The Plant Pathology Journal

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

DOI QR Code

Suppression of UDP-glycosyltransferase-coding Arabidopsis thaliana UGT74E2 Gene Expression Leads to Increased Resistance to Psuedomonas syringae pv. tomato DC3000 Infection

  • Park, Hyo-Jun (Plant Signaling Network Research Center, School of Life Sciences and Biotechnology, Korea University) ;
  • Kwon, Chang-Seob (Department of Chemistry and Biology, Korea Science Academy of KAIST) ;
  • Woo, Joo-Yong (Plant Signaling Network Research Center, School of Life Sciences and Biotechnology, Korea University) ;
  • Lee, Gil-Je (Plant Signaling Network Research Center, School of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Young-Jin (Plant Signaling Network Research Center, School of Life Sciences and Biotechnology, Korea University) ;
  • Paek, Kyung-Hee (Plant Signaling Network Research Center, School of Life Sciences and Biotechnology, Korea University)
  • Received : 2011.01.04
  • Accepted : 2011.04.13
  • Published : 2011.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Plants possess multiple resistance mechanisms that protect themselves against pathogen attack. To identify unknown components of the defense machinery in Arabidopsis, gene-expression changes were monitored in Arabidopsis thaliana under 18 different biotic or abiotic conditions using a DNA microarray representing approximately 25% of all Arabidopsis thaliana genes (www.genevestigator.com). Seventeen genes which are early responsive to salicylic acid (SA) treatment as well as pathogen infection were selected and their T-DNA insertion mutants were obtained from SALK institute. To elucidate the role of each gene in defense response, bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000 was inoculated onto individual T-DNA insertion mutants. Four mutants exhibited decreased resistance and five mutants displayed significantly enhanced resistance against Pst DC3000-infection as measured by change in symptom development as compared to wild-type plants. Among them, member of uridin diphosphate (UDP)-glycosyltransferase (UGT) was of particular interest, since a UGT mutant (At1g05680) showed enhanced resistance to Pst-infection in Arabidopsis. In systemic acquired resistance (SAR) assay, this mutant showed enhanced activation of SAR. Also, the enhanced SAR correlated with increased expression of defense-related gene, AtPR1. These results emphasize that the glycosylation of UGT74E2 is a part of the SA-mediated disease-resistance mechanism.

Keywords

References

  1. Beckers, G. J. M. and Spoel, S. H. 2006. Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol. 8:1-10. https://doi.org/10.1055/s-2005-872705
  2. Chong, J., Baltz, R., Schmitt, C., Beffa, R., Fritig, B. and Saindrenan, P. 2002. Downregulation of a pathogen-responsive tobacco UDP-glc: phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 14:1093-1107. https://doi.org/10.1105/tpc.010436
  3. Dangl, J. L. and Jones, J. D. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-833. https://doi.org/10.1038/35081161
  4. Dean, J. V., Mohammed, L. A. and Fitzpatrick, T. 2005. The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221:287-296. https://doi.org/10.1007/s00425-004-1430-3
  5. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247-1250. https://doi.org/10.1126/science.266.5188.1247
  6. Dempsey, D., Shah, J.and Klessig, D. 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci. 18:547-575. https://doi.org/10.1080/07352689991309397
  7. 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
  8. Falk, A., Feys, B. J., Frost, L. N., Jones, J., Daniels, M. J. and Parker, J. E. 1999. EDS1, an essential component of R genemediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA 96:3292-3297. https://doi.org/10.1073/pnas.96.6.3292
  9. Ferrari, S., Plotnikova, J. M., De Lorenzo, G. and Ausubel, F. M. 2003. Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35:193-205. https://doi.org/10.1046/j.1365-313X.2003.01794.x
  10. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754-756. https://doi.org/10.1126/science.261.5122.754
  11. Gachon, C., Baltz, R. and Saindrenan, P. 2004. Over-expression of a scopoletin glucosyltransferase in Nicotiana tabacum leads to precocious lesion formation during the hypersensitive response to tobacco mosaic virus but does not affect virus resistance. Plant. Mol. Biol. 54:137-146. https://doi.org/10.1023/B:PLAN.0000028775.58537.fe
  12. Gachon, C., Langlois-Meurinne, M. and Saindrenan, P. 2005. Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci. 10:542-549. https://doi.org/10.1016/j.tplants.2005.09.007
  13. Glazebrook, J. G. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 19:309-331.
  14. Hancock, J. G. and Huisman, O. C. 1981. Nutrient movement in host-pathogen systems. Annu. Rev. Phytopathol. 19:309-331. https://doi.org/10.1146/annurev.py.19.090181.001521
  15. Jackson, R. G., Lim, E.-K., Li, Y., Kowalczyk, M., Sandberg, G., Hoggett, J., Ashford, D. A. and Bowles, D. J. 2001. Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glycosyltransferase. J. Biol. Chem. 276:4350-4356 https://doi.org/10.1074/jbc.M006185200
  16. Jones, J. D. and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  17. Katagiri, F., Thilmony, R. and He, S. Y. 2002. The Arabidopsis thaliana-Pseudomonassyringae Interaction. In The Arabidopsis Book, Somervill C.R., Meyerowitz E.M., eds. (Rockville, American Society of Plant Biologists), pp. 1-35.
  18. Kunkel, B. N. and Brooks, D. M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325-331. https://doi.org/10.1016/S1369-5266(02)00275-3
  19. Langlois-Meurinne, M., Gachon, C. and Saindrenan, P. 2005. Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiol. 139:1890-1901. https://doi.org/10.1104/pp.105.067223
  20. Lee, B. J., Kim, S. K., Choi, S. B., Bae, J., Kim, K. J., Kim, Y. J. and Paek, K. H. 2009. Pathogen-inducible CaUGT1 is involved in resistance response against TMV infection by controlling salicylic acid accumulation. FEBS Lett. 13:2315-2320.
  21. Lee, H. I. and Raskin, I. 1999. Purification, cloning, and expression of a pathogen inducible UDP-glucose: salicylic acid glucosyltransferase from tobacco. J. Biol. Chem. 274:36637-36642.
  22. Lim, E. K. and Bowles, D. J. 2004. A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J. 23:2915-2922. https://doi.org/10.1038/sj.emboj.7600295
  23. Liu, Y., Schiff, M. and Kumar, D. 2002. Virus-induced gene silencing in tomato. Plant J. 31:777-786. https://doi.org/10.1046/j.1365-313X.2002.01394.x
  24. Loake, G. and Grant, M. 2007. Salicylic acid in plant defence: the players and protagonists. Curr. Opin. Plant Biol. 10:466-472. https://doi.org/10.1016/j.pbi.2007.08.008
  25. Ma, L., Liu, B., Gao, D., Pang, X., Lu, S., Yu, H., Wang, H., Yan, F., Li, Z., Li, Y. and Ye, H. 2007. Molecular cloning and overexpression of a novel UDP-glucosyltransferase elevating salidroside levels in Rhodiola sachalinensis. Plant Cell Rep. 26:989-999. https://doi.org/10.1007/s00299-007-0317-8
  26. Mou, Z., Fan, W. and Dong, X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-944. https://doi.org/10.1016/S0092-8674(03)00429-X
  27. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O. and Jones, J. D. G. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436-439. https://doi.org/10.1126/science.1126088
  28. O'Donnell, P. J., Schmelz, E. A., Moussatche, P., Lund, S. T., Jones, J. B. and Klee, H. J. 2003. Susceptible to intolerance-a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J. 33:245-257. https://doi.org/10.1046/j.1365-313X.2003.01619.x
  29. Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S. and Klessig, D. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113-116. https://doi.org/10.1126/science.1147113
  30. Quiel, J. A. and Bender, J. 2003. Glucose conjugation of anthranilate by Arabidopsis UGT74F2 glucosyltransferase is required for tryptophan mutant blue fluorescence. J. Biol. Chem. 278:6275-6281. https://doi.org/10.1074/jbc.M211822200
  31. Radman, J. C., Haas, B. J., Tanimoto, G. and Town, C. D. 2004. Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. Plant J. 38:545-561. https://doi.org/10.1111/j.1365-313X.2004.02061.x
  32. Ross, A. F. 1961. Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14:329-339. https://doi.org/10.1016/0042-6822(61)90318-X
  33. Ross, J., Li, Y., Lim, E. and Bowles, D. J. 2001. Higher plant glycosyltransferases. Genome Biol. 2:30041-30046.
  34. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E. and Williamson, V. M. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA 95:9750-9754. https://doi.org/10.1073/pnas.95.17.9750
  35. Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y. and Shinozaki, K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61-72. https://doi.org/10.1105/tpc.13.1.61
  36. Shulaev, V., Silverman, P. and Raskin, I. 1997. Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718-721. https://doi.org/10.1038/385718a0
  37. Song, J. T. 2006. Induction of a salcyclic acid glucosyltransferase, AtSGT1, is an early disease response in Arabidopsis thaliana. Mol. Cells 22:233-238.
  38. Spoel, S. H., Koornneef, A., Claessens, M. C., Korzelius, J. P., Van Pelt, J. A., Mueller, M. J., Buchala, A. J., Metraux, J., Brown, R., Kazan, K., Van Loon, L. C., Dong, X. and Pietersela, C. 2003. NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760-770. https://doi.org/10.1105/tpc.009159
  39. Spoel, S. H., Johnson, J. S. and Dong, X. 2007. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl. Acad. Sci. USA 104:18842-18847. https://doi.org/10.1073/pnas.0708139104
  40. Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou Z., Song, J. and Dong, X. 2008. Plant Immunity Requires Conformational Changes of NPR1 via S-Nitrosylation and Thioredoxins. Science 321:952-956. https://doi.org/10.1126/science.1156970
  41. The Arabidopsis Genome Initiative 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815. https://doi.org/10.1038/35048692
  42. Thilmony, R., Underwood, W. and He, S. Y. 2006. Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J. 46:34-53. https://doi.org/10.1111/j.1365-313X.2006.02725.x
  43. Tognetti, V., Van Aken, O., Morreel, K., Vandenbroucke, K., Van De Cotte, B., De Clercq, I., Chiwocha, S., Fenske, R., Prinsen, E., Boerjan, W., Genty, B., Stubbs, K., Inze, D. and Van Breusegem, F. 2010. Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22:2660-2679. https://doi.org/10.1105/tpc.109.071316
  44. Vernooij, B., Friedrich, L., Morse, A., Reist, R., KolditzJawhar, R., Ward, E., Uknes, S., Kessmann, H. and Ryals, J. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 7:959-965.
  45. Wang, R., Guegler, K., LaBrie, S. T. and Crawford, N. M. 2000. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491-1509. https://doi.org/10.1105/tpc.12.8.1491
  46. Wang, D., Pajerowska-Mukhtar, K., Culler, A. H. and Dong, X. 2007. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17:1784-1790. https://doi.org/10.1016/j.cub.2007.09.025
  47. Wildermuth, M. C., Dewdney, J., Wu, G. and Ausubel, F. M. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565. https://doi.org/10.1038/35107108
  48. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. 2004. GENEVESTIGATOR Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136:2621-2632. https://doi.org/10.1104/pp.104.046367

Cited by

  1. Dissecting the genetic architecture of Fusarium verticillioides seed rot resistance in maize by combining QTL mapping and genome-wide association analysis vol.7, 2017, https://doi.org/10.1038/srep46446
  2. Dynamics of Membrane Potential Variation and Gene Expression Induced by Spodoptera littoralis, Myzus persicae, and Pseudomonas syringae in Arabidopsis vol.7, pp.10, 2012, https://doi.org/10.1371/journal.pone.0046673
  3. The Effect on the Transcriptome of Anemone coronaria following Infection with Rust (Tranzschelia discolor) vol.10, pp.3, 2015, https://doi.org/10.1371/journal.pone.0118565
  4. Substrate specificity and safener inducibility of the plant UDP-glucose-dependent family 1 glycosyltransferase super-family 2017, https://doi.org/10.1111/pbi.12775
  5. Molecular Basis of Endophytic Bacillus megaterium-induced Growth Promotion in Arabidopsis thaliana: Revelation by Microarray-based Gene Expression Analysis vol.36, pp.1, 2017, https://doi.org/10.1007/s00344-016-9624-z
  6. Role of two UDP-Glycosyltransferases from the L group of arabidopsis in resistance against pseudomonas syringae vol.139, pp.4, 2014, https://doi.org/10.1007/s10658-014-0424-7
  7. in rice vol.8, pp.60, 2018, https://doi.org/10.1039/C8RA04993A