ARABIDOPSIS; BOTRYTIS; CELL DEATH; CYCLOPENTANES; ISOLEUCINE; MUTATION; OXYLIPINS; PLANT DISEASES; PLANT GROWTH REGULATORS; PSEUDOMONAS SYRINGAE; REACTIVE OXYGEN SPECIES; SALICYLIC ACID; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; SPHINGOSINE;

EID: 84946232811     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01126     Document Type: Article

References (99)

1. Abbas HK, Tanaka T, Duke SO, Porter JK, Wray EM, Hodges L, Sessions AE, Wang E, Merrill AH Jr, Riley RT (1994) Fumonisin- and AAL-toxininduced disruption of sphingolipid metabolism with accumulation of free sphingoid bases. Plant Physiol 106: 1085–1093
2. Alden KP, Dhondt-Cordelier S, McDonald KL, Reape TJ, Ng CK, McCabe PF, Leaver CJ (2011) Sphingolipid long chain base phosphates can regulate apoptotic-like programmed cell death in plants. Biochem Biophys Res Commun 410: 574–580
3. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657
4. Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J, Ausubel FM (2000) Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12: 1823–1836
5. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69: 473–488
6. Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21: 944–953
7. Bender CL, Alarcón-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63: 266–292
8. Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58: 4019–4026
9. Berkey R, Bendigeri D, Xiao S (2012) Sphingolipids and plant defense/ disease: the “death” connection and beyond. Front Plant Sci 3: 68
10. Bi FC, Liu Z, Wu JX, Liang H, Xi XL, Fang C, Sun TJ, Yin J, Dai GY, Rong C, et al (2014) Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts. Plant Cell 26: 3449–3467
11. Block A, Schmelz E, O’Donnell PJ, Jones JB, Klee HJ (2005) Systemic acquired tolerance to virulent bacterial pathogens in tomato. Plant Physiol 138: 1481–1490
12. Bolton MD (2009) Primary metabolism and plant defense: fuel for the fire. Mol Plant Microbe Interact 22: 487–497
13. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545–580
14. Brandwagt BF, Mesbah LA, Takken FL, Laurent PL, Kneppers TJ, Hille J, Nijkamp HJ (2000) A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 97: 4961–4966
15. Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Odum N, Jørgensen LB, Brown RE, Mundy J (2002) Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16: 490–502
16. Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic aciddependent defences in Arabidopsis thaliana. Mol Plant Pathol 6: 629–639
17. Brooks DM, Hernández-Guzmán G, Kloek AP, Alarcón-Chaidez F, Sreedharan A, Rangaswamy V, Peñaloza-Vázquez A, Bender CL, Kunkel BN (2004) Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 17: 162–174
18. Cao H, Li X, Dong X (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95: 6531–6536
19. Chen M, Markham JE, Dietrich CR, Jaworski JG, Cahoon EB (2008) Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 20: 1862–1878
20. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247–1256
21. Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera- Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal- and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal Behav 6: 1554–1563
22. Coursol S, Fromentin J, Noirot E, Brière C, Robert F, Morel J, Liang YK, Lherminier J, Simon-Plas F (2015) Long-chain bases and their phosphorylated derivatives differentially regulate cryptogein-induced production of reactive oxygen species in tobacco (Nicotiana tabacum) BY-2 cells. New Phytol 205: 1239–1249
23. Dellagi A, Brisset MN, Paulin JP, Expert D (1998) Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol Plant Microbe Interact 11: 734–742
24. Derksen H, Rampitsch C, Daayf F (2013) Signaling cross-talk in plant disease resistance. Plant Sci 207: 79–87
25. Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 98: 6957–6962
26. Donahue JL, Alford SR, Torabinejad J, Kerwin RE, Nourbakhsh A, Ray WK, Hernick M, Huang X, Lyons BM, Hein PP, et al (2010) The Arabidopsis thaliana Myo-inositol 1-phosphate synthase1 gene is required for Myo-inositol synthesis and suppression of cell death. Plant Cell 22: 888–903
27. Dunn TM, Lynch DV, Michaelson LV, Napier JA (2004) A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann Bot (Lond) 93: 483–497
28. El Oirdi M, Bouarab K (2007) Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea. New Phytol 175: 131–139
29. El Oirdi M, El Rahman TA, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23: 2405–2421
30. Geng X, Cheng J, Gangadharan A, Mackey D (2012) The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense. Plant Cell 24: 4763–4774
31. Glauser G, Vallat A, Balmer D (2014) Hormone profiling. In JJ Sanchez- Serrano, J Salinas, eds, Arabidopsis Protocols: Methods in Molecular Biology, Vol 1062. Springer Science + Business Media, New York, pp 597–608
32. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205–227
33. Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751–757
34. Govrin EM, Levine A (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol Biol 48: 267–276
35. Govrin EM, Rachmilevitch S, Tiwari BS, Solomon M, Levine A (2006) An elicitor from Botrytis cinerea induces the hypersensitive response in Arabidopsis thaliana and other plants and promotes the gray mold disease. Phytopathology 96: 299–307
36. Greenberg JT, Silverman FP, Liang H (2000) Uncoupling salicylic aciddependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics 156: 341–350
37. Kawasaki T, Nam J, Boyes DC, Holt BF III, Hubert DA, Wiig A, Dangl JL (2005) A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J 44: 258–270
38. König S, Feussner K, Schwarz M, Kaever A, Iven T, Landesfeind M, Ternes P, Karlovsky P, Lipka V, Feussner I (2012) Arabidopsis mutants of sphingolipid fatty acid a-hydroxylases accumulate ceramides and salicylates. New Phytol 196: 1086–1097
39. Koornneef A, Pieterse CM (2008) Cross talk in defense signaling. Plant Physiol 146: 839–844
40. Kraepiel Y, Pédron J, Patrit O, Simond-Côte E, Hermand V, Van Gijsegem F (2011) Analysis of the plant bos1 mutant highlights necrosis as an efficient defence mechanism during D. dadantii/Arabidopsis thaliana interaction. PLoS One 6: e18991
41. Lachaud C, Da Silva D, Amelot N, Béziat C, Brière C, Cotelle V, Graziana A, Grat S, Mazars C, Thuleau P (2011) Dihydrosphingosine-induced programmed cell death in tobacco BY-2 cells is independent of H2O2 production. Mol Plant 4: 310–318
42. Lachaud C, Da Silva D, Cotelle V, Thuleau P, Xiong TC, Jauneau A, Brière C, Graziana A, Bellec Y, Faure JD, et al (2010) Nuclear calcium controls the apoptotic-like cell death induced by d-erythro-sphinganine in tobacco cells. Cell Calcium 47: 92–100
43. Laurie-Berry N, Joardar V, Street IH, Kunkel BN (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact 19: 789–800
44. Le Hénanff G, Profizi C, Courteaux B, Rabenoelina F, Gérard C, Clément C, Baillieul F, Cordelier S, Dhondt-Cordelier S (2013) Grapevine NAC1 transcription factor as a convergent node in developmental processes, abiotic stresses, and necrotrophic/biotrophic pathogen tolerance. J Exp Bot 64: 4877–4893
45. L’Haridon F, Besson-Bard A, Binda M, Serrano M, Abou-Mansour E, Balet F, Schoonbeek HJ, Hess S, Mir R, Léon J, et al (2011) A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity. PLoS Pathog 7: e1002148
46. Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT (2003) Ceramides modulate programmed cell death in plants. Genes Dev 17: 2636–2641
47. Lohman KN, Gan S, John MC, Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92: 322–328
48. Markham JE, Jaworski JG (2007) Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 21: 1304–1314
49. Markham JE, Lynch DV, Napier JA, Dunn TM, Cahoon EB (2013) Plant sphingolipids: function follows form. Curr Opin Plant Biol 16: 350–357
50. Mayer AM, Staples RC, Gil-ad NL (2001) Mechanisms of survival of necrotrophic fungal plant pathogens in hosts expressing the hypersensitive response. Phytochemistry 58: 33–41
51. Mortimer JC, Yu X, Albrecht S, Sicilia F, Huichalaf M, Ampuero D, Michaelson LV, Murphy AM, Matsunaga T, Kurz S, et al (2013) Abnormal glycosphingolipid mannosylation triggers salicylic acid-mediated responses in Arabidopsis. Plant Cell 25: 1881–1894
52. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response: the centenary is upon us but how much do we know? J Exp Bot 59: 501–520
53. Nagano M, Takahara K, Fujimoto M, Tsutsumi N, Uchimiya H, Kawai- Yamada M (2012) Arabidopsis sphingolipid fatty acid 2-hydroxylases (AtFAH1 and AtFAH2) are functionally differentiated in fatty acid 2-hydroxylation and stress responses. Plant Physiol 159: 1138–1148
54. Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8: 335–342
55. Peer M, Bach M, Mueller MJ, Waller F (2011) Free sphingobases induce RBOHD-dependent reactive oxygen species production in Arabidopsis leaves. FEBS Lett 585: 3006–3010
56. 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
57. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, et al (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103: 1111–1120
58. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5: 308–316
59. Rasul S, Dubreuil-Maurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S (2012) Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ 35: 1483–1499
60. Ren D, Liu Y, Yang KY, Han L, Mao G, Glazebrook J, Zhang S (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105: 5638–5643
61. Rivas-San Vicente M, Larios-Zarate G, Plasencia J (2013) Disruption of sphingolipid biosynthesis in Nicotiana benthamiana activates salicylic acid-dependent responses and compromises resistance to Alternaria alternata f. sp. lycopersici. Planta 237: 121–136
62. Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49: 317–343
63. Sanchez L, Courteaux B, Hubert J, Kauffmann S, Renault JH, Clément C, Baillieul F, Dorey S (2012) Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiol 160: 1630–1641
64. Sánchez-Rangel D, Rivas-San Vicente M, de la Torre-Hernández ME, Nájera-Martínez M, Plasencia J (2015) Deciphering the link between salicylic acid signaling and sphingolipid metabolism. Front Plant Sci 6: 125
65. Saucedo-García M, Gavilanes-Ruíz M, Arce-Cervantes O (2015) Longchain bases, phosphatidic acid, MAPKs, and reactive oxygen species as nodal signal transducers in stress responses in Arabidopsis. Front Plant Sci 6: 55
66. Saucedo-García M, Guevara-García A, González-Solís A, Cruz-García F, Vázquez-Santana S, Markham JE, Lozano-Rosas MG, Dietrich CR, Ramos-Vega M, Cahoon EB, et al (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
67. Savatin DV, Bisceglia NG, Marti L, Fabbri C, Cervone F, De Lorenzo G (2014) The Arabidopsis NUCLEUS- AND PHRAGMOPLAST-LOCALIZED KINASE1-related protein kinases are required for elicitor-induced oxidative burst and immunity. Plant Physiol 165: 1188–1202
68. Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH III (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci USA 100: 10552–10557
69. Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 63: 451–482
70. Shi C, Yin J, Liu Z, Wu JX, Zhao Q, Ren J, Yao N (2015) A systematic simulation of the effect of salicylic acid on sphingolipid metabolism. Front Plant Sci 6: 186
71. Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA, et al (2007) Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res 17: 1030–1040
72. Smith JM, Heese A (2014) Rapid bioassay to measure early reactive oxygen species production in Arabidopsis leave tissue in response to living Pseudomonas syringae. Plant Methods 10: 6
73. Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104: 18842–18847
74. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, et al (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760–770
75. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16: 2117–2127
76. Takahashi Y, Berberich T, Kanzaki H, Matsumura H, Saitoh H, Kusano T, Terauchi R (2009) Unraveling the roles of sphingolipids in plant innate immunity. Plant Signal Behav 4: 536–538
77. Ternes P, Feussner K, Werner S, Lerche J, Iven T, Heilmann I, Riezman H, Feussner I (2011) Disruption of the ceramide synthase LOH1 causes spontaneous cell death in Arabidopsis thaliana. New Phytol 192: 841–854
78. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17: 260–270
79. Thomma BP, Penninckx IA, Broekaert WF, Cammue BP (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13: 63–68
80. Torres MA (2010) ROS in biotic interactions. Physiol Plant 138: 414–429
81. Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517–522
82. Tsegaye Y, Richardson CG, Bravo JE, Mulcahy BJ, Lynch DV, Markham JE, Jaworski JG, Chen M, Cahoon EB, Dunn TM (2007) Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J Biol Chem 282: 28195–28206
83. Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13: 459–465
84. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 20: 955–965
85. van Baarlen P, Staats M, van Kan JA (2004) Induction of programmed cell death in lily by the fungal pathogen Botrytis elliptica. Mol Plant Pathol 5: 559–574
86. van Baarlen P, Woltering EJ, Staats M, van Kan JA (2007) Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Mol Plant Pathol 8: 41–54
87. van Kan JA (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11: 247–253
88. van Wees SC, Luijendijk M, Smoorenburg I, van Loon LC, Pieterse CM (1999) Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonateinducible gene Atvsp upon challenge. Plant Mol Biol 41: 537–549
89. Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T (2006) The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18: 257–273
90. Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2: e123
91. Wang W, Yang X, Tangchaiburana S, Ndeh R, Markham JE, Tsegaye Y, Dunn TM, Wang GL, Bellizzi M, Parsons JF, et al (2008) An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20: 3163–3179
92. Wu JX, Li J, Liu Z, Yin J, Chang ZY, Rong C, Wu JL, Bi FC, Yao N (2015) The Arabidopsis ceramidase AtACER functions in disease resistance and salt tolerance. Plant J 81: 767–780
93. Xin XF, He SY (2013) Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 51: 473–498
94. Zhang H, Li L, Yu Y, Mo J, Sun L, Liu B, Li D, Song F (2013) Cloning and characterization of two rice long-chain base kinase genes and their function in disease resistance and cell death. Mol Biol Rep 40: 117–127
95. Zhang L, Jia C, Liu L, Zhang Z, Li C, Wang Q (2011) The involvement of jasmonates and ethylene in Alternaria alternata f. sp. lycopersici toxininduced tomato cell death. J Exp Bot 62: 5405–5418
96. Zhang Y, Yang X, Zeng H, Guo L, Yuan J, Qiu D (2014) Fungal elicitor protein PebC1 from Botrytis cinerea improves disease resistance in Arabidopsis thaliana. Biotechnol Lett 36: 1069–1078
97. Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36: 485–499
98. Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11: 587–596
99. Zimmerli L, Métraux JP, Mauch-Mani B (2001) b-Aminobutyric acidinduced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol 126: 517–523