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Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis

Authors

  • Yuko Sasaki-Sekimoto,

    Corresponding author
    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
      (fax +81 45 924 5823; e-mail ysasaki@bio.titech.ac.jp).
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  • Nozomi Taki,

    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
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  • Takeshi Obayashi,

    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
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  • Mitsuko Aono,

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

    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
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  • Nozomu Sakurai,

    1. Kazusa DNA Research Institute, PM NEDO laboratory, 2-6-7 Kazusa-kamatari, Kisarazu, Chiba, 292-0818, Japan,
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  • Hideyuki Suzuki,

    1. Kazusa DNA Research Institute, PM NEDO laboratory, 2-6-7 Kazusa-kamatari, Kisarazu, Chiba, 292-0818, Japan,
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  • Masami Yokota Hirai,

    1. Chiba University, Graduate School of Pharmaceutical Sciences, 1-33, Yayoi-cho, Inage-ku, Chiba, Chiba, 263-8522, Japan,
    2. CREST, JST (Japan Science and Technology Corporation), Japan,
    3. RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045, Japan, and
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  • Masaaki Noji,

    1. Chiba University, Graduate School of Pharmaceutical Sciences, 1-33, Yayoi-cho, Inage-ku, Chiba, Chiba, 263-8522, Japan,
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  • Kazuki Saito,

    1. Chiba University, Graduate School of Pharmaceutical Sciences, 1-33, Yayoi-cho, Inage-ku, Chiba, Chiba, 263-8522, Japan,
    2. CREST, JST (Japan Science and Technology Corporation), Japan,
    3. RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045, Japan, and
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  • Tatsuru Masuda,

    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
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    • Present address: Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan.

  • Ken-ichiro Takamiya,

    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
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  • Daisuke Shibata,

    1. Kazusa DNA Research Institute, PM NEDO laboratory, 2-6-7 Kazusa-kamatari, Kisarazu, Chiba, 292-0818, Japan,
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  • Hiroyuki Ohta

    1. Tokyo Institute of Technology, Graduate School of Bioscience and Biotechnology, 4259 B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa, 226–8501, Japan,
    2. Tokyo Institute of Technology, Research Center for Evolving Earth and Planets, 4259 B-14, Nagatsuta-cho, Midoritku, Yokohama, 226-8501, Japan
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(fax +81 45 924 5823; e-mail ysasaki@bio.titech.ac.jp).

Summary

Jasmonic acid (JA) and methyl jasmonate (MeJA), collectively termed jasmonates, are ubiquitous plant signalling compounds. Several types of stress conditions, such as wounding and pathogen infection, cause endogenous JA accumulation and the expression of jasmonate-responsive genes. Although jasmonates are important signalling components for the stress response in plants, the mechanism by which jasmonate signalling contributes to stress tolerance has not been clearly defined. A comprehensive analysis of jasmonate-regulated metabolic pathways in Arabidopsis was performed using cDNA macroarrays containing 13516 expressed sequence tags (ESTs) covering 8384 loci. The results showed that jasmonates activate the coordinated gene expression of factors involved in nine metabolic pathways belonging to two functionally related groups: (i) ascorbate and glutathione metabolic pathways, which are important in defence responses to oxidative stress, and (ii) biosynthesis of indole glucosinolate, which is a defence compound occurring in the Brassicaceae family. We confirmed that JA induces the accumulation of ascorbate, glutathione and cysteine and increases the activity of dehydroascorbate reductase, an enzyme in the ascorbate recycling pathway. These antioxidant metabolic pathways are known to be activated under oxidative stress conditions. Ozone (O3) exposure, a representative oxidative stress, is known to cause activation of antioxidant metabolism. We showed that O3 exposure caused the induction of several genes involved in antioxidant metabolism in the wild type. However, in jasmonate-deficient Arabidopsis 12-oxophytodienoate reductase 3 (opr3) mutants, the induction of antioxidant genes was abolished. Compared with the wild type, opr3 mutants were more sensitive to O3 exposure. These results suggest that the coordinated activation of the metabolic pathways mediated by jasmonates provides resistance to environmental stresses.

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