CaCDPK15 positively regulates pepper responses to Ralstonia solanacearum inoculation and forms a positive-feedback loop with CaWRKY40 to amplify defense signaling

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Shen, Lei ^a   Yang, Sheng ^a   Yang, Tong ^a   Liang, Jiaqi ^a   Cheng, Wei ^a   Wen, Jiayu ^a   Liu, Yanyan ^a   Li, Jiazhi ^a   Shi, Lanping ^a   Tang, Qian ^a   Shi, Wei ^a   Hu, Jiong ^a   Liu, Cailing ^a   Zhang, Yangwen ^a   Mou, Shaoliang ^a   Liu, Zhiqin ^a   Cai, Hanyang ^a   He, Li ^b   Guan, Deyi ^a   Wu, Yang ^b   He, Shuilin ^a   more..

^a FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^b Jing Gang Shan University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ACETIC ACID DERIVATIVE; CALCIUM-DEPENDENT PROTEIN KINASE; CYCLOPENTANE DERIVATIVE; ETHEPHON; HYDROGEN PEROXIDE; JASMONIC ACID METHYL ESTER; ORGANOPHOSPHORUS COMPOUND; OXYLIPIN; PHYTOHORMONE; PROTEIN BINDING; PROTEIN KINASE; SALICYLIC ACID; TRANSCRIPTION FACTOR;

CELL DEATH; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PEPPER; PHYSIOLOGY; PLANT DISEASE; PROMOTER REGION; RALSTONIA SOLANACEARUM; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ACETATES; CAPSICUM; CELL DEATH; CYCLOPENTANES; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; HYDROGEN PEROXIDE; ORGANOPHOSPHORUS COMPOUNDS; OXYLIPINS; PLANT DISEASES; PLANT GROWTH REGULATORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN KINASES; RALSTONIA SOLANACEARUM; SALICYLIC ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84959524638     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22439     Document Type: Article

References (60)

1. Moore, J. W., Loake, G. J. & Spoel, S. H. Transcription dynamics in plant immunity. Plant Cell 23, 2809-2820 (2011).
2. Tsuda, K. & Somssich, I. E. Transcriptional networks in plant immunity. New Phytol 206, 932-947 (2015).
3. Caarls, L., Pieterse, C. M. & Van Wees, S. C. How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6, 170 (2015).
4. Fragkostefanakis, S., Roth, S., Schleiff, E. & Scharf, K. D. Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ (2014).
5. Tang, N., Zhang, H., Li, X., Xiao, J. & Xiong, L. Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158, 1755-1768 (2012).
6. Ma, W., Smigel, A., Tsai, Y. C., Braam, J. & Berkowitz, G. A. Innate immunity signaling: cytosolic Ca2+.elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 148, 818-828 (2008).
7. Choi, W. G., Toyota, M., Kim, S. H., Hilleary, R. & Gilroy, S. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111, 6497-6502 (2014).
8. Marti, M. C., Stancombe, M. A. & Webb, A. A. Cell-and stimulus type-specific intracellular free Ca2+ signals in Arabidopsis. Plant Physiol 163, 625-634 (2013).
9. Fragkostefanakis, S., Roth, S., Schleiff, E. & Scharf, K. D. Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ 38, 1881-1895 (2015).
10. Cheng, S. H., Willmann, M. R., Chen, H. C. & Sheen, J. Calcium signaling through protein kinases. The Arabidopsis calciumdependent protein kinase gene family. Plant Physiol 129, 469-485 (2002).
11. Asano, T., Tanaka, N., Yang, G., Hayashi, N. & Komatsu, S. Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46, 356-366 (2005).
12. Kong, X. et al. Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genomics 14, 433 (2013).
13. Li, A. L. et al. Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66, 429-443 (2008).
14. Huang, Y., Deng, T. & Zuo, K. Cotton annexin proteins participate in the establishment of fiber cell elongation scaffold. Plant Signal Behav 8 (2013).
15. Liu, W. et al. Genome-Wide Survey and Expression Analysis of Calcium-Dependent Protein Kinase in Gossypium raimondii. PLoS One 9, e98189 (2014).
16. Romeis, T. & Herde, M. From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Curr Opin Plant Biol 20, 1-10 (2014).
17. Chen, F. et al. The evolutionary history and diverse physiological roles of the grapevine calcium-dependent protein kinase gene family. PLoS One 8, e80818 (2013).
18. Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K. & Izui, K. Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23, 319-327 (2000).
19. Ludwig, A. A., Romeis, T. & Jones, J. D. CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55, 181-188 (2004).
20. Vivek, P. J., Tuteja, N. & Soniya, E. V. CDPK1 from ginger promotes salinity and drought stress tolerance without yield penalty by improving growth and photosynthesis in Nicotiana tabacum. PLoS One 8, e76392 (2013).
21. Wan, B., Lin, Y. & Mou, T. Expression of rice Ca(2+ )-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581, 1179-1189 (2007).
22. Huang, T. L. et al. Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol 80, 587-608 (2012).
23. Kobayashi, M. et al. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19, 1065-1080 (2007).
24. Romeis, T. & Herde, M. From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Curr Opin Plant Biol 20C, 1-10 (2014).
25. Eulgem, T., Rushton, P. J., Robatzek, S. & Somssich, I. E. The WRKY superfamily of plant transcription factors. Trends Plant Sci 5, 199-206 (2000).
26. Ding, Z. J. et al. Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79, 13-27 (2014).
27. Rizhsky, L., Liang, H. & Mittler, R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130, 1143-1151 (2002).
28. Yokotani, N. et al. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64, 5085-5097 (2013).
29. Wang, H. H. et al. Chimeric repressor of PtSND2 severely affects wood formation in transgenic Populus. Tree Physiol 33, 878-886 (2013).
30. Skibbe, M., Qu, N., Galis, I. & Baldwin, I. T. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20, 1984-2000 (2008).
31. Turck, F., Zhou, A. & Somssich, I. E. Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to Its native promoter and the defense-related gene PcPR1-1 in Parsley. Plant Cell 16, 2573-2585 (2004).
32. Eulgem, T. Dissecting the WRKY web of plant defense regulators. PLoS Pathog 2, e126 (2006).
33. Ciolkowski, I., Wanke, D., Birkenbihl, R. P. & Somssich, I. E. Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68, 81-92 (2008).
34. Chi, Y. et al. Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant 6, 287-300 (2013).
35. Shan, W., Chen, J. Y., Kuang, J. F. & Lu, W. J. Banana fruit NAC transcription factor MaNAC5 cooperates with MaWRKYs to enhance the expression of pathogenesis-related genes against Colletotrichum musae. Mol Plant Pathol (2015).
36. Dang, F. F. et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ 36, 757-774 (2013).
37. Cai, H. et al. CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers hightemperature and high-humidity tolerance in pepper. J Exp Bot 66, 3163-3174 (2015).
38. Kim, S. et al. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46, 270-278 (2014).
39. Kim, H. Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiologia Plantarum (2000).
40. Mee Do, H., Chul Lee, S., Won Jung, H., Hoon Sohn, K. & Kook Hwang, B. Differential expression and in situ localization of a pepper defensin (CADEF1) gene in response to pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Plant Science 166, 1297-1305 (2004).
41. Choi, H. W., Kim, Y. J., Lee, S. C., Hong, J. K. & Hwang, B. K. Hydrogen Peroxide Generation by the Pepper Extracellular Peroxidase CaPO2 Activates Local and Systemic Cell Death and Defense Response to Bacterial Pathogens. Plant Physiology 145, 890-904 (2007).
42. Choi The Hypersensitive Induced Reaction and Leucine-Rich Repeat Proteins Regulate Plant Cell Death Associated with Disease and Plant Immunity - CaHIR1. Molecular Plant-Microbe Interactions (2011).
43. Arthikala, M.-K., Nanjareddy, K., Lara, M. & Sreevathsa, R. Utility of a tissue culture-independent Agrobacterium-mediated in planta transformation strategy in bell pepper to develop fungal disease resistant plants-CaNPR1. Scientia Horticulturae 170, 61-69 (2014).
44. Kim, N. H., Kim, D. S., Chung, E. H. & Hwang, B. K. Pepper suppressor of the G2 allele of skp1 interacts with the receptor-like cytoplasmic kinase1 and type III effector AvrBsT and promotes the hypersensitive cell death response in a phosphorylationdependent manner. Plant Physiol 165, 76-91 (2014).
45. Boudsocq, M. & Sheen, J. CDPKs in immune and stress signaling. Trends Plant Sci 18, 30-40 (2013).
46. Bartsch, M. et al. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18, 1038-1051 (2006).
47. Eulgem, T., Rushton, P. J., Schmelzer, E., Hahlbrock, K. & Somssich, I. E. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 18, 4689-4699 (1999).
48. Levine, A., Pennell, R. I., Alvarez, M. E., Palmer, R. & Lamb, C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6, 427-437 (1996).
49. Seybold, H. et al. Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. New Phytol 204, 782-790 (2014).
50. Geng, S. et al. TaCPK2-A, a calcium-dependent protein kinase gene that is required for wheat powdery mildew resistance enhances bacterial blight resistance in transgenic rice. J Exp Bot 64, 3125-3136 (2013).
51. Gao, X. & He, P. Nuclear dynamics of Arabidopsis calcium-dependent protein kinases in effector-triggered immunity. Plant Signal Behav 8, e23868 (2013).
52. Tateda, C. et al. Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26, 4171-4187 (2014).
53. Lin, M. Y. et al. A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol 164, 2045-2053 (2014).
54. Xiong, L., Lee, H., Ishitani, M. & Zhu, J. K. Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277, 8588-8596 (2002).
55. Cecchini, N. M., Jung, H. W., Engle, N., Tschaplinski, T. J. & Greenberg, J. ALD1 regulates basal immune components and early inducible defense responses in Arabidopsis. Mol Plant Microbe Interact (2014).
56. Choi, D. S., Hwang, I. S. & Hwang, B. K. Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper. Plant Cell 24, 1675-1690 (2012).
57. Liu, Y., Schiff, M. & Dinesh-Kumar, S. P. Virus-induced gene silencing in tomato. Plant J 31, 777-786 (2002).
58. Choi, D. S. & Hwang, B. K. Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 23, 823-842 (2011).
59. Oh, S. H., Choi, W. G., Lee, I. T. & Yun, S. J. Cloning and characterization of a rice cDNA encoding glutamate decarboxylase. J Biochem Mol Biol 38, 595-601 (2005).
60. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45, 616-629 (2006).