The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Identification and Expression Profiles of Six Transcripts Encoding Carboxylesterase Protein in Vitis flexuosa Infected with Pathogens

  • Islam, Md. Zaherul (Department of Horticulture and Life Science, Yeungnam University) ;
  • Yun, Hae Keun (Department of Horticulture and Life Science, Yeungnam University)
  • Received : 2015.11.12
  • Accepted : 2016.04.04
  • Published : 2016.08.01
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Abstract

Plants protect themselves from pathogen attacks via several mechanisms, including hypersensitive cell death. Recognition of pathogen attack by the plant resistance gene triggers expression of carboxylesterase genes associated with hypersensitive response. We identified six transcripts of carboxylesterase genes, Vitis flexuosa carboxylesterase 5585 (VfCXE5585), Vf-CXE12827, VfCXE13132, VfCXE17159, VfCXE18231, and VfCXE47674, which showed different expression patterns upon transcriptome analysis of V. flexuosa inoculated with Elsinoe ampelina. The lengths of genes ranged from 1,098 to 1,629 bp, and their encoded proteins consisted of 309 to 335 amino acids. The predicted amino acid sequences showed hydrolase like domains in all six transcripts and contained two conserved motifs, GXSXG of serine hydrolase characteristics and HGGGF related to the carboxylesterase family. The deduced amino acid sequence also contained a potential catalytic triad consisted of serine, aspartic acid and histidine. Of the six transcripts, Vf-CXE12827 showed upregulated expression against E. ampelina at all time points. Three genes (VfCXE5585, VfCXE12827, and VfCXE13132) showed upregulation, while others (VfCXE17159, VfCXE18231, and VfCXE47674) were down regulated in grapevines infected with Botrytis cinerea. All transcripts showed upregulated expression against Rhizobium vitis at early and later time points except VfCXE12827, and were downregulated for up to 48 hours post inoculation (hpi) after upregulation at 1 hpi in response to R. vitis infection. All tested genes showed high and differential expression in response to pathogens, indicating that they all may play a role in defense pathways during pathogen infection in grapevines.

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References

  1. Aarts, N., Metz, M., Holub, E., Staskawicz, B. J., Daniels, M. J. and Parker, J. E. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R genemediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 95:10306-10311. https://doi.org/10.1073/pnas.95.17.10306
  2. Ade, J., DeYoung, B. J., Golstein, C. and Innes, R. W. 2007. Indirect activation of a plant nucleotide binding site-leucinerich repeat protein by a bacterial protease. Proc. Natl. Acad. Sci. U. S. A. 104:2531-2536. https://doi.org/10.1073/pnas.0608779104
  3. Ahn, S. Y., Kim, S. A., Jo, S. H. and Yun, H. K. 2014. De novo transcriptome assembly of Vitis flexuosa grapevine inoculated with Elsinoe ampelina. Plant Genetic. Resour. 12: S130-S133. https://doi.org/10.1017/S1479262114000410
  4. Baudouin, E., Charpenteau, M., Roby, D., Marco, Y., Ranjeva, R. and Ranty, B. 1997. Functional expression of a tobacco gene related to the serine hydrolase family: esterase activity towards short-chain dinitrophenyl acylesters. Eur. J. Biochem. 248:700-706. https://doi.org/10.1111/j.1432-1033.1997.t01-1-00700.x
  5. Bezier, A., Lambert, B. and Baillieul, F. 2002. Cloning of a grapevine Botrytis-responsive gene that has homology to the tobacco hypersensitivity-related hsr203J. J. Exp. Bot. 53: 2279-2280. https://doi.org/10.1093/jxb/erf101
  6. Chahinian, H. and Sarda, L. 2009. Distinction between esterases and lipases: comparative biochemical properties of sequencerelated carboxylesterases. Protein Pept. Lett. 16:1149-1161. https://doi.org/10.2174/092986609789071333
  7. Chang, S., Puryear, J. and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. 11:113-116. https://doi.org/10.1007/BF02670468
  8. Choi, Y. J., Yun, H. K., Park, K. S., Noh, J. H., Heo, Y. Y., Kim, S. H., Kim, D. W. and Lee, H. J. 2010. Transcriptional profiling of ESTs responsive to Rhizobium vitis from 'Tamnara' grapevines (Vitis sp.). J. Plant Physiol. 167:1084-1092. https://doi.org/10.1016/j.jplph.2010.02.005
  9. Chong, J., Le Henanff, G., Bertsch, C. and Walter, B. 2008. Identification, expression analysis and characterization of defense and signaling genes in Vitis vinifera. Plant Physiol. Biochem. 46:469-481. https://doi.org/10.1016/j.plaphy.2007.09.010
  10. Cunnac, S., Wilson, A., Nuwer, J., Kirik, A., Baranage, G. and Mudgett, M. B. 2007. A conserved carboxylesterase is a supressor of AvrBst-elicited resistance in Arabidopsis. Plant Cell 19:688-705. https://doi.org/10.1105/tpc.106.048710
  11. Dunigan, D. D. and Madlener, J. C. 1995. Serine/threonine protein phosphatase is required for tobacco mosaic virus-mediated programmed cell death. Virology 207:460-6. https://doi.org/10.1006/viro.1995.1105
  12. Gershater, M. C. and Edwards, R. 2007. Regulating biological activity in plants with carboxylesterase. Plant Sci. 173:579-588. https://doi.org/10.1016/j.plantsci.2007.08.008
  13. Greenberg, J. T. 1996. Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. U. S. A. 93:12094-12097. https://doi.org/10.1073/pnas.93.22.12094
  14. Guruprasad, K., Reddy, B. V. and Pandit, M. W. 1990. Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng. 4:155-161. https://doi.org/10.1093/protein/4.2.155
  15. Hammond-Kosack, K. E. and Jones, J. D. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791. https://doi.org/10.1105/tpc.8.10.1773
  16. Hammond-Kosack, K. E. and Jones, J. D. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:575-607. https://doi.org/10.1146/annurev.arplant.48.1.575
  17. Islam, M. Z., Ahn, S. Y. and Yun, H. K. 2015a. Identification of six transcripts encoding putative receptor-likeprotein kinase (RLK) and their expression profiles in Vitis flexuosa infected with pathogens. Sci. Hortic. 192:108-116. https://doi.org/10.1016/j.scienta.2015.05.025
  18. Islam, M. Z., Ahn, S. Y. and Yun, H. K. 2015b. Analysis of structure and differential expression of Pseudomonas syringae 5-like (RPS5-like) genes in pathogen-infected Vitis flexuosa. Turk. J. Biol. 39:775-789. https://doi.org/10.3906/biy-1502-38
  19. Jirage, D., Tootle, T. L., Reubert, T. L., Frost, L. N., Feyes, B. J., Parker, J. E., Ausubel, F. M. and Glazebrook, J. 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl. Acad. Sci. U. S. A. 96:13583-13588. https://doi.org/10.1073/pnas.96.23.13583
  20. Kaschani, F., Gu, C., Niessen, S., Hoover, H., Cravatt, B. F. and van der Hoorn, R. A. 2009. Diversity of serine hydrolase activities of unchallenged and Botrytis-infected Arabidopsis thaliana. Mol. Cell Proteomics 8:1082-1093. https://doi.org/10.1074/mcp.M800494-MCP200
  21. Ko, M. K., Jeon, W. B., Kim, K. S., Lee, H. H., Seo, H. H., Kim, Y. S. and Oh, B. J. 2005. A Colletotrichum gloeosporioides-induced esterase gene of nonclimacteric pepper (Capsicum annuum) fruit during ripening plays a role in resistance against fungal infection. Plant Mol. Biol. 58:529-541. https://doi.org/10.1007/s11103-005-7088-9
  22. Kong, X., Lv, W., Jiang, S., Zhang, D., Cai, G., Pan, J. and Li, D. 2013. Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genomics 14:433. https://doi.org/10.1186/1471-2164-14-433
  23. Lee, G. C., Chepyshko, H., Chen, H. H., Chu, C. C., Chou, Y. F., Akoh, C. C. and Shaw, J. F. 2010. Genes and biochemical characterization of three novel chlorophyllase isozymes from Brassica oleracea. J. Agric. Food Chem. 58:8651-8657. https://doi.org/10.1021/jf1016384
  24. Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. $H_2O_2$ from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593. https://doi.org/10.1016/0092-8674(94)90544-4
  25. Liu, J., Liu, X., Dai, L. and Wang, G. 2007. Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J. Genet. Genomics 34:765-776. https://doi.org/10.1016/S1673-8527(07)60087-3
  26. Macro, Y. J., Ragheh, F., Godiard, L. and Froissard, D. 1990. Transcriptional activation of 2 classes of genes during the hypersensitive reaction of tobacco leaves infiltrated with an incompatible isolate of the phytopathogenic bacterium Pseudomonas solanacearum. Plant Mol. Biol. 15:145-154. https://doi.org/10.1007/BF00017732
  27. Marshall, S. D., Putterill, J. J., Plummer, K. M. and Newcomb, R. D. 2003. The carboxylesterase gene family from Arabidopsis thaliana. J. Mol. Evol. 57:487-500. https://doi.org/10.1007/s00239-003-2492-8
  28. Mittler, R., Shulaev, V. and Lam, E. 1995. Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell. 7:29-42. https://doi.org/10.1105/tpc.7.1.29
  29. Nurnberger, T., Nennstiel, D., Jabs, D., Sacks, T., Hahlbrock, K. and Scheel, D. 1994. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78:449-460. https://doi.org/10.1016/0092-8674(94)90423-5
  30. Osterlund, T., Danielsson, B., Degerman, E., Contreras, J. E., Edgren, G., Davis, R. C., Schotz, M. C. and Holm, C. 1996. Domain-structure analysis of recombinant rat hormonesensitive lipase. Biochem. J. 319:411-420. https://doi.org/10.1042/bj3190411
  31. Parker, J. E., Holub, E. B., Frost, L. N., Falk, A., Gunn, N. D. and Daniel, M. J. 1996. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033-2046. https://doi.org/10.1105/tpc.8.11.2033
  32. Pontier, D., Balague, C. and Roby, D. 1998a. The hypersensitive response. A programmed cell death associated with plant resistance. C. R. Acad. Sci. III 321:721-734. https://doi.org/10.1016/S0764-4469(98)80013-9
  33. Pontier, D., Godiard, L., Marco, Y. and Roby, D. 1994. hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J. 5:507-521. https://doi.org/10.1046/j.1365-313X.1994.5040507.x
  34. Pontier, D., Tronchet, M., Rogowsky, P., Lam, E. and Roby, D. 1998b. Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol. Plant-Microbe Interact. 11: 544-554. https://doi.org/10.1094/MPMI.1998.11.6.544
  35. Reina, J. J., Guerrero, C. and Heredia, A. 2007. Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis. J. Exp. Bot. 258:2717-2731.
  36. Sharmin, S., Moosa, M. M., Islam, M. S., Kabir, I., Akter, A. and Khan, H. 2011. Identification of a novel dehydration responsive transcript from tossa jute (Corchorus olitirius L.). J. Cell Mol. Biol. 9:21-29.
  37. Tada, Y., Mori, T., Shinogi, T., Yao, N., Takahashi, S., Betsuyaku, S., Sakamoto, M., Park, P., Nakayashiki, H., Tosa, Y. and Mayama, S. 2004. Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of oat. Mol. Plant-Microbe Interact. 17:245-253. https://doi.org/10.1094/MPMI.2004.17.3.245
  38. Thomma, B. P., Eggermont, K., Penninckx, I. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. 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. U. S. A. 95:15107-15111. https://doi.org/10.1073/pnas.95.25.15107
  39. Tronchet, M., Ranty, B., Macro, Y. and Roby, D. 2001. HSR203 antisense suppression in tobacco accelerates development of hypersensitive cell death. Plant J. 27:115-127. https://doi.org/10.1046/j.1365-313x.2001.01072.x
  40. Wang, Q., Zhang, Y., Gao, M., Jiao, C. and Wang, X. 2011. Identification and expression analysis of a pathogen responsive PR-1 gene from Chinese wild Vitis quinquangularis. Afr. J. Biotechnol. 10:17062-17069.
  41. Yun, H. K., Park, K. S., Rho, J. H., Kwon, B. O. and Jeong, S. B. 2003. Development of an efficient screening system for anthracnose resistance in grapes. J. Korean Soc. Hortic. Sci. 44:809-812.
  42. Zhang, L. and Birch, R. G. 1997. The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane. Proc. Natl. Acad. Sci. U. S. A. 94:9984-9989. https://doi.org/10.1073/pnas.94.18.9984
  43. Zurbriggen, M. D., Carrillo, N. and Hajirezaei, M. R. 2010. ROS signaling in the hypersensitive response: when, where and what for? Plant Signal Behav. 5:393-396. https://doi.org/10.4161/psb.5.4.10793