The Plant Pathology Journal

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

DOI QR Code

An Acidic PATHOGENESIS-RELATED1 Gene of Oryza grandiglumis is Involved in Disease Resistance Response Against Bacterial Infection

  • Shin, Sang Hyun (National Crop Experiment Station, Rural Development Administration) ;
  • Pak, Jung-Hun (Department of Genetic Engineering, Dong-A University) ;
  • Kim, Mi Jin (Department of Genetic Engineering, Dong-A University) ;
  • Kim, Hye Jeong (Department of Genetic Engineering, Dong-A University) ;
  • Oh, Ju Sung (Department of Genetic Engineering, Dong-A University) ;
  • Choi, Hong Kyu (Department of Genetic Engineering, Dong-A University) ;
  • Jung, Ho Won (Department of Genetic Engineering, Dong-A University) ;
  • Chung, Young Soo (Department of Genetic Engineering, Dong-A University)
  • Received : 2013.11.27
  • Accepted : 2014.02.18
  • Published : 2014.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Wild rice, Oryza grandiglumis shows hyper-resistance response to pathogen infection. In order to identify genes necessary for defense response in plants, we have carried out a subtractive hybridization coupled with a cDNA macroarray. An acidic PATHOGENESIS-RELATED1 (PR1) gene of the wild rice is highly identical to the acidic PR1 genes of different plant species. The OgPR1a cDNA has an apparent single open reading frame with a predicted molecular mass 40,621 Da and an isoelectic point of 5.14. Both in silico analysis and a transient expression assay in onion epidermal cells revealed that the OgPR1a protein could be localized in intercellular space in plants. The OgPR1a mRNA was strongly transcribed by the exogenous treatment with ethylene and jasmonic acid as well as protein phosphatase inhibitors. Additionally, ectopic expression of the OgPR1a conferred disease resistance on Arabidopsis to the bacterial and fungal infections.

Keywords

References

  1. Agrawal, G. K., Jwa, N. S. and Rakwal, R. 2000. A novel rice (Oryza sativa L.) acidic PR1 gene highly responsive to cut, phytohormones, and protein phosphatase inhibitors. Biochem. Biophys. Res. Commun. 274:157-165. https://doi.org/10.1006/bbrc.2000.3114
  2. Alexander, D., Goodman, R. M., Gut-Rella, M., Glascock, C., Weymann, K., Friedrich, L., Maddox, D., Ahl-Goy, P., Luntz, T., Ward, E. and Ryals, J. 1993. Increased tolerance to 2 oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein-1a. Proc. Natl. Acad, Sci. USA. 90:7327-7331. https://doi.org/10.1073/pnas.90.15.7327
  3. Basja, J., Pan, Z. and Duke, S. O. 2011. Transcriptional responses to cantharidin, a protein phosphatase inhibitor, in Arabidopsis thaliana reveal the involvement of multiple signal transduction pathway. Physiol. Plant. 143:188-205. https://doi.org/10.1111/j.1399-3054.2011.01494.x
  4. Brederode, F. T., Linthorst, H. J. M. and Bol. J. F. 1991. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol. Biol. 17:1117-1125. https://doi.org/10.1007/BF00028729
  5. Buchel, A. S. and Linthorst, H. J. M. 1999. PR1: a group of plant proteins induced upon pathogen infection. In: Pathogenesisrelated proteins in plants, eds. By S. K. Datta and S. Muthukrishnan, pp. 21-47. CRC Press, United States.
  6. Carr, P., Dixon, D. C., Nikolau, B. J., Voelkerding, K. V. and Klessig, D. F. 1987. Synthesis and localization of pathogenesis-related proteins in tobacco. Mol. Cell. Biol. 7:1580-1583. https://doi.org/10.1128/MCB.7.4.1580
  7. Clough, S. H. 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
  8. Conrath, U., Silva, H. and Klessig, D. F. 1997. Protein dephosphorylation mediates salicylic acid-induced expression of PR-1 genes in tobacco. Plant J. 11:747-757. https://doi.org/10.1046/j.1365-313X.1997.11040747.x
  9. Cornelissen, B. J. C., Horowitz, J., Van Kan, J. A. L., Goldberg, R. and Bol. J. F. 1987. Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucleic acids Res. 15:6799-6811. https://doi.org/10.1093/nar/15.17.6799
  10. David, S. J. and Vierstra, R. D. 1996. Soluble derivatives of green fluorescent protein (GFP) for use in Arabidopsis thaliana. Weeds World 3:43-48.
  11. De Vos, M., Van Oosten, V. R., Van Poecke, R. M., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Metraux, J. P., Van Loon, L. C., Dicke, M. and Pieterse, C. M. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18:923-937. https://doi.org/10.1094/MPMI-18-0923
  12. Denance, N., Sanchez-Vallet, A., Goffner, D. and Molina, A. 2013. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant Sci. 4:155.
  13. Diaz, J., ten Have, A. and Van Kan, J. A. L. 2002. The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol. 129:1341-1351. https://doi.org/10.1104/pp.001453
  14. Han, S. W. and Jung, H. W. 2013. Molecular sensors for plant immunity; pattern recognition receptors and race-specific resistance proteins. J. Plant Biol. 56:357-366. https://doi.org/10.1007/s12374-013-0323-z
  15. Jeon, E. H., Pak, J. H., Kim, M. J., Kim, H. J., Shin, S. H., Lee, J. H., Kim, D. H., Oh, J. S., Oh, B. J., Jung, H. W. and Chung, Y. S. 2012. Ectopic expression of ubiquitin-conjugating enzyme gene from wild rice, OgUBC1, confers resistance against UV-B radiation and Botrytis infection in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 427:309-314. https://doi.org/10.1016/j.bbrc.2012.09.048
  16. Jones, J. D. G. and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  17. Jung, H. W. and Hwang, B. K. 2000. Isolation, partial sequencing, and expression of pathogenesis-related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. vesicatoria. Mol. Plant-Microbe Interact. 13:136-142. https://doi.org/10.1094/MPMI.2000.13.1.136
  18. Jung, H. W., Lim, C. W., Lee, S. C., Choi, H. W., Hwang, C. H. and Hwang, B. K. 2008. Distinct roles of the pepper hypersensitive induced reaction protein gene CaHIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses. Planta 227:409-425.
  19. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J. and Greenberg, J. T. 2009. Priming in systemic plant immunity.Science 324:89-91. https://doi.org/10.1126/science.1170025
  20. Katagiri, F. and Tsuda, K. 2010. Understanding the plant immune system. Mol. Plant-Microbe Interact. 23:1531-1536. https://doi.org/10.1094/MPMI-04-10-0099
  21. Kawahara, Y., Oono, Y., Kanamori, H., Matsumoto, T., Itoh, T. and Minami, E. 2012. Simultaneous RNA-Seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS ONE 7:e49423. https://doi.org/10.1371/journal.pone.0049423
  22. Kim, K. M., Cho, S. K., Shin, S. H., Kim, G. T., Lee, J. H., Oh, B. J., Kang, K. H., Hong, J. C., Choi, J. Y., Shin, J. S. and Chung, Y. S. 2005. Analysis of differentially expressed transcripts of fungal elicitor- and wound-treated wild rice (Oryza grandiglumis). J. Plant Res. 118:347-354. https://doi.org/10.1007/s10265-005-0228-0
  23. Kim, Y. J. and Hwang, B. K. 2000. Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiol. Plant. 108:51-60. https://doi.org/10.1034/j.1399-3054.2000.108001051x./
  24. Li, L., Li, C., Lee, G. I. and Howe, G. A. 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc. Natl. Acad. Sci. USA. 99:6416-6421. https://doi.org/10.1073/pnas.072072599
  25. Linthorst, H. J., Meuwissen, R. L., Kauffmann, S. and Bol. J. F. 1989. Constitutive expression of pathogenesis-related proteins PR1, GRP, and PR-5 in tobacco has no effect on virus infection. Plant Cell 1:285-291. https://doi.org/10.1105/tpc.1.3.285
  26. Mitsuhara, I., Iwai, T., Seo, S., Yanagawa, Y., Kawahigasi, H., Hirose, S., Ohkawa, Y. and Ohashi, Y. 2008. Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol. Genet. Genomics 279:415-427. https://doi.org/10.1007/s00438-008-0322-9
  27. Niderman, T., Genetet, I., Bruyere, T., Gees, R., Stinzi, A., Legrand, M., Fritig, B. and Mosinger, E. 1995. Pathogenesis-related PR1-proteins are antifungal. Isolation and characterization of three 14 kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol. 108:17-27. https://doi.org/10.1104/pp.108.1.17
  28. Parent, J. G. and Asselin, A. 1984. Detection of pathogenesisrelated proteins (PR or b) and of other proteins in the intercellular fluid of hypersensitive plants infected with Tobacco mosaic virus. Can. J. Bot. 52:564-569.
  29. Payne, G., Middlesteadt, W., Desai, N., Williams, S., Dincher, S., Carnes, J. and Ryals, J. 1989. Isolation and sequence of a genomic clone encoding the basic form of pathogenesis-related protein 1 from Nicotiana tabacum. Plant Mol. Biol. 12:595-596. https://doi.org/10.1007/BF00036973
  30. Reymond, P. and Farmer, E. E. 1998. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1:404-411. https://doi.org/10.1016/S1369-5266(98)80264-1
  31. Sarowar, S., Kim, Y. J., Kim, W. N., Kim, K. D., Hwagn, B. K., Islam, R. and Shin, J. S. 2005. Overexpression of a pepper basic pathogenesis-related 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep. 24:216-224. https://doi.org/10.1007/s00299-005-0928-x
  32. Sessa, G., Yang, X. Q., Raz, V., Eyal, Y. and Fluhr, R. 1995. Darkinduction and subcellular localization of the pathogenesisrelated PRB-1b protein. Plant Mol. Biol. 28:537-547. https://doi.org/10.1007/BF00020400
  33. Shin, S. H., Pak, J. H., Kim, M. J., Kim, H. J., Lee, J. H., Kim, D. H., Choi, H. K., Kang, K. H., Jeong, J. U., Kang, C. S., Jung H. W. and Chung, Y. S. 2012. Cloning and characterization of pathogenesis-related gene 10a (OgPR10a) derived from wild rice (Oryza grandiglumis). Kor. J. Breed. Sci. 44:1-10.
  34. Spoel, S. H. and Dong, X. 2012. How do plants achieve immunity? Defense without specialized immune cells. Nat. Rev. Immun. 12:89-100. https://doi.org/10.1038/nri3141
  35. Takeuchi, Y., Dotson, M. and Keen, N. T. 1992. Plant transformation: a simple particle bombardment device based on flowing helium. Plant Mol. Biol. 18:835-839. https://doi.org/10.1007/BF00020031
  36. Van Loon, L. C. and Van Kammen, A. 1970. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. 'Samsun' and 'Samsun NN'. II. Changes in protein constitution after infection with Tobacco mosaic virus. Virology 40:199-211. https://doi.org/10.1016/0042-6822(70)90395-8
  37. Van Loon, L. C. and Van Strien, E. A. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55:85-97. https://doi.org/10.1006/pmpp.1999.0213
  38. Van Loon, L. C., Rep, M. and Pieterse, C. M. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-162. https://doi.org/10.1146/annurev.phyto.44.070505.143425
  39. Zhang, J., Du, X., Wang, Q., Chen, X., Lv, D., Xu, K., Qu, S. and Zhang, Z. 2010. Expression of pathogenesis related genes in response to salicylic acid, methyl jasmonate and 1aminocyclopropane-1carboxylic acid in Malus hupehensis (Pamp.) Rehd. BMC Res. Notes 3:208. https://doi.org/10.1186/1756-0500-3-208

Cited by

  1. Emerging Insights into the Functions of Pathogenesis-Related Protein 1 vol.22, pp.10, 2017, https://doi.org/10.1016/j.tplants.2017.06.013
  2. Molecular Cloning of HbPR-1 Gene from Rubber Tree, Expression of HbPR-1 Gene in Nicotiana benthamiana and Its Inhibition of Phytophthora palmivora vol.11, pp.6, 2016, https://doi.org/10.1371/journal.pone.0157591