The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Expression of hpa1 Gene Encoding a Bacterial Harpin Protein in Xanthomonas oryzae pv. oryzae Enhances Disease Resistance to Both Fungal and Bacterial Pathogens in Rice and Arabidopsis

  • Choi, Min-Seon (Department of Horticultural Biotechnology and Institute of Life Sciences & Resources, Kyung Hee University) ;
  • Heu, Sunggi (Microbial Safety Division, National Academy of Agricultural Science, Rural Development Administration) ;
  • Paek, Nam-Chon (Department of Plant Science, Seoul National University) ;
  • Koh, Hee-Jong (Department of Plant Science, Seoul National University) ;
  • Lee, Jung-Sook (Genomics Division, National Academy of Agricultural Science, Rural Development Administration) ;
  • Oh, Chang-Sik (Department of Horticultural Biotechnology and Institute of Life Sciences & Resources, Kyung Hee University)
  • Received : 2012.09.04
  • Accepted : 2012.09.23
  • Published : 2012.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

Xanthomonas oryzae pv. oryzae causing bacterial leaf blight disease in rice produces and secretes Hpa1 protein that belongs to harpin protein family. Previously it was reported that Hpa1 induced defense responses when it was produced in tobacco. In this study, we expressed hpa1 gene in rice and Arabidopsis to examine the effects of Hpa1 expression on disease resistance to both fungal and bacterial pathogens. Expression of hpa1 gene in rice enhanced disease resistance to both X. oryzae pv. oryzae and Magnaporthe grisea. Interestingly, individual transgenic rice plants could be divided into four groups, depending on responses to both pathogens. hpa1 expression in Arabidopsis also enhanced disease resistance to both Botrytis cineria and Xanthomonas campestris pv. campestris. To examine genes that are up-regulated in the transgenic rice plants after inoculation with X. oryzae pv. oryzae, known defense-related genes were assessed, and also microarray analysis with the Rice 5 K DNA chip was performed. Interestingly, expression of OsACS1 gene, which was found as the gene that showed the highest induction, was induced earlier and stronger than that in the wild type plant. These results indicate that hpa1 expression in the diverse plant species, including monocot and dicot, can enhance disease resistance to both fungal and bacterial plant pathogens.

Keywords

References

  1. Ahn, I. P., Kim, S., Kang, S., Suh, S. C. and Lee, Y. H. 2005a. Rice defense mechanisms against Cochliobolus miyabeanus and Magnaporthe grisea are distinct. Phytopathology 95: 1248-1255. https://doi.org/10.1094/PHYTO-95-1248
  2. Ahn, I. P., Kim, S. and Lee, Y. H. 2005b. Vitamin B1 functions as an activator of plant disease resistance. Plant Physiol. 138:1505-1515. https://doi.org/10.1104/pp.104.058693
  3. Alfano, J. R. and Collmer, A. 1997. The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J. Bacteriol. 179:5655-5662. https://doi.org/10.1128/jb.179.18.5655-5662.1997
  4. Arlat, M., Van Gijsegem, F., Huet, J. C., Pernollet, J. C. and Boucher, C. A. 1994. PopA1, a protein which induces a hypersensitivity- like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13:543-553.
  5. Beer, S. V., Wei, Z. M., Laby, R. J., He, S. Y., Bauer, D. W., Collmer, A. and Zumoff, C. 1993. Are harpins universal elicitors of the hypersensitive response of phytopathogenic bacteria? In Advances in molecular genetics of plant-microbe intractions, (ed. E. N. Nester and D. P. S. Verma), pp. 281-286. Dordrecht, The Netherlands: Kluwer Academic Publishers.
  6. Boyes, D. C., Zayed, A. M., Ascenzi, R., McCaskill, A. J., Hoffman, N. E., Davis, K. R. and Gorlach, J. 2001. Growth stagebased phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499- 1510. https://doi.org/10.1105/tpc.13.7.1499
  7. Cao, H., Bowling, S. A., Gordon, A. S. and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583- 1592. https://doi.org/10.1105/tpc.6.11.1583
  8. Charkowski, A. O., Alfano, J. R., Preston, G., Yuan, J., He, S. Y. and Collmer, A. 1998. The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J. Bacteriol. 180:5211-5217.
  9. Chuang, H., Harnrak, A., Chen, Y.-C. and Hsu, C.-M. 2010. A harpin-induced ethylene-responsive factor regulates plant growth and responses to biotic and abiotic stresses. Biochem. Biophys. Res. Commun. 402:414-420. https://doi.org/10.1016/j.bbrc.2010.10.047
  10. 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. https://doi.org/10.1046/j.1365-313x.1998.00343.x
  11. Delaney, T. P., Friedrich, L. and Ryals, J. A. 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA 95:6602-6606.
  12. Dong, H., Delaney, T. P., Bauer, D. W. and Beer, S. V. 1999. Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J. 20:207-215. https://doi.org/10.1046/j.1365-313x.1999.00595.x
  13. Dong, H. P., Peng, J., Bao, Z., Meng, X., Bonasera, J. M., Chen, G., Beer, S. V. and Dong, H. 2004. Downstream divergence of the ethylene signaling pathway for harpin-stimulated Arabidopsis growth and insect defense. Plant Physiol. 136:3628- 3638. https://doi.org/10.1104/pp.104.048900
  14. Durrant, W. E. and Dong, X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209. https://doi.org/10.1146/annurev.phyto.42.040803.140421
  15. Hammond-Kosack, K. E. and Parker, J. E. 2003. Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14:177-193. https://doi.org/10.1016/S0958-1669(03)00035-1
  16. He, S. Y., Huang, H.-C. and Collmer, A. 1993. Pseudomonas syringae pv. syringae $harpin_{pss}$: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-1266. https://doi.org/10.1016/0092-8674(93)90354-S
  17. Hiei, Y., Ohta, S., Komari, T. and Kumashiro, T. 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6:271-282. https://doi.org/10.1046/j.1365-313X.1994.6020271.x
  18. International Network for Genetic Evaluation of Rice and International Rice Research Institute. 1996. Standard evaluation system for rice. 4th ed. International Rice Research Institute, Manila, Philippines. 18 pp.
  19. Ji, Z., Song, C., Lu, X. and Wang, J. 2011. Two coiled-coil regions of Xanthomonas oryzae pv. oryzae harpin differ in oligomerization and hypersensitive response induction. Amino Acids 40:381-392. https://doi.org/10.1007/s00726-010-0643-y
  20. Keen, N. T. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447-463. https://doi.org/10.1146/annurev.ge.24.120190.002311
  21. Kim, J. F. and Beer, S. V. 1998. HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class. J. Bacteriol. 180:5203-5210.
  22. Kim, J. G., Park, B. K., Yoo, C. H., Jeon, E., Oh, J. and Hwang, I. 2003. Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J. Bacteriol. 185:3155- 3166. https://doi.org/10.1128/JB.185.10.3155-3166.2003
  23. Koh, Y. J., Hwang, B. K. and Chung, H. S. 1987. Adult-plant resistance of rice to leaf blast. Phytopathology 77:232-236. https://doi.org/10.1094/Phyto-77-232
  24. Kvitko, B. H., Ramos, A. R., Morello, J. E., Oh, H.-S. and Collmer, A. 2007. Identification of harpins in Pseudomonas syringae pv. tomato DC3000, which are functionally similar to HrpK1 in promoting translocation of type III secretion system effectors. J. Bacteriol. 189:8059-8072. https://doi.org/10.1128/JB.01146-07
  25. McElroy, D., Zhang, W., Cao, J. and Wu, R. 1990. Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163-171. https://doi.org/10.1105/tpc.2.2.163
  26. Miao, W., Wang, X., Song, C., Wang, Y., Ren, Y. and Wang, J. 2010. Transcriptome analysis of Hpa1Xoo transformed cotton revealed constitutive expression of genes in multiple signaling pathways related to disease resistance. J. Exp. Bot. 61:4263- 4275. https://doi.org/10.1093/jxb/erq227
  27. Noel, L., Thieme, F., Nennstiel, D. and Bonas, U. 2002. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J. Bacteriol. 184:1340-1348. https://doi.org/10.1128/JB.184.5.1340-1348.2002
  28. Peng, J. L., Bao, Z. L., Ren, H. Y., Wang, J. S. and Dong, H. S. 2004. Expression of harpin(xoo) in transgenic tobacco induces pathogen defense in the absence of hypersensitive cell death. Phytopathology 94:1048-1055. https://doi.org/10.1094/PHYTO.2004.94.10.1048
  29. Perino, C., Gaudriault, S., Vian, B. and Barny, M. A. 1999. Visualization of harpin secretion in planta during infection of apple seedlings by Erwinia amylovora. Cell Microbiol. 1:131-141. https://doi.org/10.1046/j.1462-5822.1999.00013.x
  30. Reymond, P., Weber, H., Damond, M. and Farmer, E. E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707-720. https://doi.org/10.1105/tpc.12.5.707
  31. Thomma, B. P. H. J., Eggermont, K., Penninckz, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A. and Broekaert, W. F. 1998. Separate jasmonate-dependent and salicylate- dependent defense response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95:15107-15111. https://doi.org/10.1073/pnas.95.25.15107
  32. Thomma, B. P. H. J., Eggermont, K., Tierens, K. F. M.-J. and Broekaert, W. F. 1999. Requirement of functional EIN2 (ethylene insensitive 2) gene for efficient resistance of Arabidopsis thaliana to infection by Botrytis cinerea. Plant Physiol. 121:1093-1101. https://doi.org/10.1104/pp.121.4.1093
  33. Wei, Z. M., Laby, R. J., Zumoff, C. H., Bauer, D. W., He, S. Y., Collmer, A. and Beer, S. V. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85-88. https://doi.org/10.1126/science.1621099
  34. Zarembinski, T. I. and Theologis, A. 1997. Expression characteristics of Os-ACS1 and Os-ACS2, two members of the 1-aminocyclopropane- 1-carboxylate synthase gene family in rice (Oryza sativa L. cv. Habiganj Aman II) during partial submergence. Plant Mol. Biol. 33:71-77. https://doi.org/10.1023/B:PLAN.0000009693.26740.c3
  35. Zhu, W., MaGbanua, M. M. and White, F. F. 2000. Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J. Bacteriol. 182:1844-1853. https://doi.org/10.1128/JB.182.7.1844-1853.2000

Cited by

  1. Enhancing Production of Terpenoids in Metabolically Engineered Transgenic Spearmint (Mentha spicata L.) by Salt and Fungal Elicitors vol.30, pp.2, 2014, https://doi.org/10.7747/JFS.2014.30.2.243
  2. Harpins, Multifunctional Proteins Secreted by Gram-Negative Plant-Pathogenic Bacteria vol.26, pp.10, 2013, https://doi.org/10.1094/MPMI-02-13-0050-CR
  3. The signal peptide-like segment of hpaXm is required for its association to the cell wall in transgenic tobacco plants vol.12, pp.1, 2017, https://doi.org/10.1371/journal.pone.0170931
  4. Overexpression of a harpin-encoding gene popW in tobacco enhances resistance against Ralstonia solanacearum vol.60, pp.1, 2016, https://doi.org/10.1007/s10535-015-0571-5
  5. Overexpression of SSBXoc, a Single-Stranded DNA-Binding Protein From Xanthomonas oryzae pv. oryzicola, Enhances Plant Growth and Disease and Salt Stress Tolerance in Transgenic Nicotiana benthamiana vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.00953
  6. Development of PSP1, a Biostimulant Based on the Elicitor AsES for Disease Management in Monocot and Dicot Crops vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.00844