Skip to main content
SpringerLink
Log in

Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: Analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

From Arabidopsis full-length cDNA libraries, we collected ca. 7000 (7K) independent full-length cDNAs to prepare a cDNA microarray. The 7K cDNA collection contains 49 cytochrome P450 genes. In this study, expression patterns of these cytochrome P450 genes were analyzed by a full-length cDNA microarray under various treatments, such as hormones (salicylic acid, jasmonic acid, ethylene, abscisic acid), pathogen-inoculation (Alternaria brassicicola, Alternaria alternata), paraquat, rose bengal, UV stress (UV-C), heavy metal stress (CuSO_4), mechanical wounding, drought, high salinity and low temperature. Expression of 29 cytochrome P450 genes among them was induced by various treatments. Inoculation with A. brassicicola and A. alternata as biotic stresses increased transcript levels of 12 and 5 genes in Arabidopsis plants, respectively. In addition, some of the genes were also expressed by abiotic stresses. This suggests crosstalk between abiotic and biotic stresses. The promoter sequences and cis-acting elements of each gene were studied on the basis of full-length cDNA sequences. Most cytochrome P450 genes induced by both abiotic and biotic stresses contained the recognition sites of MYB and MYC, ACGT-core sequence, TGA-box and W-box for WRKY transcription factors in their promoters. These cis-acting elements are known to participate in the regulation of plant defense. The response of each gene to multiple stresses is strictly regulated.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D. and Shinozaki, K., 1997. Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acidregulated gene expression. Plant Cell 9: 1859–1868.

    PubMed  Google Scholar 

  • Babu, T. S., Akhtar, T. A., Lampi, M. A., Tripuranthakam, S., Dixon, D. G. and Greenberg, B. M. 2003. Similar stress responses are elicited by copper and ultraviolet radiation in the aquatic plant Lemna gibba: implication of reactive oxygen species as common signals. Plant Cell Physiol. 44:1320–1329.

    PubMed  Google Scholar 

  • Bak, S., Tax, F. E., Feldman, K. A., Galbraith, D. W. and Feyereisen, R. 2001. CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13: 101–111.

    PubMed  Google Scholar 

  • Batard, Y., LeRet, M., Schalk, M., Robineau, T., Durst, F. and Werck-Reichhart, D. 1998. Molecular cloning and functional expression in yeast of CYP76B1, a xenobiotic-inducible 7-ethoxycoumarin O-de-ethylase from Helianthus tuberosus. Plant J. 14: 111–120.

    PubMed  Google Scholar 

  • Block, A., Dangl, J. L., Hahlbrock, K. and Schulze-Lefert, P. 1990. Functional borders, genetic fine structure, and distance requirements of cis elements mediating light responsiveness of the parsley chalcone synthase promoter. Proc. Natl. Acad. Sci. USA 87: 5387–5391.

    PubMed  Google Scholar 

  • Bolwell, G. P., Bozak, K. and Zimmerlin, A. 1994. Plant cytochrome P450. Phytochemistry 37: 1491–1506.

    PubMed  Google Scholar 

  • Bowler, C., Van Montagu, M. and Inze, D. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 83–116.

    Google Scholar 

  • Busk, P. K. and Pages, M. 1998. Regulation of abscisic acidinduced transcription. Plant Mol. Biol. 37: 425–435.

    PubMed  Google Scholar 

  • Chapple, C. 1998. Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 311–343.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Donald, R. G. K. and Cashmore, A. R. 1990. Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter. EMBO J. 9: 1717–1726.

    PubMed  Google Scholar 

  • Donaldson, R. P. and Luster, D. G. 1991. Multiple forms of plant cytochromes P450. Plant Physiol. 96: 669–674.

    Google Scholar 

  • Eisen, M. B. and Brown, P. O. 1999. DNA arrays for analysis of gene expression. Methods Enzymol. 303: 179–205.

    PubMed  Google Scholar 

  • Eulgem, T., Rushton, P. J., Robatzek, S. and Somssich, I. E. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5: 199–206.

    PubMed  Google Scholar 

  • Eyal, Y., Meller, Y., Lev-Yadun, S. and Fluhr, R. 1993. A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. Plant J. 4: 225–234.

    PubMed  Google Scholar 

  • Fahrendorf, T. and Dixon, R. A. 1993. Stress responses in alfalfa (Medicago sativa L. ). XVIII: molecular cloning and expression of the elicitor-inducible cinnamic acid 4-hydroxylase cytochrome P450. Arch. Biochem. Biophys. 305: 509–515.

    PubMed  Google Scholar 

  • Frank, M. R., Deyneka, J. M. and Schuler, M. A. 1996. Cloning of wound-induced cytochrome P450 monooxygenases expressed in pea. Plant Physiol. 110: 1035–1046.

    PubMed  Google Scholar 

  • Garreton, V., Carpinelli, J., Jordana, X. and Holuigue, L. 2002. The as-1 promoter element is an oxidative stressresponsive element and salicylic acid activates it via oxidative species. Plant Physiol. 130: 1516–1526.

    PubMed  Google Scholar 

  • Godiard, L, Sauviac, L., Dalbin, N., Liaubet, L., Callard, D., Czernic, P and Marco, Y. 1998. CYP76C2, an Arabidopsis thaliana cytochrome P450 gene expressed during hypersensitive and developmental cell death. FEBS Lett. 438: 245–249.

    PubMed  Google Scholar 

  • Green., and Fluhr., 1995. UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203–212.

    PubMed  Google Scholar 

  • Guan., and Scandalios, J. G. 1993. Characterization of the catalase antioxidant defense gene Cat1 of maize and its developmentally regulated expression in transgenic tobacco. Plant J. 3: 527–536.

    PubMed  Google Scholar 

  • Guan, L. M., Zhao, J. and Scandalios, J. G. 2000. Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J. 22: 87–95.

    PubMed  Google Scholar 

  • Guiltinan, M. J., Marcotte, W. R. and Quatrano, R. S. 1990. A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 267–271.

    PubMed  Google Scholar 

  • Halkier, B. A. and Du, L. 1997. The biosynthesis of glucosinolates. Trends Plant Sci. 11: 425–430.

    Google Scholar 

  • Hansen, C. H., Du, L., Naur, P., Olsen, C. E., Axelsen, K. B., Hick, A. J, Pickett, J. A and Halkier, B. A. 2001. CYP83B1 is the oxime-metabolizing enzyme in the glucosinolate pathway in Arabidopsis. J. Biol. Chem. 276: 24790–24796.

    PubMed  Google Scholar 

  • Hattori, T., Totsuka, M., Hobo, T., Kagaya, Y. and Yamamoto-Toyoda, A. 2002. Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol. 43: 136–40.

    PubMed  Google Scholar 

  • Hatzios, K. K. 1991. Biotransformations of herbicides in higher plants. In: R. Grover and A. J. Cessna (s. ) Environmental Chemistry of Herbicides, vol. 2, CRC Press, Boca Raton, FL., pp. 1451–1185.

    Google Scholar 

  • Hernandes, J. A., Olmos, E., Corpas, F. J., Sevilla, F. and del Rio, L. A. 1995. Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci. 105: 151–167.

    Google Scholar 

  • Hull, A. K., Vij, R. and Celenza, J. L. 2000. Arabidopsis cytochrome P450s that catalyze the first step of tryptophandependent indole-3-acetic acid biosynthesis. Proc. Natl. Acad. Sci. USA 97: 2379–2384.

    PubMed  Google Scholar 

  • Iwasaki, T., Kiyosue, T., Yamaguchi-Shinozaki, K. and Shinozaki, K. 1997. The dehydration-inducible RD17 (Cor47) gene and its promoter region in Arabidopsis thaliana (accession no. AB004872) (PGR97–156). Plant Physiol. 115: 1287.

    PubMed  Google Scholar 

  • Kutchan, T. M. 1995. Alkaloid biosynthesis–The basis for metabolic engineering of medicinal plants. Plant Cell 7: 1059–1070.

    PubMed  Google Scholar 

  • Lam, E., Benfey, P. N., Gilmartin, P. M., Fang, R.-X. and Chua, N.-H. 1989. Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc. Natl. Acad. Sci. USA 86: 7890–7894.

    PubMed  Google Scholar 

  • Leon, J., Yalpani, N. and Lawton, M. A. 1993. Induction of benzoic acid 2-hydroxylase in virus-inoculated tobacco Plant Physiol. 103: 323–328.

    PubMed  Google Scholar 

  • Loake, G. J., Faktor, O., Lamb, C. J. and Dixon, R. A. 1992. Combination of H-box [CCTACC(N)7CT] and G-box (CACGTG) cis elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate p-coumaric acid. Proc. Natl. Acad. Sci. USA. 89: 9230–9234.

    PubMed  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.

    PubMed  Google Scholar 

  • Marcotte, W. R., Jr., Russell, S. H. and Quatrano, R. S. 1989. Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1: 969–976.

    PubMed  Google Scholar 

  • Mason, H. S., DeWald, D. B. and Mullet, J. E. 1993. Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5: 241–251.

    PubMed  Google Scholar 

  • Mckendree, W. L. and Ferl, R. J. 1992. Functional elements of the Arabidopsis Adh promoter include the G-box. Plant Mol. Biol. 19: 859–862.

    PubMed  Google Scholar 

  • Mehdy, M. C. 1994. Active oxygen species in plant defense against pathogen. Plant Physiol. 105: 467–472.

    PubMed  Google Scholar 

  • Miki, R., Kadota, K., Bono, H., Mizuno, Y., Tomaru, Y., Carninci, P., Itoh, M., Shibata, K., Kawai, J., Konno, H., Watanabe, S., Sato, K., Tokusumi, Y., Kikuchi, N., Ishii, Y., Hamaguchi, Y., Nishizuka, I., Goto, H., Nitanda, H., Satomi, S., Yoshiki, A., Kusakabe, M., DeRisi, J. L., Eisen, M. B., Iyer, V. R., Brown, P. O., Muramatsu, M., Shimada, H., Okazaki, Y. and Hayashizaki, Y. 2001. Delineating developmental and metabolic pathways in vivo by expression profiling using the RIKEN set of 18, 816 full-length enriched mouse cDNA arrays. Proc. Natl. Acad. Sci. USA 98: 2199–2204.

    PubMed  Google Scholar 

  • Mikkelsen, M. D., Hansen, C. H., Wittstock, U. and Halkier, B. A. 2000. Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J. Biol. Chem. 275: 33712–33717.

    PubMed  Google Scholar 

  • Mikkelsen, M. D., Petersen, B. L., Glawischnig, E., Jensen, A. B., Andreasson, E. and Halkier, B. A. 2003. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol. 131: 298–308.

    PubMed  Google Scholar 

  • Mittler, R. and Zilinskas, B. A. 1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J. 5: 397–405.

    PubMed  Google Scholar 

  • Mizutani, M., Ward, E. and Ohta, D. 1998. Cytochrome P450 superfamily in Arabidopsis thaliana: isolation of cDNAs, differential expression, and RFLP mapping of multiple cytochromes P450. Plant Mol. Biol. 37: 39–52.

    PubMed  Google Scholar 

  • Mundy, J., Yamaguchi-Shinozaki, K. and Chua, N.-H. 1990. Nuclear proteins bind conserved elements in the abscisic acidresponsive promoter of a rice rab gene. Proc. Natl. Acad. Sci. USA 87: 1406–1410.

    PubMed  Google Scholar 

  • Narusaka, Y., Narusaka, M., Seki, M., Fujita, M., Ishida, J., Nakashima, M., Enju, A., Sakurai, T., Satou, M., Kamiya, A., Park, P., Kobayashi, M. and Shinozaki, K. 2003a. Expression profiles of Arabidopsis phospholipase A IIA gene in response to biotic and abiotic stresses. Plant Cell Physiol. 44: 1246–1252

    PubMed  Google Scholar 

  • Narusaka, Y., Narusaka, M., Seki, M., Ishida, J., Nakashima, M., Enju, A., Kamiya, A., Sakurai, T., Satoh, M., Kobayashi, M., Tosa, Y., Park, P. and Shinozaki, K. 2003b. The cDNA microarray analysis using an Arabidopsis pad3 mutant reveals the expression profiles and classification of genes induced by Alternaria brassicicola attack. Plant Cell Physiol. 44: 377–387.

    PubMed  Google Scholar 

  • Normanly, J. and Bartel, B. 1999. Redundancy as a way of life–IAA metabolism. Curr. Opin. Plant Biol. 2: 207–213.

    PubMed  Google Scholar 

  • Paquette, S. M., Bak, S. and Feyereisen, R. 2000. Intron-exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana. DNA Cell Biol. 19: 307–317.

    PubMed  Google Scholar 

  • Penninckx, I. A. M. A., Thomma, B. P. H. J., Buchala, A., Metraux, J.-P. and Broekaert, W. F. 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103–2113.

    PubMed  Google Scholar 

  • Radwanski, E. R. and Last, R. L. 1995. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7: 921–934.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Reuveni, M., Agapov, V. and Reuveni, R. 1997. A foliar spray of micronutrient solutions induces local and systemic protection against powdery mildew (Sphaerotheca fuliginia) in cucumber plants. Europ. J. Plant Pathol. 103: 581–588.

    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.

    PubMed  Google Scholar 

  • Riviere, J. L. and Cabbane, F. 1987. Animal and plant cytochrome P450 systems. Biochemie 69: 743–752.

    Google Scholar 

  • Rushmore, T. H., Morton, M. R. and Pickett, C. B. 1991. The antioxidant responsive element. J. Biol. Chem. 266: 11632–11639.

    PubMed  Google Scholar 

  • Sandermann, H. 1992. Xenobiotics. Trends Biochem. Sci. 17: 82–84.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Schopfer, C. R. and Ebel, J. 1998. Identification of elicitorinduced cytochrome P450s of soybean (Glycine max L. ) using differential display of mRNA. Mol. Gen. Genet. 258: 315–322.

    PubMed  Google Scholar 

  • Schuler, M. A. 1996. Plant cytochrome P450 monooxygenases. Crit. Rev. Plant Sci. 15: 235–284.

    Google Scholar 

  • 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.

    PubMed  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. 2002a. Monitoring the expression profiles of ca. 7000 Arabidopsis genes under drought, cold, and highsalinity stresses using a full-length cDNA microarray. Plant J 31: 279–292.

    PubMed  Google Scholar 

  • Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., Oono, Y., Muramatsu, M., Hayashizaki, Y., Kawai, J., Carninci, P., Itoh, M., Ishii, Y., Arakawa, T., Shibata, K., Shinagawa, A., and Shinozaki, K. 2002b. Functional annotation of a full-length Arabidopsis cDNA collection. Science 296: 141–145.

    PubMed  Google Scholar 

  • Seo, S., Sano, H. and Ohashi, Y. 1997. Jasmonic acid in wound signal transduction pathways. Physiol. Plant 101: 740–745.

    Google Scholar 

  • Shah, J., Kachroo, P. and Klessig, D. F. 1999. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell 11: 191–206.

    PubMed  Google Scholar 

  • Shen, Q., Zhang, P. and Ho, T. H. D. 1996. Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8: 1107–1119.

    PubMed  Google Scholar 

  • Shen, Q. and Ho, T. H. D. 1995. Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7: 295–307.

    PubMed  Google Scholar 

  • Shinozaki, K. and Yamaguchi-Shinozaki, K. 1999. Molecular responses to drought stress. In: K. Shinozaki and K. Yamaguchi-Shinozaki (s.) Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants, R. G. Landes Co., Austin, Texas: pp. 11–28.

    Google Scholar 

  • Shinozaki, K. and Yamaguchi-Shinozaki, K. 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3: 217–223.

    PubMed  Google Scholar 

  • Smolen, G. and Bender, J. 2002. Arabidopsis cytochrome P450 cyp83B1 mutations activate the tryptophan biosynthetic pathway. Genetics 160: 323–332.

    PubMed  Google Scholar 

  • Teutsch, H. G., Hasenfralz, M. P., Lesot, A., Stolz, C., Garnier, J. M., Jeltsch, J. M., Durst, F. and Werck-Reichhart, D. 1993. Isolation and sequence of a cDNA encoding the Jerusalem artichoke cinnamate 4-hydroxylase, a major plant cytochrome P450 involved in the general phenylpropanoid pathway. Proc. Natl. Acad. Sci. USA 90: 4102–4106.

    PubMed  Google Scholar 

  • Thomma, B. P. H. J., Eggermont, K., Tierens, K. F. and Broekaert, W. F. 1999a. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121: 1093–1101.

    PubMed  Google Scholar 

  • Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A. 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. Sci. USA 95: 15107–15111.

    Google Scholar 

  • Thomma, B. P. H. J., Nelissen, I., Eggermont, K. and Broekaert, W. F. 1999b. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alteraria brassicicola. Plant J. 19: 163–171.

    PubMed  Google Scholar 

  • Tierens, K. F., Thomma, B. P., Bari, R. P., Garmier, M., Eggermont, K., Brouwer, M., Penninckx, I. A., Broekaert, W. F. and Cammue, B. P. 2002. Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defense responses by reactive oxygen generating compounds. Plant J. 29: 131–40.

    PubMed  Google Scholar 

  • Yamaguchi-Shinozaki, K. and Shinozaki, K. 1994. A novel cisacting element in an Arabidopsis gene is involved in respon-siveness to drought, low-temperature, or high-salinity stress. Plant Cell 6: 251–264

    PubMed  Google Scholar 

  • Zhao, J. and Last, R. L. 1996. Coordinate regulation of the tryptophan biosynthetic pathway and indolic phytoalexin accumulation in Arabidopsis. Plant Cell 8: 2235–2244.

    PubMed  Google Scholar 

  • Zhao, J., Williams, C. C. and Last, R. L. 1998. Induction of Arabidopsis tryptophan pathway enzymes and camalexin by amino acid starvation, oxidative stress, and an abiotic elicitor. Plant Cell 10: 359–370.

    PubMed  Google Scholar 

  • Zhao, Y., Hull, A. K., Gupta, N. R., Goss, K. A., Alonso, J., Ecker, J. R., Normanly, J., Chory, J. and Celenza, J. L. 2002. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Develop. 16: 3100–3112.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Tokyo Gakugei University, 4-1-1 Nukuikita-machi, Koganei-shi, Japan

    Yoshihiro narusaka & Mari Narusaka

  2. Laboratory of Plant Molecular Biology, RIKEN Tsukuba Institute, 3-1-1 Koyadai, Japan

    Yoshihiro narusaka, Motoaki Seki & Kazuo Shinozaki

  3. Plant Mutation Exploration Team, Plant Functional Genomics Research Group, RIKEN Genomic Sciences Center (GSC), RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Japan

    Mari Narusaka, Motoaki Seki, Taishi Umezawa, Junko Ishida, Maiko Nakajima, Akiko Enju & Kazuo Shinozaki

Authors
  1. Yoshihiro narusaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mari Narusaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Motoaki Seki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taishi Umezawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junko Ishida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maiko Nakajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Akiko Enju
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kazuo Shinozaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

narusaka, Y., Narusaka, M., Seki, M. et al. Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: Analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55, 327–342 (2004). https://doi.org/10.1007/s11103-004-0685-1

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-0685-1

Search

Navigation