Plant Molecular Biology

, Volume 52, Issue 3, pp 537–551

Rice gene expression in response to N-acetylchitooligosaccharide elicitor: comprehensive analysis by DNA microarray with randomly selected ESTs

  • Chiharu Akimoto-Tomiyama
  • Katsumi Sakata
  • Junshi Yazaki
  • Keiko Nakamura
  • Fumiko Fujii
  • Kanako Shimbo
  • Kimiko Yamamoto
  • Takuji Sasaki
  • Naoki Kishimoto
  • Shoshi Kikuchi
  • Naoto Shibuya
  • Eiichi Minami
Article
  • 207 Downloads

Abstract

N-acetylchitooligosaccharides are potent elicitors to suspension-cultured rice cells, inducing a set of defense reactions. Expression of defense-related genes is considered to play an important role in defense reactions, and we employed microarray analysis of 8987 randomly selected expressed sequence tags to analyze the changes in gene expression caused by N-acetylchitooctaose. In this experiment, 166 genes were significantly induced and 93 genes were repressed. RNA gel blot analysis of 16 of these genes confirmed the microarray results. Of the 259 ESTs identified as responsive to N-acetylchytooctaose, 18 genes are related to signal transduction, including five calcium-dependent protein kinases (CDPKs). Among these, three novel CDPKs responsive to N-acetylchitooctaose were isolated.

CDPK microarray N-acetylchitooligosaccharides Oryza sativa rice cells 

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References

  1. Allwood, E.G., Davies, D.R., Gerrish, C., Ellis, B.E. and Bolwell, G.P. 1999. Phosphorylation of phenylalanine ammonia-lyase: evidence for a novel protein kinase and identification of the phosphorylated residue. FEBS Lett. 457: 47-52.Google Scholar
  2. Blume, B., Nürnberger, T., Nass, N. and Sheel D. 2000. Receptormediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12: 1425-1440.Google Scholar
  3. Breviario, D., Morello, L. and Giani, S. 1995. Molecular cloning of two novel rice cDNA sequences encoding putative calciumdependent protein kinases. Plant Mol. Biol. 27: 953-967.Google Scholar
  4. Bush, S.D. 1996. Effects of gibberellic acid and environmental factors on cytosolic calcium in wheat aleurone cells. Planta 199: 89-99.Google Scholar
  5. Desikan, R., Mackerness, S., Hancock, J.T. and Neill, S.J. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127: 159-172.Google Scholar
  6. Doke, N. 1983. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Path. 23: 345-357.Google Scholar
  7. Fahrendorf, T., Ni, W., Shorrosh, B.S. and Dixon, R.A. 1995. Stress responses in alfalfa (Medicago sativa L.) XIX. Transcriptional activation of oxidative pentose phosphate pathway genes at the onset of the isoflavonoid phytoalexin response. Plant Mol. Biol. 28: 885-900.Google Scholar
  8. Harmon, A.C., Gribskov, M. and Harper, J.F. 2000. CDPKs: a kinase for every Ca2+ signal? Trends Plant Sci. 5: 154-159.Google Scholar
  9. Harmon, A.C., Gribskov, M., Gubrium, E. and Harper, J.F. 2001. The CDPK superfamily of protein kinases. New Phytol. 151: 175-183.Google Scholar
  10. He, D.-Y., Yazaki, Y., Nishizawa, Y., Takai, R., Yamada, K., Sakano, K., Shibuya, N. and Minami, E. 1998. Gene activation by cytoplasmic acidification in suspension-cultured rice cells in response to the potent elicitor, N-acetylchitoheptaose. Mol. Plant-Microbe Interact. 11: 1167-1174.Google Scholar
  11. Kapros, T., Robertson, A.J. and Waterborg, J.H. 1995. Histone H3 transcript stability in alfalfa. Plant Mol. Biol. 28: 901-914.Google Scholar
  12. Kawasaki, T., Hayashida, N., Baba, T., Shinozaki, K. and Shimada, H. 1993. The gene encoding a calcium-dependent protein kinase located near the sbe1 gene encoding starch branching enzyme I is specifically expressed in developing rice seeds. Gene 129: 183-189.Google Scholar
  13. Keller, T., Damude, H.G., Werner, D., Doerner, P., Dixon, R.A. and Lamb, C. 1998. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10: 255-266.Google Scholar
  14. Kuchitsu, K., Kikuyama, M. and Shibuya, N. 1993. Nacetylchitooligosaccharides, biotic elicitor for phytoalexin production, induce transient membrane depolarization in suspension-cultured rice cells. Protoplasma 174: 79-81.Google Scholar
  15. Kuchitsu K., Kosaka H., Shiga T. and Shibuya, N. 1995. EPR evidence for generation of hydroxyl radical triggered by Nacetylchitooligosaccharide elicitor and a protein phosphatase inhibitor in suspension-cultured rice cells. Protoplasma 188: 138-142.Google Scholar
  16. Lapous, D., Mathieu, Y., Guern, J. and Lauriére, C. 1998. Increase of defense gene transcripts by cytoplasmic acidification in tobacco cell suspension. Planta 205: 452-458.Google Scholar
  17. MacKintosh, C., Lyon, D.G. and MacKintosh, W.R. 1994. Protein phosphatase inhibitors activate anti-fungal defense responses of soybean cotyladons and cell cultures Plant J. 5: 137-147.Google Scholar
  18. Minami, E., Kuchitsu, K., He, D.-Y., Kouchi, H., Midoh, N., Ohtsuki, Y. and Shibuya, N. 1996. Two novel genes rapidly and transiently activated in suspension-cultured rice cells by treatment with N-acetylchitoheptaose, a biotic elicitor for phytoalexin production. Plant Cell Physiol. 37: 563-567.Google Scholar
  19. Nishizawa, Y., Kawakami, A., Hibi, T., He, D.-Y., Shibuya, N. and Minami, E. 1999. Regulation of the chitinase gene expression in suspension-cultured rice cells by N-acetylchitooligosaccharides: differences in the signal transduction pathways leading to the activation of elicitor-responsive genes. Plant Mol. Biol. 39: 907-914.Google Scholar
  20. Nojiri, H., Sugimori, M., Yamane, H., Nishimura, Y., Yamada, A., Shibuya, N., Kodama, O., Murofushi, N. and Omori, T. 1996. Involvement of jasmonic acid in elicitor-induced phytoalexin production in suspension-cultured rice cells. Plant Physiol. 110: 387-392.Google Scholar
  21. Nürnberger, T. and Scheel, D. 2001. Signal transmission in the plant immune response. Trends Plant Sci. 6: 372-379.Google Scholar
  22. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., Sharma, S.B., Klessig, D.F., Martienssen, R., Mattsson, O., Jensen, A.B. and Mundy, J. 2000. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103: 1111-1120.Google Scholar
  23. Ramonell, K.M., Zhang, B., Ewing R.M., Chen, Y., Xu, D., Stacey, G. and Somerville, S. 2002. Microarray analysis of chitin elicitation in Arabidopsis thaliana. Mol. Plant Path. 3: 301-311.Google Scholar
  24. Robertson, D., Davies, D.R., Gerrish, C., Jupe, S.C. and Bolwell, G.P. 1995.Rapid changes in oxidative metabolism as a consequence of elicitor treatment of suspension-cultured cells of French bean (Phaseolus vulgaris L.). Plant Mol. Biol. 27: 59-67.Google Scholar
  25. Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K. and Izui, K. 2000. Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J. 23: 319-327.Google Scholar
  26. Schaffer, R., Landgraf, J., Accerbi, M., Simon, V.V., Larson, M. and Wisman, E. 2001. Microarray analysis of diurnal and circadianregulated genes in Arabidopsis. Plant Cell 13: 113-123.Google Scholar
  27. 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.Google Scholar
  28. 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.Google Scholar
  29. Sheen, J. 1996. Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274: 1900-1902.Google Scholar
  30. Tähtiharju, S., Sangwan, V., Monroy, A.F., Dhindsa, R.S. and Borg, M. 1997. The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203: 442-447.Google Scholar
  31. Takahashi, K., Isobe, M. and Muto, S. 1997. An increase in cytosolic calcium ion concentration precedes hypoosmotic shockinduced activation of protein kinases in tobacco suspension culture cells. FEBS Lett. 401: 202-206.Google Scholar
  32. Takai, R., Hasegawa, K., Kaku, H., Shibuya, N. and Minami, E. 2001. Isolation and analysis of expression mechanisms of a rice gene, EL5, which shows structural similarity to ATL family from Arabidopsis, in response to N-acetylchitooligosaccharide elicitor. Plant Sci. 160: 577-583.Google Scholar
  33. Tenhaken, R. and Rübel, C. 1998. Induction of alkalinization and an oxidative burst by low doses of cycloheximide in soybean cells. Planta 206: 666-672.Google Scholar
  34. Thimm, O., Essigmann, B., Kloska, S., Altmann, T. and Buckhout, T.J. 2001. Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol. 127: 1030-1043.Google Scholar
  35. Urao, T., Katagiri, T., Mizoguchi, T., Yamaguchi-Shinozaki, K., Hayashida, N. and Shinozaki, K. 1994. Two genes that encode Ca2+-dependent protein-kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol. Gen. Genet. 244: 331-340.Google Scholar
  36. Wasternack, C. and Parthier, B. 1997. Jasmonate-signalled plant gene expression. Trend Plant Sci. 2: 302-307.Google Scholar
  37. Watanabe, A. and Price, C.A. 1982. Translation of mRNAs for subunits of chloroplast coupling factor 1 in spinach. Proc. Natl. Acad. Sci. USA 79: 6304-6308.Google Scholar
  38. Yamada, A., Shibuya, N., Kodama, O. and Akatsuka, T. 1993. Induction of phytoalexin formation in suspension-cultured rice cells by N-acetylchitooligosaccharides. Biosci. Biotech. Biochem. 57: 405-409.Google Scholar
  39. Yazaki, J., Kishimoto, N., Nakamura, K., Fujii, F., Shimbo, K., Otsuka, Y., Wu, J., Yamamoto, K., Sakata, K., Sasaki, T. and Kikuchi S. 2000. Embarking on rice functional genomics via cDNA microarray: use of 3? UTR probes for specific gene expression analysis. DNA Res. 7: 367-370.Google Scholar
  40. Yoon, G.M., Cho, H.S., Ha, H.J., Liu, J.R. and Lee, H.S.P. 1999. Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol. Biol. 39: 991-1001.Google Scholar
  41. Zhang, B., Ramonell, K., Smerville, S. and Stacey, G. 2002. Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 15: 963-970.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Chiharu Akimoto-Tomiyama
    • 1
  • Katsumi Sakata
    • 2
  • Junshi Yazaki
    • 3
  • Keiko Nakamura
    • 4
  • Fumiko Fujii
    • 4
  • Kanako Shimbo
    • 4
  • Kimiko Yamamoto
    • 4
  • Takuji Sasaki
    • 2
  • Naoki Kishimoto
    • 3
  • Shoshi Kikuchi
    • 3
  • Naoto Shibuya
    • 1
  • Eiichi Minami
    • 1
  1. 1.Department of BiochemistryJapan
  2. 2.Department of Genome ResearchJapan
  3. 3.Department of Molecular GeneticsNational Institute of Agrobiological SciencesTsukubaJapan
  4. 4.STAFF InstituteKamiyokoba, TsukubaJapan

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