Skip to main content
SpringerLink
Log in

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

  • Chapter
Book cover Salicylic Acid: A Plant Hormone

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bowles, D., Isayenkova, J., Lim, E. K., and Poppenberger, B., 2005. Glycosyltransferases: managers of small molecules. Curr. Opin. Plant Biol., 8: 254-263.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Dharmasiri, N., Dharmasiri, S., and Estelle, M., 2005. The F-box protein TIR1 is an auxin receptor. Nature, 435: 441-445.

    Article  PubMed  CAS  Google Scholar 

  • Dixon, R. A., and Paiva, N. L., 1995. Stress-induced phenylpropanoid metabolism. Plant Cell, 7: 1085-1097.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Eulgem, T., 2005. Regulation of the Arabidopsis defense transcriptome. Tren. Plant Sci., 10: 71-78.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Frova, C., 2003. The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol. Plant., 119: 469-479.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gozzo, F., 2003. Systemic acquired resistance in crop protection: From nature to a chemical approach. J. Agric. Food Chem., 51: 4487-4503.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kepinski, S. and Leyser, O., 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature, 435: 446-451.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Leon, J., Rojo, E., and Sanchez-Serrano, J. J., 2001. Wound signalling in plants. J. Exp. Bot., 52: 1-9.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Metraux, J. P., 2002. Recent breakthroughs in the study of salicylic acid biosynthesis. Tren. Plant Sci., 7: 332-334.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Tren. Plant Sci. 7: 405-410.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pedley, K. F., and Martin, G. B., 2005. Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol., 8: 541-547.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Scholthof, K. B. G., 2004. Tobacco mosaic virus: A model system for plant biology. Annu. Rev. Phytopath., 42: 13-34.

    Article  CAS  Google Scholar 

  • Seskar, M., Shulaev, V., and Raskin, I., 1998. Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol., 116: 387-392.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Smigocki, A. C., 1991. Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene. Plant Mol. Biol., 16: 105-115.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Thomann, A., Dieterle, M., and Genschik, P., 2005. Plant CULLIN-based E3s: Phytohormones come first. FEBS Lett., 579: 3239-3245.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Wiermer, M., Feys, B. J., and Parker, J. E., 2005. Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol., 8: 383-389.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Yazaki, K., 2005. Transporters of secondary metabolites. Curr. Opin. Plant Biol., 8: 301-307.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, S. Q., and Klessig, D. F., 1997. Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell, 9: 809-824.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Japan

    I. Galis & K. Matsuoka

Authors
  1. I. Galis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Matsuoka
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    S. Hayat

  2. Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    A. Ahmad

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer

About this chapter

Cite this chapter

Galis, I., Matsuoka, K. (2007). Transcriptomic Analysis of Salicylic Acid-Responsive Genes in Tobacco By-2 Cells. In: Hayat, S., Ahmad, A. (eds) Salicylic Acid: A Plant Hormone. Springer, Dordrecht. https://doi.org/10.1007/1-4020-5184-0_13

Download citation

Publish with us

Policies and ethics

Search

Navigation