The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Transcriptional Changes of Plant Defense-Related Genes in Response to Clavibacter Infection in Pepper and Tomato

  • Hwang, In Sun (Department of Horticultural Biotechnology, College of Life Science, Kyung Hee University) ;
  • Oh, Eom-Ji (Graduate School of Biotechnology, Kyung Hee University) ;
  • Oh, Chang-Sik (Department of Horticultural Biotechnology, College of Life Science, Kyung Hee University)
  • Received : 2020.07.10
  • Accepted : 2020.08.24
  • Published : 2020.10.01
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Abstract

Pepper and tomato plants infected with two Clavibacter species, C. capsici and C. michiganensis have shown different patterns of disease development depending on their virulence. Here, we investigated how pepper and tomato plants respond to infection by the high-virulent or low-virulent Clavibacter strains. For this, we chose two strains of each Clavibacter species to show different virulence level in the host plants. Although low-virulent strains showed less disease symptoms, they grew almost the same level as the high-virulent strains in both plants. To further examine the response of host plants to Clavibacter infection, we analyzed the expression patterns of plant defense-related genes in the leaves inoculated with different strains of C. capsici and C. michiganensis. Pepper plants infected with high-virulent C. capsici strain highly induced the expression of CaPR1, CaDEF, CaPR4b, CaPR10, and CaLOX1 at 5 days after inoculation (dai), but their expression was much less in low-virulent Clavibacter infection. Expression of CaSAR8.2 was induced at 2 dai, regardless of virulence level. Expression of GluA, Pin2, and PR2 in tomato plants infected with high-virulent C. michiganensis were much higher at 5 dai, compared with mock or low-virulent strain. Expression of PR1a, Osmotin-like, Chitinase, and Chitinase class 2 was increased, regardless of virulence level. Expression of LoxA gene was not affected by Clavibacter inoculation. These results suggested that Clavibacter infection promotes induction of certain defense-related genes in host plants and that differential expression of those genes by low-virulent Clavibacter infection might be affected by their endophytic lifestyle in plants.

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References

  1. Abramovitch, R. B., Anderson, J. C. and Martin, G. B. 2006. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 7:601-611. https://doi.org/10.1038/nrm1984
  2. Balaji, V., Mayrose, M., Sherf, O., Jacob-Hirsch, J., Eichenlaub, R., Iraki, N., Manulis-Sasson, S., Rechavi, G., Barash, I. and Sessa, G. 2008. Tomato transcriptional changes in response to Clavibacter michiganensis subsp. michiganensis reveal a role for ethylene in disease development. Plant Physiol. 146:1797-1809. https://doi.org/10.1104/pp.107.115188
  3. Bari, R. and Jones, J. D. G. 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69:473-488. https://doi.org/10.1007/s11103-008-9435-0
  4. Choi, H. W. and Hwang, B. K. 2015. Molecular and cellular control of cell death and defense signaling in pepper. Planta 241:1-27. https://doi.org/10.1007/s00425-014-2171-6
  5. Ciardi, J. A., Tieman, D. M., Lund, S. T., Jones, J. B., Stall, R. E. and Klee, H. J. 2000. Response to Xanthomonas campestris pv. vesicatoria in tomato involves regulation of ethylene receptor gene expression. Plant Physiol. 123:81-92. https://doi.org/10.1104/pp.123.1.81
  6. Do, H. M., Lee, S. C., Jung H. W., Sohn K. H. and Hwang B. K. 2004. 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 Sci. 166:1297-1305. https://doi.org/10.1016/j.plantsci.2004.01.008
  7. Dodds, P. N. and Rathjen, J. P. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548. https://doi.org/10.1038/nrg2812
  8. Eichenlaub, R. and Gartemann, K.-H. 2011. The Clavibacter michiganensis subspecies: molecular investigation of grampositive bacterial plant pathogens. Annu. Rev. Phytopathol. 49:445-464. https://doi.org/10.1146/annurev-phyto-072910-095258
  9. Gartemann, K.-H., Abt, B., Bekel, T., Burger, A., Engemann, J., Flugel, M., Gaigalat, L., Goesmann, A., Graen, I., Kalinowski, J., Kaup, O., Kirchner, O., Krause, L., Linke, B., McHardy, A., Meyer, F., Pohle, S., Ruckert, C., Schneiker, S., Zellermann, E.-M., Pühler, A., Eichenlaub, R., Kaiser, O. and Bartels, D. 2008. The genome sequence of the tomatopathogenic actinomycete Clavibacter michiganensis subsp. michiganensis NCPPB382 reveals a large island involved in pathogenicity. J. Bacteriol. 190:2138-2149. https://doi.org/10.1128/JB.01595-07
  10. Han, S. W. and Hwang, B. K. 2017. Molecular functions of Xanthomonas type III effector AvrBsT and its plant interactors in cell death and defense signaling. Planta 245:237-253. https://doi.org/10.1007/s00425-016-2628-x
  11. Herman, M. A. B., Davidson, J. K. and Smart, C. D. 2008. Induction of plant defense gene expression by plant activators and Pseudomonas syringae pv. tomato in greenhouse-grown tomatoes. Phytopathology 98:1226-1232. https://doi.org/10.1094/PHYTO-98-11-1226
  12. Hong, J. K., Hwang, I. S. and Hwang, B. K. 2017. Functional roles of the pepper leucine-rich repeat protein and its interactions with pathogenesis-related and hypersensitive-induced proteins in plant cell death and immunity. Planta 246:351-364. https://doi.org/10.1007/s00425-017-2709-5
  13. Hwang, I. S. and Hwang, B. K. 2010. The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol. 152:948-967. https://doi.org/10.1104/pp.109.147827
  14. Hwang, I. S., Lee, H. M., Oh, E.-J., Lee, S., Heu, S. and Oh, C.-S. 2020. Plasmid composition and the chpG gene determine the virulence level of Clavibacter capsici natural isolates in pepper. Mol. Plant Pathol. 21:808-819. https://doi.org/10.1111/mpp.12932
  15. Hwang, I. S., Oh, E.-J., Kim, D. and Oh, C.-S. 2018. Multiple plasmid-borne virulence genes of Clavibacter michiganensis ssp. capsici critical for disease development in pepper. New Phytol. 217:1177-1189. https://doi.org/10.1111/nph.14896
  16. Hwang, I. S., Oh, E.-J., Lee, H. B. and Oh, C.-S. 2019. Functional characterization of two cellulase genes in the gram-positive pathogenic bacterium Clavibacter michiganensis for wilting in tomato. Mol. Plant-Microbe Interact. 32:491-501. https://doi.org/10.1094/MPMI-08-18-0227-R
  17. Jahr, H., Dreier, J., Meletzus, D., Bahro, R. and Eichenlaub, R. 2000. The endo-beta-1,4-glucanase CelA of Clavibacter michiganensis subsp. michiganensis is a pathogenicity determinant required for induction of bacterial wilt of tomato. Mol. Plant-Microbe Interact. 13:703-714. https://doi.org/10.1094/MPMI.2000.13.7.703
  18. Jin, J.-H., Zhang, H.-X., Tan, J.-Y., Yan, M.-J., Li, D.-W., Khan, A. and Gong, Z.-H. 2015. A new ethylene-responsive factor CaPTI1 gene of pepper (Capsicum annuum L.) involved in the regulation of defense response to Phytophthora capsici. Front. Plant Sci. 6:1217. https://doi.org/10.3389/fpls.2015.01217
  19. Jones, J. D. G. and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  20. Kim, N. H., Choi, H. W. and Hwang, B. K. 2010. Xanthomonas campestris pv. vesicatoria effector AvrBsT induces cell death in pepper, but suppresses defense responses in tomato. Mol. Plant-Microbe Interact. 23:1069-1082. https://doi.org/10.1094/MPMI-23-8-1069
  21. Kim, S. H., Hong, J. K., Lee, S. C., Sohn, K. H., Jung, H. W. and Hwang, B. K. 2004. CAZFP1, Cys2/His2-type zinc-finger transcription factor gene functions as a pathogen-induced early-defense gene in Capsicum annuum. Plant Mol. Biol. 55:883-904. https://doi.org/10.1007/s11103-005-2151-0
  22. Lee, S. C. and Hwang, B. K. 2006. CASAR82A, a pathogeninduced pepper SAR8.2, exhibits an antifungal activity and its overexpression enhances disease resistance and stress tolerance. Plant Mol. Biol. 61:95-109. https://doi.org/10.1007/s11103-005-6102-6
  23. Lee, S.-D., Yoon, C.-M., Lee, Y.-K., Choi, Y.-H. and Cho, Y.-S. 1999. Occurrence and distribution of bacterial canker of red pepper caused by Clavibacter michiganensis subsp. michignensis. Plant Dis. Agric. 5:105-110.
  24. Li, X., Tambong, J., Yuan, K. X., Chen, W., Xu, H., Levesque, C. A., and De Boer, S. H. 2018. Re-classification of Clavibacter michiganensis subspecies on the basis of whole-genome and multi-locus sequence analyses. Int. J. Syst. Evol. Microbiol. 68:234-240. https://doi.org/10.1099/ijsem.0.002492
  25. Milling, A., Babujee, L. and Allen, C. 2011. Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS ONE 6:e15853. https://doi.org/10.1371/journal.pone.0015853
  26. Myung, I.-S., Kim, D. G., An, S. H., Lee, Y.-K. and Kim, W. G. 2008. First report of bacterial canker of tomato caused by Clavibacter michiganensis subsp. michiganensis in Korea. Plant Dis. 92:1472.
  27. Nandi, M., Macdonald, J., Liu, P., Weselowski, B. and Yuan, Z.-C. 2018. Clavibacter michiganensis ssp. michiganensis: bacterial canker of tomato, molecular interactions and disease management. Mol. Plant. Pathol. 19:2036-2050. https://doi.org/10.1111/mpp.12678
  28. Oh, E.-J., Bae, C., Lee, H.-B., Hwang, I. S., Lee, H.-I., Yea, M. C., Yim, K.-O., Lee, S., Heu, S., Cha, J.-S. and Oh, C.-S. 2016. Clavibacter michiganensis subsp. capsici subsp. nov., causing bacterial canker disease in pepper. Int. J. Syst. Evol. Microbiol. 66:4065-4070. https://doi.org/10.1099/ijsem.0.001311
  29. Potnis, N., Timilsina, S., Strayer, A., Shantharaj, D., Barak, J. D., Paret, M. L., Vallad, G. E. and Jones, J. B. 2015. Bacterial spot of tomato and pepper: diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Mol. Plant. Pathol. 16:907-920. https://doi.org/10.1111/mpp.12244
  30. Thapa, S. P., Davis, E. W., Lyu, Q., Weisberg, A. J., Stevens, D. M., Clarke, C. R., Coaker, G. and Chang, J. H. 2019. The evolution, ecology, and mechanisms of infection by gram-positive, plant-associated bacteria. Annu. Rev. Phytopathol. 57:341-365. https://doi.org/10.1146/annurev-phyto-082718-100124
  31. Thapa, S. P., Pattathil, S., Hahn, M. G., Jacques, M.-A., Gilbertson, R. L. and Coaker, G. 2017. Genomic analysis of Clavibacter michiganensis reveals insight into virulence strategies and genetic diversity of a gram-positive bacterial pathogen. Mol. Plant-Microbe Interact. 30:786-802. https://doi.org/10.1094/MPMI-06-17-0146-R
  32. Wang, J.-E., Li, D.-W., Zhang, Y.-L., Zhao, Q., He, Y.-M. and Gong, Z.-H. 2013. Defence responses of pepper (Capsicum annuum L.) infected with incompatible and compatible strains of Phytophthora capsici. Eur. J. Plant Pathol. 136:625-638. https://doi.org/10.1007/s10658-013-0193-8
  33. Yim, K.-O., Lee, H.-I., Kim, J.-H., Lee, S.-D., Cho, J.-H. and Cha, J.-S. 2012. Characterization of phenotypic variants of Clavibacter michiganensis subsp. michiganensis isolated from Capsicum annuum. Eur. J. Plant Pathol. 133:559-575. https://doi.org/10.1007/s10658-011-9927-7