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Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression

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Abstract

To analyze cellular responses to ozone (O3), we performed a large-scale analysis of the Arabidopsis transcriptome after plants were exposed to O3 for 12 h. By using cDNA macroarray technology, we identified 205 non-redundant expressed sequence tags (ESTs) that were regulated by O3. Of these, 157 were induced and 48 were suppressed by O3. A substantial proportion of these ESTs had predicted functions in cell rescue/defense processes. Using these isolated ESTs, we also undertook a comprehensive investigation of how three hormones, ethylene (ET), jasmonic acid (JA), and salicylic acid (SA), interact to regulate O3-induced genes in various genetic backgrounds of Arabidopsis, such as the ET-insensitive ein2-1, JA-resistant jar1-1, and SA-insensitive npr1-1. The expression of half of the 157 induced genes, especially cell rescue/defense genes, was controlled by ET and JA signaling, indicating that O3-induced defense gene expression at this stage was mainly regulated by ET and JA. Clustering analysis of the 157 O3-induced gene expressions revealed that multiple signal pathways act mutually antagonistically to induce the expression of these genes, and many cell rescue/defense genes induced by ET and JA signal pathways were suppressed by SA signaling, suggesting that the SA pathway acts as a strong antagonist to gene expression induced by ET and JA signaling.

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References

  • Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

    Article  Google Scholar 

  • Asamizu, E., Nakamura, Y., Sato, S. and Tabata, S. 2000. A largescale analysis of cDNA in Arabidopsis thaliana: generation of 12 028 non-redundant expressed sequence tags from normalized and size-selected cDNA libraries. DNA Res. 30: 175–180.

    Article  Google Scholar 

  • Banzet, N., Richaud, C., Deveaux, Y., Kazmier, M., Gagnon, J. and Triantaphylidès, C. 1998. Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J. 13: 519–527.

    Article  CAS  PubMed  Google Scholar 

  • Brosche, M., Schuler, M.A., Kalbina, I., Connor, L. and Strid, A. 2002. Gene regulation by low level UV-B radiation: identification by DNA array analysis. Photochem. Photobiol. Sci. 1: 656–664.

    Article  CAS  PubMed  Google Scholar 

  • Burczynski, M.E., Sridhar, G.R., Palackal, N.T. and Pennings, T.M. 2001. The reactive oxygen species-and Michael acceptorinducible human aldo-keto reductase AKRC1 reduces the α, β-unsaturated aldehyde 4-hydroxy-2-nonenal to 1,4-dihydroxy-2-nonene. J. Biol. Chem. 276: 2890–2897.

    Article  CAS  PubMed  Google Scholar 

  • Cao, H., Bowling, S.A., Gordon, A.S. and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583–1592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clayton, H., Knight, M.R., Knight, H., MacAinsh, M.R. and Hetherington, A.M. 1999. Dissection of ozone-induced calcium signature. Plant J. 17: 575–579.

    Article  CAS  PubMed  Google Scholar 

  • Conklin, P.L. and Last, R.L. 1995. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol. 109: 203–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dat, J.F., Lopez-Delgado, H., Foyer, C.H. and Scott, I.M. 1998. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedling. Plant Physiol. 116: 1351–1357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desikan, R., Mackerness, A.-H. S., Hancock, J.T. and Neill, S.J. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127: 159–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doares, S.H., Narváez-Vásquez, J., Conconi, A. and Ryan, C.A. 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108: 1741–1746.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E. and Jones, J.D.G. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound-response gene expression profiles. Plant Cell 12: 963–977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95: 14863–14868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feys, B.J. and Parker, J.E. 2000. Interplay of signaling pathways in plant disease resistance. Trends Genet. 16: 449–455.

    Article  CAS  PubMed  Google Scholar 

  • Glick, R.E., Schlagnhaufer, C.D., Arteca, R.N. and Pell, E.J. 1995. Ozone-induced ethylene emission accelerates the loss of ribulose-1,5-bisphosphatecarboxylase/oxygenase and nuclearencoded mRNAs in senescing potato leaves. Plant Physiol. 109: 891–898.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Godon, C., Lagniel, G., Lee, J., Buhler, J-M., Kieffer, S., Perrot, M., Boucherie, H., Toledano, M.B. and Labarre, J. 1998. The H2O2 stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 273: 22480–22489.

    Article  CAS  PubMed  Google Scholar 

  • Grant, J.J., Yun, B.-W. and Loake, G.J. 2000. Oxidative burst and cognate redox signaling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J. 24: 87–95.

    Article  Google Scholar 

  • Gupta, V., Willits, M.G. and Glazebrook, J. 2000. Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol. Plant-Microbe Interact. 13: 503–511.

    Article  CAS  PubMed  Google Scholar 

  • Guzman, P. and Ecker, J.R. 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513–523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoigné, J. and Bader, H. 1975. Ozonation of water: role of hydroxyl radicals as oxidizing intermediates. Science 190: 782–784.

    Article  Google Scholar 

  • Hubatsch, I., Ridderström M. and Mannervik, B. 1998. Human glutathione transferase A4-4: an alfa class enzyme with high catalytic efficiency in the conjugation of 4-hydroxynonenal and other genotoxic products of lipid peroxidation. Biochem J. 330: 175–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kangasjärvi, J., Talvinen, J., Utriainen, M. and Karjalainen, R. 1994. Plant defense systems induced by ozone. Plant Cell Environ. 17: 783–794.

    Article  Google Scholar 

  • Kanofsky, J.R. and Sima, P. 1991. Singlet oxygen production from the reactions of ozone with biological molecules. J. Biol. Chem. 266: 9039–9042.

    CAS  PubMed  Google Scholar 

  • Kliebenstein, D.J., Monde, R.-A. and Last, S.M. 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118: 637–650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura, M., Yamamoto, Y.Y., Seki, M., Sakurai, T., Sato, M., Abe, T., Yoshida, S., Manabe, K., Shinozaki K. and Matsui M. 2003. Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem. Photobiol. 77: 226–233.

    CAS  PubMed  Google Scholar 

  • Krupa, S.V. and Manning, W.J. 1988. Atmospheric ozone: formation and effect on vegetation. Environ. Poll. 50: 101–137.

    Article  CAS  Google Scholar 

  • Kubo, A., Saji, H., Tanaka, K. and Kondo, N. 1995. Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Mol. Biol. 29: 479–489.

    Article  CAS  PubMed  Google Scholar 

  • Lawton, K., Potter, S.C., Friedrich, L., Vernooij, B., Uknes, S. and Ryals, J. 1994. Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6: 581–588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593.

    Article  CAS  PubMed  Google Scholar 

  • Maccarrone, M., Veldink, G.A. and Vliegenthart, J.F.G. 1992. Thermal injury and ozone stress affect soybean lipoxygenase expression. FEBS Lett. 309: 225–230.

    Article  CAS  PubMed  Google Scholar 

  • Mahalingam, R., Gomez-Buitrago, A., Eckardt, N., Shah, N., Guevara-Garcia, A., Day, P., Raina, R. and Fedoroff, N.V. 2003. Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol. 4: R20.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L. and Dietrich, R.A. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet. 26: 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Mano, J., Torii, Y., Hayashi, S., Takimoto, K., Matsui, K., Nakaura, K., Inzé, D., Babiychuk, E., Kushnir, S. and Asada, K. 2002. The NADPH:quinone oxidoreductase P1-ζ –crystallin in Arabidopsis catalyzes the α, β-hydrogenation of 2-alkenals: detoxification of the lipid peroxide-derived reactive aldehydes. Plant Cell Physiol. 43: 1445–1455.

    Article  CAS  PubMed  Google Scholar 

  • Matsuyama, T., Tamaoki, M., Nakajima, N., Aono, M., Kubo, A., Moriya, S., Ichihara, T., Suzuki, O. and Saji, H. 2002. cDNA microarray assessment for ozone-stressed Arabidopsis thaliana. Environ. Poll. 117: 191–194.

    Article  CAS  Google Scholar 

  • Mehlhorn, H., Tabner, B. and Wellburn A.R. 1990. Electron spin resonance evidence for the formation of free radicals in plants exposed to ozone. Physiol. Plant. 79: 377–383.

    Article  CAS  Google Scholar 

  • Miller, J.D., Arteca, R.N. and Pell, E.J. 1999. Senescenceassociated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol. 120: 1015–1023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman, T., De Bruijn, F.J., Green, P., Keegstra, K., Kende, H., Mcintosh, L., Ohlrogge, J., Raikhel, N., Somerville, S., Thomashow, M., Retzel, E. and Somerville, C. 1994. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol. 106: 1241–1255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N. and Ohashi, Y. 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39: 500–507.

    Article  CAS  Google Scholar 

  • Overmyer, K., Tuominen, H., Kettunen, R,. Betz, C., Langebartels, C., Sandermann, H. and Kangasjärvi, J. 2000. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxidedependent cell death. Plant Cell 12: 1849–1862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pell, E.J., Schlagnhaufer, C.D. and Arteca, R.N. 1997. Ozoneinduced oxidative stress: mechanisms of action and reaction. Physiol. Plant. 100: 264–273.

    Article  CAS  Google Scholar 

  • Pieterse, C.J.M. and van Loon, L.C. 1999. Salicylic acidindependent plant defense pathways. Trends Plant Sci. 4: 52–58.

    Article  PubMed  Google Scholar 

  • Rao, M.V. and Davis, K.R. 1999. Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J. 17: 603–614.

    Article  CAS  PubMed  Google Scholar 

  • Rao, M.V. and Davis, K.R. 2001. The physiology of ozone induced cell death. Planta 213: 682–690.

    Article  CAS  PubMed  Google Scholar 

  • Rao, M.V., Lee, H-I., Creelman, R.A., Raskin, I., Mullet, J.E. and Davis, K.R. 2000. Jasmonic acid signaling modulates ozoneinduced hypersensitive cell death. Plant Cell 12: 1633–1646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao, M.V., Lee, H. and Davis, K.R. 2002. Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J. 32: 447–456.

    Article  CAS  PubMed  Google Scholar 

  • Reymond, P. and Farmer, E.E. 1998. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1: 404–411.

    Article  CAS  PubMed  Google Scholar 

  • Reymond, P., Weber, H., Damond, M. and Farmer, E.E. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707–719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossel, J.B., Wilson, I.W. and Pogson, B.J. 2002. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130: 1109–1120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandermann, H., Ernst, D., Heller, W. and Langebertles, C. 1998. Ozone: an abiotic elicitor of plant defense reaction. Trends Plant Sci. 3: 47–50.

    Article  Google Scholar 

  • Sasaki, Y., Asamizu, E., Shibata, D., Nakamura, Y., Kaneko, T., Awai, K., Amagai, M., Kuwata, C., Tsugane, T., Masuda, T., Shimada, H., Takamiya, X., Ohta, H. and Tabata, S. 2001. Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res. 8: 153–161.

    Article  CAS  PubMed  Google Scholar 

  • Schaffer, R., Landgraf, J,. Accerbi, M., Simon, V., Larson, M. and Wisman, E. 2001. Microarray analysis of diurnal and circadianregulated genes in Arabidopsis. Plant Cell 13: 113–123.

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y. and Shinozaki, K. 2002. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31: 279–292.

    Article  CAS  PubMed  Google Scholar 

  • Sellin, S., Holmquist, B., Mannervik, B. and Vallee, B.L. 1991. Oxidation and reduction of 4-hydroxyalkenals atalyzed by isozymes of human alcohol dehydrogenase. Biochemistry 30: 2514–2518.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, Y.K. and Davis, K.R. 1997. The effect of ozone on antioxidant response in plants. Free Radical Biol. Med. 23: 480–488.

    Article  CAS  Google Scholar 

  • Sharma, Y.K., León, J., Raskin, I. and Davis, K.R. 1996. Ozoneinduced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc. Natl. Acad. Sci. USA 93: 5099–5104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shena, M., Shalon, D., Davis, R.W. and Brown, P.O. 1995. Quantitative monitoring of gene expression patterns with a complimentary DNA microarray. Science 270: 467–470.

    Article  Google Scholar 

  • Srivastava, S., Chandra, A., Bhatnagar, A., Srivastava, S.K. and Ansari, N.H. 1995. Lipid peroxidation product, 4-hydroxynonenal and its conjugate with GSH are excellent substrates of bovine lens aldose reductase. Biochem. Biophys. Res. Commun. 217: 741–746.

    Article  CAS  PubMed  Google Scholar 

  • Staswick, P.E., Su, W. and Howell, S.H. 1992. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. USA 89: 6837–6840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamaoki, M., Matsuyama, T., Kanna, M., Nakajima, N., Kubo, A., Aono, M. and Saji H. 2003. Differential O3 sensitivity among Arabidopsis accessions and its relevance to ethylene synthesis. Planta 216: 552–560.

    CAS  PubMed  Google Scholar 

  • Thomma, B.P.H.J., Penninckx, I.A.M.A., Broekart, W.F. and Cammue, B.P.A. 2001. The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 13: 63–68.

    Article  CAS  PubMed  Google Scholar 

  • Treshow, M. and Anderson, F.K. 1989. Plant Stress from Air Pollution. John Wiley, New York.

    Google Scholar 

  • Vahala, J., Ruonala, R., Keinanen, M., Tuominen, H. and Kangasjärvi, J. 2003. Ethylene insensitivity modulates ozone-induced cell death in birch. Plant Physiol. 132: 185–195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, P., Ma, L., Hou, X., Wang, M., Wu, Y., Liu, F. and Deng, X.W. 2003. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 132: 1260–1271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng, M., Åslund, F. and Storz, G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718–1721.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Biodiversity Conservation Research Project, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki, 305-8506, Japan

    Masanori Tamaoki & Nobuyoshi Nakajima

  2. Environmental Biology Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki, 305-8506, Japan

    Akihiro Kubo, Mitsuko Aono & Hikaru Saji

  3. Biotechnology Division, Toyota Central R & D Labs., Inc., Nagakute, Aichi, 480-1192, Japan

    Takashi Matsuyama

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  1. Masanori Tamaoki
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  2. Nobuyoshi Nakajima
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  3. Akihiro Kubo
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  4. Mitsuko Aono
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  5. Takashi Matsuyama
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  6. Hikaru Saji
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Correspondence to Masanori Tamaoki.

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Tamaoki, M., Nakajima, N., Kubo, A. et al. Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol Biol 53, 443–456 (2003). https://doi.org/10.1023/B:PLAN.0000019064.55734.52

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