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Transcriptomic Analysis of Salicylic Acid-Responsive Genes in Tobacco By-2 Cells

  • I. Galis
  • K. Matsuoka
Chapter

Abstract

Tobacco has played historically important role in the discovery and functional analysis of salicylic acid (SA) as a plant hormone. Using this model, it was demonstrated for the first time that tobacco mosaic virus (TMV) infection results in the accumulation of SA in infected tissues that is to activate local and systemic expression of pathogenesis-related proteins in the cells. Furthermore, SA has been shown to function as a major factor in the development of systemic acquired resistance (SAR) in plants. To promote the importance of tobacco as a model plant, we generated and sequenced cDNA libraries from tobacco BY-2 cells, depositing about 20,000 EST sequence information in the public databases. Selected cDNA clones were then used to prepare the first large-scale 16K microarray of tobacco. In this chapter, we describe our results of a large scale gene expression analysis, using the tobacco BY-2 cells, treated with a 40 μM salicylic acid. In total, 376 genes (corresponding to individual ESTs) were at least 2-fold upregulated by SA, relative to their expression levels in control cells. Amid, a large number of genes overlapped with known defense-related genes in plants, whilst the others represented novel targets of SA in plants. The kinetic analysis of the SA-responsive genes, together with functional analysis of these genes in the plant defense, is presented in this chapter.

Key words

Global gene expression microarray analysis plant defense salicylic acid tobacco BY-2 cells 

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References

  1. Bieza, K., and Lois, R., 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol., 126: 1105-1115.PubMedCrossRefGoogle Scholar
  2. Bowles, D., Isayenkova, J., Lim, E. K., and Poppenberger, B., 2005. Glycosyltransferases: managers of small molecules. Curr. Opin. Plant Biol., 8: 254-263.PubMedCrossRefGoogle Scholar
  3. Buchanan, C. D., Lim, S. Y., Salzman, R. A., Kagiampakis, L., Morishige, D. T., Weers, B. D., Klein, R. R., Pratt, L. H., Cordonnier-Pratt, M. M., Klein, P. E., and Mullet, J. E., 2005. Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol. Biol., 58: 699-720.PubMedCrossRefGoogle Scholar
  4. De Gara, L., de Pinto, M. C., and Tommasi, F., 2003. The antioxidant systems vis-a-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol. Biochem., 41: 863-870.CrossRefGoogle Scholar
  5. De Paepe, A., Vuylsteke, M., Van Hummelen, P., Zabeau, M., and Van Der Straeten, D., 2004. Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J., 39: 537-559.PubMedCrossRefGoogle Scholar
  6. De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., 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. J., 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Micro. Inter., 18: 923-937.CrossRefGoogle Scholar
  7. Dharmasiri, N., Dharmasiri, S., and Estelle, M., 2005. The F-box protein TIR1 is an auxin receptor. Nature, 435: 441-445.PubMedCrossRefGoogle Scholar
  8. Dixon, R. A., and Paiva, N. L., 1995. Stress-induced phenylpropanoid metabolism. Plant Cell, 7: 1085-1097.PubMedCrossRefGoogle Scholar
  9. Dong, J. X., Chen, C. H., and Chen, Z. X., 2003. Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol., 51: 21-37.PubMedCrossRefGoogle Scholar
  10. Enyedi, A. J., Yalpani, N., Silverman, P., and Raskin, I., 1992. Localization, conjugation, and function of salicylic-acid in tobacco during the hypersensitive reaction to tobacco mosaic-virus. Proc. Natl. Acad. Sci. USA., 89: 2480-2484.PubMedCrossRefGoogle Scholar
  11. Eulgem, T., 2005. Regulation of the Arabidopsis defense transcriptome. Tren. Plant Sci., 10: 71-78.CrossRefGoogle Scholar
  12. Eulgem, T., Rushton, P. J., Robatzek, S., and Somssich, I. E., 2000. The WRKY superfamily of plant transcription factors. Tren. Plant Sci., 5: 199-206.CrossRefGoogle Scholar
  13. Foyer, C. H., and Noctor, G., 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ., 28: 1056-1071.CrossRefGoogle Scholar
  14. Fraissinet-Tachet, L., Baltz, R., Chong, J., Kauffmann, S., Fritig, B., and Saindrenan, P., 1998. Two tobacco genes induced by infection, elicitor and salicylic acid encode glucosyltransferases acting on phenylpropanoids and benzoic acid derivatives, including salicylic acid. FEBS Lett., 437: 319-323.PubMedCrossRefGoogle Scholar
  15. Frova, C., 2003. The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol. Plant., 119: 469-479.CrossRefGoogle Scholar
  16. Fujita, T., Kouchi, H., Ichikawa, T., and Syono, K., 1994. Cloning of cDNAs for genes that are specifically or preferentially expressed during the development of tobacco genetic tumors. Plant J., 5: 645-654.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. Galis, I., Šimek, P., Narisawa, T., Sasaki, M., Horiguchi, T., Fukuda, F., and Matsuoka, K., 2006. A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenypropanoid-conjugate biosynthesis in tobacco. Plant J. (In Press). Google Scholar
  19. Galis, I., Smith, J. L., and Jameson, P. E., 2004. Salicylic acid-, but not cytokinin-induced, resistance to WClMV is associated with increased expression of SA-dependent resistance genes in Phaseolus vulgaris. J. Plant Physiol., 161: 459-466.PubMedCrossRefGoogle Scholar
  20. Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y., and Yoshida, S., 2004. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol., 134: 1555-1573.PubMedCrossRefGoogle Scholar
  21. Goda, H., Shimada, Y., Asami, T., Fujioka, S., and Yoshida, S., 2002. Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol., 130: 1319-1334.PubMedCrossRefGoogle Scholar
  22. Goossens, A., Hakkinen, S. T., Laakso, I., Seppanen-Laakso, T., Biondi, S., De Sutter, V., Lammertyn, F., Nuutila, A. M., Soderlund, H., Zabeau, M., Inze, D., and Oksman-Caldentey, K. M., 2003. A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc. Natl. Acad. Sci. USA., 100: 8595-8600.PubMedCrossRefGoogle Scholar
  23. Goy, P. A., Signer, H., Reist, R., Aichholz, R., Blum, W., Schmidt, E., and Kessmann, H., 1993. Accumulation of scopoletin is associated with the high disease resistance of the hybrid Nicotiana-glutinosa X Nicotiana-debneyi. Planta, 191: 200-206.CrossRefGoogle Scholar
  24. Gozzo, F., 2003. Systemic acquired resistance in crop protection: From nature to a chemical approach. J. Agric. Food Chem., 51: 4487-4503.PubMedCrossRefGoogle Scholar
  25. Grace, S. C., and Logan, B. A., 2000. Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philos. Trans. R. Soc. Lond. Ser. B-Biol. Sci., 355: 1499-1510.CrossRefGoogle Scholar
  26. Kepinski, S. and Leyser, O., 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature, 435: 446-451.PubMedCrossRefGoogle Scholar
  27. Kim, H. S., and Delaney, T. P., 2002. Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell, 14: 1469-1482.PubMedCrossRefGoogle Scholar
  28. Kubigsteltig, II., and Weiler, E. W., 2003. Arabidopsis mutants affected in the transcriptional control of allene oxide synthase, the enzyme catalyzing the entrance step in octadecanoid biosynthesis. Planta, 217: 748-757.PubMedCrossRefGoogle Scholar
  29. Leon, J., Rojo, E., and Sanchez-Serrano, J. J., 2001. Wound signalling in plants. J. Exp. Bot., 52: 1-9.PubMedCrossRefGoogle Scholar
  30. Ludwikow, A., Gallois, P., and Sadowski, J., 2004. Ozone-induced oxidative stress response in Arabidopsis: Transcription profiling by microarray approach. Cell. Mol. Biol. Lett., 9: 829-842.PubMedGoogle Scholar
  31. Malamy, J., Carr, J. P., Klessig, D. F., and Raskin, I., 1990. Salicylic-acid - a likely endogenous signal in the resistance response of tobacco to viral-infection. Science, 250: 1002-1004.CrossRefGoogle Scholar
  32. Matsuoka, K., Demura, T., Galis, I., Horiguchi, T., Sasaki, M., Tashiro, G., and Fukuda, H., 2004. A comprehensive gene expression analysis toward the understanding of growth and differentiation of tobacco BY-2 cells. Plant Cell Physiol., 45: 1280-1289.PubMedCrossRefGoogle Scholar
  33. Metraux, J. P., 2002. Recent breakthroughs in the study of salicylic acid biosynthesis. Tren. Plant Sci., 7: 332-334.CrossRefGoogle Scholar
  34. Metraux, J. P., Signer, H., Ryals, J., Ward, E., Wyssbenz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., and Inverardi, B., 1990. Increase in salicylic-acid at the onset of systemic acquired-resistance in cucumber. Science, 250: 1004-1006.CrossRefGoogle Scholar
  35. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Tren. Plant Sci. 7: 405-410.CrossRefGoogle Scholar
  36. Nagata, T., Hasezawa, S., and Inze, D. 2004. Tobacco BY-2 cells: Biotechnology in Agriculture and Forestry, vol. 53, Springer-Verlag, Heidelberg, pp. 7-65.Google Scholar
  37. Ogawa, M., Hanada, A., Yamauchi, Y., Kuwalhara, A., Kamiya, Y., and Yamaguchi, S., 2003. Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell, 15: 1591-1604.PubMedCrossRefGoogle Scholar
  38. Parani, M., Rudrabhatla, S., Myers, R., Weirich, H., Smith, B., Leaman, D. W., and Goldman, S. L., 2004. Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotech. J., 2: 359-366.CrossRefGoogle Scholar
  39. Pedley, K. F., and Martin, G. B., 2005. Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol., 8: 541-547.PubMedCrossRefGoogle Scholar
  40. Pieterse, C. M., and Van Loon, L., 2004. NPR1: the spider in the web of induced resistance signaling pathways. Curr. Opin. Plant Biol., 7: 456-464.PubMedCrossRefGoogle Scholar
  41. Rashotte, A. M., Carson, S. D. B., To, J. P. C., and Kieber, J. J., 2003. Expression profiling of cytokinin action in Arabidopsis. Plant Physiol., 132: 1998-2011.PubMedCrossRefGoogle Scholar
  42. Ryan, K. G., Swinny, E. E., Winefield, C., and Markham, K. R., 2001. Flavonoids and UV photoprotection in Arabidopsis mutants. Z.Naturforsch., 56: 745-754.Google Scholar
  43. Salzman, R. A., Brady, J. A., Finlayson, S. A., Buchanan, C. D., Summer, E. J., Sun, F., Klein, P. E., Klein, R. R., Pratt, L. H., Cordonnier-Pratt, M. M., and Mullet, J. E., 2005. Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol., 138: 352-368.PubMedCrossRefGoogle Scholar
  44. Sappl, P. G., Onate-Sanchez, L., Singh, K. B., and Millar, A. H., 2004. Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Mol. Biol., 54: 205-219.PubMedCrossRefGoogle Scholar
  45. Schenk, P. M., Kazan, K., Wilson, I., Anderson, J. P., Richmond, T., Somerville, S. C., and Manners, J. M., 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA., 97: 11655-11660.PubMedCrossRefGoogle Scholar
  46. Scholthof, K. B. G., 2004. Tobacco mosaic virus: A model system for plant biology. Annu. Rev. Phytopath., 42: 13-34.CrossRefGoogle Scholar
  47. Seskar, M., Shulaev, V., and Raskin, I., 1998. Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol., 116: 387-392.CrossRefGoogle Scholar
  48. Singh, K. B., Foley, R. C., and Onate-Sanchez, L., 2002. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol., 5: 430-436.PubMedCrossRefGoogle Scholar
  49. Smart, C. M., Scofield, S. R., Bevan, M. W., and Dyer, T. A., 1991. Delayed leaf senescence in tobacco plants transformed with tmr, a gene for cytokinin production in Agrobacterium. Plant Cell, 3: 647-656.PubMedCrossRefGoogle Scholar
  50. Smigocki, A. C., 1991. Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene. Plant Mol. Biol., 16: 105-115.PubMedCrossRefGoogle Scholar
  51. Stein, M., and Somerville, S. C., 2002. MLO, a novel modulator of plant defenses and cell death, binds calmodulin. Tren. Plant Sci., 7: 379-380.CrossRefGoogle Scholar
  52. Suzuki, H., Reddy, M. S. S., Naoumkina, M., Aziz, N., May, G. D., Huhman, D. V., Sumner, L. W., Blount, J. W., Mendes, P., and Dixon, R. A., 2005. Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta, 220: 696-707.PubMedCrossRefGoogle Scholar
  53. Swiatek, A., Lenjou, M., Van Bockstaele, D., Inze, D., and Van Onckelen, H., 2002. Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol., 128: 201-211.PubMedCrossRefGoogle Scholar
  54. Takahashi, S., Seki, M., Ishida, J., Satou, M., Sakurai, T., Narusaka, M., Kamiya, A., Nakajima, M., Enju, A., Akiyama, K., Yamaguchi-Shinozaki, K., and Shinozaki, K., 2004. Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol. Biol., 56: 29-55.PubMedCrossRefGoogle Scholar
  55. Tamaoki, M., Nakajima, N., Kubo, A., Aono, M., Matsuyama, T., and Saji, H., 2003. Transcriptome analysis of O-3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol. Biol., 53: 443-456.PubMedCrossRefGoogle Scholar
  56. Thatcher, L. F., Anderson, J. P., and Singh, K. B., 2005. Plant defence responses: what have we learnt from Arabidopsis? Funct. Plant Biol., 32: 1-19.CrossRefGoogle Scholar
  57. Thomann, A., Dieterle, M., and Genschik, P., 2005. Plant CULLIN-based E3s: Phytohormones come first. FEBS Lett., 579: 3239-3245.PubMedCrossRefGoogle Scholar
  58. Uknes, S., Dincher, S., Friedrich, L., Negrotto, D., Williams, S., Thompsontaylor, H., Potter, S., Ward, E., and Ryals, J., 1993. Regulation of pathogenesis-related protein-1a gene-expression in tobacco. Plant Cell, 5: 159-169.PubMedCrossRefGoogle Scholar
  59. Van Zhong, G., and Burns, J. K., 2003. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol. Biol., 53: 117-131.PubMedCrossRefGoogle Scholar
  60. Veronese, P., Ruiz, M. T., Coca, M. A., Hernandez-Lopez, A., Lee, H., Ibeas, J. I., Damsz, B., Pardo, J. M., Hasegawa, P. M., Bressan, R. A., and Narasimhan, M. L., 2003. In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiol., 131: 1580-1590.PubMedCrossRefGoogle Scholar
  61. Wiermer, M., Feys, B. J., and Parker, J. E., 2005. Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol., 8: 383-389.PubMedCrossRefGoogle Scholar
  62. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D. A., and Raskin, I., 1991. Salicylic-acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell, 3: 809-818.PubMedCrossRefGoogle Scholar
  63. Yang, K. Y., Liu, Y. D., and Zhang, S. Q., 2001. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. PNAS., 98: 741-746.PubMedCrossRefGoogle Scholar
  64. Yang, Y. N., Qi, M., and Mei, C. S., 2004. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J., 40: 909-919.PubMedCrossRefGoogle Scholar
  65. Yazaki, J., Shimatani, Z., Hashimoto, A., Nagata, Y., Fujii, F., Kojima, K., Suzuki, K., Taya, T., Tonouchi, M., Nelson, C., Nakagawa, A., Otomo, Y., Murakami, K., Matsubara, K., Kawai, J., Carninci, P., Hayashizaki, Y., and Kikuchi, S., 2004. Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis. Physiol. Genom., 17: 87-100.CrossRefGoogle Scholar
  66. Yazaki, K., 2005. Transporters of secondary metabolites. Curr. Opin. Plant Biol., 8: 301-307.PubMedCrossRefGoogle Scholar
  67. Zhang, S. Q., and Klessig, D. F., 1997. Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell, 9: 809-824.PubMedCrossRefGoogle Scholar
  68. Zhang, S. Q., and Liu, Y. D., 2001. Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell, 13: 1877-1889.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • I. Galis
    • 1
  • K. Matsuoka
    • 1
  1. 1.RIKEN Plant Science CenterTsurumi-ku, YokohamaJapan

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