Two-Component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity
Recent studies have revealed an important role for hormones in plant immunity. We are now beginning to understand the contribution of crosstalk among different hormone signaling networks to the outcome of plant–pathogen interactions. Cytokinins are plant hormones that regulate development and responses to the environment. Cytokinin signaling involves a phosphorelay circuitry similar to two-component systems used by bacteria and fungi to perceive and react to various environmental stimuli. In this study, we asked whether cytokinin and components of cytokinin signaling contribute to plant immunity. We demonstrate that cytokinin levels in Arabidopsis are important in determining the amplitude of immune responses, ultimately influencing the outcome of plant–pathogen interactions. We show that high concentrations of cytokinin lead to increased defense responses to a virulent oomycete pathogen, through a process that is dependent on salicylic acid (SA) accumulation and activation of defense gene expression. Surprisingly, treatment with lower concentrations of cytokinin results in increased susceptibility. These functions for cytokinin in plant immunity require a host phosphorelay system and are mediated in part by type-A response regulators, which act as negative regulators of basal and pathogen-induced SA–dependent gene expression. Our results support a model in which cytokinin up-regulates plant immunity via an elevation of SA–dependent defense responses and in which SA in turn feedback-inhibits cytokinin signaling. The crosstalk between cytokinin and SA signaling networks may help plants fine-tune defense responses against pathogens.
Vyšlo v časopise:
Two-Component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002448
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002448
Souhrn
Recent studies have revealed an important role for hormones in plant immunity. We are now beginning to understand the contribution of crosstalk among different hormone signaling networks to the outcome of plant–pathogen interactions. Cytokinins are plant hormones that regulate development and responses to the environment. Cytokinin signaling involves a phosphorelay circuitry similar to two-component systems used by bacteria and fungi to perceive and react to various environmental stimuli. In this study, we asked whether cytokinin and components of cytokinin signaling contribute to plant immunity. We demonstrate that cytokinin levels in Arabidopsis are important in determining the amplitude of immune responses, ultimately influencing the outcome of plant–pathogen interactions. We show that high concentrations of cytokinin lead to increased defense responses to a virulent oomycete pathogen, through a process that is dependent on salicylic acid (SA) accumulation and activation of defense gene expression. Surprisingly, treatment with lower concentrations of cytokinin results in increased susceptibility. These functions for cytokinin in plant immunity require a host phosphorelay system and are mediated in part by type-A response regulators, which act as negative regulators of basal and pathogen-induced SA–dependent gene expression. Our results support a model in which cytokinin up-regulates plant immunity via an elevation of SA–dependent defense responses and in which SA in turn feedback-inhibits cytokinin signaling. The crosstalk between cytokinin and SA signaling networks may help plants fine-tune defense responses against pathogens.
Zdroje
1. JonesJDGDanglJL 2006 The plant immune system. Nature 444 323 329
2. FeysBJParkerJE 2000 Interplay of signaling pathways in plant disease resistance. Trends in Genetics 16 449 455
3. SpoelSHDongXN 2008 Making sense of hormone crosstalk during plant immune responses. Cell Host & Microbe 3 348 351
4. Robert-SeilaniantzANavarroLBariRJonesJD 2007 Pathological hormone imbalances. Current Opinion in Plant Biology 10 372 379
5. ArguesoCTFerreiraFJKieberJJ 2009 Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell and Environment 32 1147 1160
6. SchallerGEKieberJJShiuS 2008 Two-component signaling elements and histidyl-aspartyl phosphorelays. SomervilleCMeyerowitzEM The Arabidopsis Book Rockville American Society of Plant Biologists 1 12
7. HwangISheenJ 2001 Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413 383 389
8. KibaTYamadaHSatoSKatoTTabataS 2003 The type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. Plant and Cell Physiology 44 868 874
9. LeeDJParkJYKuSJHaYMKimS 2007 Genome-wide expression profiling of ARABIDOPSIS RESPONSE REGULATOR 7(ARR7) overexpression in cytokinin response. Molecular Genetics and Genomics 277 115 137
10. ToJPCHabererGFerreiraFJDeruereJMasonMG 2004 Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16 658 671
11. SakaiHHonmaTAoyamaTSatoSKatoT 2001 ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294 1519 1521
12. MasonMGMathewsDEArgyrosDAMaxwellBBKieberJJ 2005 Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17 3007 3018
13. ArgyrosRDMathewsDEChiangYHPalmerCMThibaultDM 2008 Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20 2102 2116
14. ClarkeSFBurrittDJGuyPL 1998 Influence of plant hormones on virus replication and pathogenesis-related proteins in Phaseolus vulgaris L. infected with white clover mosaic potexvirus. Physiological and Molecular Plant Pathology 53 195 207
15. SchaferSKrolzikSRomanovGASchmullingT 2000 Cytokinin-regulated transcripts in tobacco cell culture. Plant Growth Regulation 32 307 313
16. RashotteAMCarsonSDBToJPCKieberJJ 2003 Expression profiling of cytokinin action in Arabidopsis. Plant Physiology 132 1998 2011
17. ChoiJHuhSUKojimaMSakakibaraHPaekKH 2010 The Cytokinin-Activated Transcription Factor ARR2 Promotes Plant Immunity via TGA3/NPR1-Dependent Salicylic Acid Signaling in Arabidopsis. Developmental Cell 19 284 295
18. AshbyAM 2000 Biotrophy and the cytokinin conundrum. Physiological and Molecular Plant Pathology 57 147 158
19. LevinIM 1984 Effect of phytohormones on development of brown rust on isolated wheat leaves. Soviet Plant Physiology 31 356 361
20. BaboshaAV 2009 Regulation of resistance and susceptibility in wheat-powdery mildew pathosystem with exogenous cytokinins. Journal of Plant Physiology 166 1892 1903
21. JamesonPE 2000 Cytokinins and auxins in plant-pathogen interactions - An overview. Plant Growth Regulation 32 369 380
22. ToufighiKBradySMAustinRLyEProvartNJ 2005 The Botany Array Resource: e-Northerns, Expression Angling, and Promoter analyses. Plant Journal 43 153 163
23. BrandstatterIKieberJJ 1998 Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell 10 1009 1019
24. MaymonIGreenboim-WainbergYSagivSKieberJJMoshelionM 2009 Cytosolic activity of SPINDLY implies the existence of a DELLA-independent gibberellin-response pathway. Plant Journal 58 979 988
25. GordonSPChickarmaneVSOhnoCMeyerowitzEM 2009 Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences of the United States of America 106 16529 16534
26. GlazebrookJ 2005 Contrasting mechanisms of defense agianst biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43 205 227
27. TsudaKSatoMStoddardTGlazebrookJKatagiriF 2009 Network Properties of Robust Immunity in Plants. PLoS Genet 5 e1000772 doi:10.1371/journal.pgen.1000772
28. DewdneyJReuberTLWildermuthMCDevotoACuiJP 2000 Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant Journal 24 205 218
29. WildermuthMCDewdneyJWuGAusubelFM 2001 Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414 562 565
30. ZipfelCKunzeGChinchillaDCaniardAJonesJDG 2006 Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125 749 760
31. LuXTintorNMentzelTKombrinkEBollerT 2009 Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proceedings of the National Academy of Sciences of the United States of America 106 22522 22527
32. DonofrioNMDelaneyTP 2001 Abnormal callose response phenotype and hypersusceptibility to Peronospora parasitica in defense-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Molecular Plant-Microbe Interactions 14 439 450
33. ToJPCDeruereJMaxwellBBMorrisVFHutchisonCE 2007 Cytokinin regulates type-A Arabidopsis response regulator activity and protein stability via two-component phosphorelay. Plant Cell 19 3901 3914
34. NishimuraCOhashiYSatoSKatoTTabataS 2004 Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16 1365 1377
35. HiguchiMPischkeMSMahonenAPMiyawakiKHashimotoY 2004 In planta functions of the Arabidopsis cytokinin receptor family. Proceedings of the National Academy of Sciences of the United States of America 101 8821 8826
36. RieflerMNovakOStrnadMSchmullingT 2006 Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18 40 54
37. Mauch-ManiBSlusarenkoAJ 1996 Production of Salicylic Acid Precursors Is a Major Function of Phenylalanine Ammonia-Lyase in the Resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8 203 212
38. VallonUGrafJAKullU 1989 Influence of calcium and calcium and calmodulin antagonists on the cytokinin-induced amaranthin accumulation in Amaranthus tricolor. Journal of Plant Growth Regulation 8 81 92
39. LeeTT 1971 Cytokinin-controlled indoleacetic acid oxidase isoenzymes in tobacco callus cultures. Plant Physiology 47 181 185
40. VogelJPWoesteKETheologisAKieberJJ 1998 Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. 1998 95 4766 4771
41. SpichalLRakovaNYRieflerMMizunoTRomanovGA 2004 Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK2 and AHK3, differ in their ligand specificity in a bacterial assay. Plant and Cell Physiology 45 1299 1305
42. YamadaHSuzukiTTeradaKTakeiKIshiwakaK 2001 The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant and Cell Physiology 42 1017 1023
43. RomanovGALominSNSchmullingT 2006 Biochemical characteritics and ligand binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. Journal of Experimental Botany 57 4051 4058
44. StolzARieflerMLominSNAchaziKRomanovGA 2011 The specificity of cytokinin signaling in Arabidopsis thaliana is mediated by different ligand affinities and expression profiles of the receptors. Plant Journal 67 157 168
45. HwangISakakibaraH 2006 Cytokinin biosynthesis and perception. Physiologia Plantarum 126 528 538
46. SanoHSeoSKoizumiNNikiTIwamuraH 1996 Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant and Cell Physiology 37 762 769
47. GoellnerKConrathU 2008 Priming: it's all the world tp induced disease resistance. 2008 121 233 242
48. SiemensDHKeckAGZiegenbeinS 2010 Optimal defense in plants: assessment of resource allocation costs. Evolutionary Ecology 24 1291 1305
49. vanderWerfANagelOW 1996 Carbon allocation to shoots and roots in relation to nitrogen supply is mediated by cytokinins and sucrose: Opinion. Plant and Soil 185 21 32
50. RoitschTEhnessR 2000 Regulation of source/sink relations by cytokinins. Plant Growth Regulation 32 359 367
51. SatoNKawaharaHToh-eAMaedaT 2003 Phosphorelay-regulated degradation of the yeast Ssk1p response regulator by the ubiquitin-proteasome system. Molecular and Cellular Biology 23 6662 6671
52. SilvermanPSeskarMKanterDSchweizerPMetrauxJP 1995 Salicylic acid in rice - Biosynthesis, Conjugation, and Possible Role. Plant Physiology 108 633 639
53. RashotteAMMasonMGHutchisonCEFerreiraFJSchallerGE 2006 A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proceedings of the National Academy of Sciences of the United States of America 103 11081 11085
54. PfafflMWHorganGWDempfleL 2002 Relative expression software tool (REST (c)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30
55. DeFraiaCTSchmelzEAMouZL 2008 A rapid biosensor-based method for quantification of free and glucose-conjugated salicylic acid. Plant Methods 4
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 1
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