DOI QR코드

DOI QR Code

Arabidopsis WRKY55 Transcription Factor Enhances Soft Rot Disease Resistance with ORA59

  • Ji Eun Kang (Department of Plant Biotechnology, College of Life Sciences & Biotechnology, Korea University) ;
  • Hyunsun Kim (National Institute of Agricultural Science, Rural Development Administration) ;
  • Kyungyoung Song (National Institute of Agricultural Science, Rural Development Administration) ;
  • Changhyun Choi (National Institute of Agricultural Science, Rural Development Administration) ;
  • Yun Ju Kim (Department of Systems Biology, Yonsei University) ;
  • Duk-Ju Hwang (National Institute of Agricultural Science, Rural Development Administration) ;
  • Eui-Hwan Chung (Department of Plant Biotechnology, College of Life Sciences & Biotechnology, Korea University)
  • Received : 2024.08.21
  • Accepted : 2024.09.03
  • Published : 2024.10.01

Abstract

Pectobacterium is a major bacterial causal agent leading to soft rot disease in host plants. With the Arabidopsis-Pectobacterium pathosystem, we investigated the function of an Arabidopsis thaliana WRKY55 during defense responses to Pectobacterium carotovorum ssp. carotovorum (Pcc). Pcc-infection specifically induced WRKY55 gene expression. The overexpression of WRKY55 was resistant to the Pcc infection, while wrky55 knockout plants compromised the defense responses against Pcc. WRKY55 expression was mediated via Arabidopsis COI1-dependent signaling pathway showing that WRKY55 can contribute to the gene expression of jasmonic acid-mediated defense marker genes such as PDF1.2 and LOX2. WRKY55 physically interacts with Arabidopsis ORA59 facilitating the expression of PDF1.2. Our results suggest that WRKY55 can function as a positive regulator for resistance against Pcc in Arabidopsis.

Keywords

Acknowledgement

We thank Ms. Eunyoung Park for her technical support. The working model in Fig. 6 was generated by BioRender. E-HC was supported by Korea University Grants (K2021521 & K2106871), the Korea University Insung Research Grant (K2128041), and the Institute of Life Science and Natural Resources, Korea University. DJH was funded by Wu Jang-Choon Project by the Rural Development Administration (PJ00785003).

References

  1. Aerts, N., Pereira Mendes, M. and Van Wees, S. C. M. 2021. Multiple levels of crosstalk in hormone networks regulating plant defense. Plant J. 105:489-504.
  2. Andreasson, E., Jenkins, T., Brodersen, P., Thorgrimsen, S., Petersen, N. H. T., Zhu, S., Qiu, J.-L., Micheelsen, P., Rocher, A., Petersen, M., Newman, M.-A., Bjorn Nielsen, H., Hirt, H., Somssich, I., Mattsson, O. and Mundy, J. 2005. The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 24:2579-2589.
  3. Bae, H., Lee, D. S. and Hwang, I. 2006. Dual targeting of xylanase to chloroplasts and peroxisomes as a means to increase protein accumulation in plant cells. J. Exp. Bot. 57:161-169.
  4. Bhaumik, S. and Gambhir, S. S. 2002. Optical imaging of Renilla luciferase reporter gene expression in living mice. Proc. Natl. Acad Sci. U. S. A. 99:377-382.
  5. Birkenbihl, R. P., Diezel, C. and Somssich, I. E. 2012. Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol. 159:266-285.
  6. Bouley, D. M., Ghori, N., Mercer, K. L., Falkow, S. and Ramakrishnan, L. 2001. Dynamic nature of host-pathogen interactions in Mycobacterium marinum granulomas. Infect. Immun. 69:7820-7831.
  7. Brader, G., Tas, E. and Palva, E. T. 2001. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol. 126:849-860.
  8. Caarls, L., Elberse, J., Awwanah, M., Ludwig, N. R., de Vries, M., Zeilmaker, T., Van Wees, S. C. M., Schuurink, R. C. and Van den Ackerveken, G. 2017. Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc. Natl. Acad. Sci. U. S. A. 114:6388-6393.
  9. Chen, L., Zhang, L., Xiang, S., Chen, Y., Zhang, H. and Yu, D. 2021. The transcription factor WRKY75 positively regulates jasmonate-mediated plant defense to necrotrophic fungal pathogens. J. Exp. Bot. 72:1473-1489.
  10. Chen, X., Liu, J., Lin, G., Wang, A., Wang, Z. and Lu, G. 2013. Overexpression of AtWRKY28 and AtWRKY75 in Arabidopsis enhances resistance to oxalic acid and Sclerotinia sclerotiorum. Plant Cell Rep. 32:1589-1599.
  11. Choi, C., Park, Y. H., Kwon, S. I., Yun, C., Ahn, I., Park, S. R. and Hwang, D.-J. 2014. Identification of AtWRKY75 as a transcriptional regulator in the defense response to Pcc through the screening of Arabidopsis activation-tagged lines. Plant Biotechnol. Rep. 8:183-192.
  12. Clough, S. J. and Bent, A. F. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.
  13. Cui, Q., Yan, X., Gao, X., Zhang, D.-M., He, H.-B. and Jia, G.-X. 2018. Analysis of WRKY transcription factors and characterization of two Botrytis cinerea-responsive LrWRKY genes from Lilium regale. Plant Physiol. Biochem. 127:525-536.
  14. Davidsson, P. R., Kariola, T., Niemi, O. and Palva, E. T. 2013. Pathogenicity of and plant immunity to soft rot pectobacteria. Front. Plant Sci. 4:191.
  15. Douet, V., Loiseau, L., Barras, F. and Py, B. 2004. Systematic analysis, by the yeast two-hybrid, of protein interaction between components of the type II secretory machinery of Erwinia chrysanthemi. Res. Microbiol. 155:71-75.
  16. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K. and Pikaard, C. S. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45:616-629.
  17. Egusa, M., Ozawa, R., Takabayashi, J., Otani, H. and Kodama, M. 2009. The jasmonate signaling pathway in tomato regulates susceptibility to a toxin-dependent necrotrophic pathogen. Planta 229:965-976.
  18. Eulgem, T., Rushton, P. J., Robatzek, S. and Somssich, I. E. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5:199-206.
  19. Ghorbel, M., Brini, F., Sharma, A. and Landi, M. 2021. Role of jasmonic acid in plants: the molecular point of view. Plant Cell Rep. 40:1471-1494.
  20. Gimenez-Ibanez, S., Boter, M. and Solano, R. 2015. Novel players fine-tune plant trade-offs. Essays Biochem. 58:83-100.
  21. He, X., Jiang, J., Wang, C.-Q. and Dehesh, K. 2017. ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. J. Integr. Plant Biol. 59:275-287.
  22. Howe, G. A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41-66.
  23. Kariola, T., Palomaki, T. A., Brader, G. and Palva, E. T. 2003. Erwinia carotovora subsp. carotovora and Erwinia-derived elicitors HrpN and PehA trigger distinct but interacting defense responses and cell death in Arabidopsis. Mol. PlantMicrobe Interact. 16:179-187.
  24. Kim, N. Y., Jang, Y. J. and Park, O. K. 2018. AP2/ERF family transcription factors ORA59 and RAP2.3 interact in the nucleus and function together in ethylene responses. Front. Plant Sci. 9:1675.
  25. Kravchenko, U., Gogoleva, N., Kalubaka, N., Kruk, A., Diubo, Y., Gogolev, Y. and Nikolaichik, Y. 2020. The PhoPQ two-component system is the major regulator of cell surface properties, stress responses and plant-derived substrate utilisation during development of Pectobacterium versatile-host plant pathosystems. Front. Microbiol. 11:621391.
  26. Li, G., Meng, X., Wang, R., Mao, G., Han, L., Liu, Y. and Zhang, S. 2012. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet. 8:e1002767.
  27. Liu, H., Coulthurst, S. J., Pritchard, L., Hedley, P. E., Ravensdale, M., Humphris, S., Burr, T., Takle, G., Brurberg, M.-B., Birch, P. R. J., Salmond, G. P. C. and Toth, I. K. 2008. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog. 4:e1000093.
  28. Liu, L., Sonbol, F.-M., Huot, B., Gu, Y., Withers, J., Mwimba, M., Yao, J., He, S. Y. and Dong, X. 2016. Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nat. Commun. 7:13099.
  29. Maeo, K., Hayashi, S., Kojima-Suzuki, H., Morikami, A. and Nakamura, K. 2001. Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. Biosci. Biotechnol. Biochem. 65:2428-2436.
  30. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z. and Zhang, S. 2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639-1653.
  31. Moleleki, L. N., Pretorius, R. G., Tanui, C. K., Mosina, G. and Theron, J. 2017. A quorum sensing-defective mutant of Pectobacterium carotovorum ssp. brasiliense 1692 is attenuated in virulence and unable to occlude xylem tissue of susceptible potato plant stems. Mol. Plant Pathol. 18:32-44.
  32. Norman-Setterblad, C., Vidal, S. and Palva, E. T. 2000. Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol. Plant-Microbe Interact. 13:430-438.
  33. Pandey, S. P. and Somssich, I. E. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiol. 150:1648-1655.
  34. Park, Y. H., Choi, C., Park, E. M., Kim, H. S., Park, H. J., Bae, S. C., Ahn, I., Kim, M. G., Park, S. R. and Hwang, D.-J. 2012. Over-expression of rice leucine-rich repeat protein results in activation of defense response, thereby enhancing resistance to bacterial soft rot in Chinese cabbage. Plant Cell Rep. 31:1845-1850.
  35. Perombelon, M. C. M. 2002. Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol. 51:1-12.
  36. Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A. and Van Wees, S. C. M. 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489-521.
  37. Po-Wen, C., Singh, P. and Zimmerli, L. 2013. Priming of the Arabidopsis pattern-triggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Mol. Plant Pathol. 14:58-70.
  38. Pollumaa, L., Alamae, T. and Mae, A. 2012. Quorum sensing and expression of virulence in pectobacteria. Sensors (Basel) 12:3327-3349.
  39. Pre, M., Atallah, M., Champion, A., De Vos, M., Pieterse, C. M. J. and Memelink, J. 2008. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147:1347-1357.
  40. Qiu, D., Xiao, J., Ding, X., Xiong, M., Cai, M., Cao, Y., Li, X., Xu, C. and Wang, S. 2007. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol. Plant-Microbe Interact. 20:492-499.
  41. Qiu, D., Xiao, J., Xie, W., Cheng, H., Li, X. and Wang, S. 2009. Exploring transcriptional signalling mediated by OsWRKY13, a potential regulator of multiple physiological processes in rice. BMC Plant Biol. 9:74.
  42. Qiu, J.-L., Fiil, B. K., Petersen, K., Nielsen, H. B., Botanga, C. J., Thorgrimsen, S., Palma, K., Suarez-Rodriguez, M. C., Sandbech-Clausen, S., Lichota, J., Brodersen, P., Grasser, K. D., Mattsson, O., Glazebrook, J., Mundy, J. and Petersen, M. 2008. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27:2214-2221.
  43. Robert-Seilaniantz, A., Grant, M. and Jones, J. D. G. 2011. Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu. Rev. Phytopathol. 49:317-343.
  44. Sasaki-Sekimoto, Y., Jikumaru, Y., Obayashi, T., Saito, H., Masuda, S., Kamiya, Y., Ohta, H. and Shirasu, K. 2013. Basic helix-loop-helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol. 163:291-304.
  45. Singh, A. A., Singh, A. K. and Nerurkar, A. 2021. Disrupting the quorum sensing mediated virulence in soft rot causing Pectobacterium carotovorum by marine sponge associated Bacillus sp. OA10. World J. Microbiol. Biotechnol. 37:5.
  46. Torres, M. A., Dangl, J. L. and Jones, J. D. G. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. U. S. A. 99:517-522.
  47. Van der Does, D., Leon-Reyes, A., Koornneef, A., Van Verk, M. C., Rodenburg, N., Pauwels, L., Goossens, A., Korbes, A. P., Memelink, J., Ritsema, T., Van Wees, S. C. M. and Pieterse, C. M. J. 2013. Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744-761.
  48. Walter, M., Chaban, C., Schutze, K., Batistic, O., Weckermann, K., Nake, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K. and Kudla, J. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40:428-438.
  49. Wani, S. H., Anand, S., Singh, B., Bohra, A. and Joshi, R. 2021. WRKY transcription factors and plant defense responses: latest discoveries and future prospects. Plant Cell Rep. 40:1071-1085.
  50. Xu, P., Wang, H., Qin, C., Li, Z., Lin, C., Liu, W. and Miao, W. 2021. Analysis of the taxonomy and pathogenic factors of Pectobacterium aroidearum L6 using whole-genome sequencing and comparative genomics. Front. Microbiol. 12:679102.
  51. Yamasaki, K., Kigawa, T., Inoue, M., Tateno, M., Yamasaki, T., Yabuki, T., Aoki, M., Seki, E., Matsuda, T., Tomo, Y., Hayami, N., Terada, T., Shirouzu, M., Tanaka, A., Seki, M., Shinozaki, K. and Yokoyama, S. 2005. Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17:944-956.
  52. Yan, J., Yao, R., Chen, L., Li, S., Gu, M., Nan, F. and Xie, D. 2018. Dynamic perception of jasmonates by the F-Box protein COI1. Mol. Plant 11:1237-1247.
  53. Yang, Y. N., Kim, Y., Kim, H., Kim, S. J., Cho, K.-M., Kim, Y., Lee, D. S., Lee, M.-H., Kim, S. Y., Hong, J. C., Kwon, S. J., Choi, J. and Park, O. K. 2021. The transcription factor ORA59 exhibits dual DNA binding specificity that differentially regulates ethylene- and jasmonic acid-induced genes in plant immunity. Plant Physiol. 187:2763-2784.
  54. Zarei, A., Korbes, A. P., Younessi, P., Montiel, G., Champion, A. and Memelink, J. 2011. Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol. Biol. 75:321-331.
  55. Zheng, Z., Qamar, S. A., Chen, Z. and Mengiste, T. 2006. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 48:592-605.