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Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development

Authors

  • Hisae Kojima,

    1. Laboratory of Biochemistry, Department of Biological Functions and Mechanisms, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan,
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  • Takamasa Suzuki,

    1. Laboratory of Biochemistry, Department of Biological Functions and Mechanisms, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan,
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  • Takenori Kato,

    1. Laboratory of Biochemistry, Department of Biological Functions and Mechanisms, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan,
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  • Ken-ichi Enomoto,

    1. Laboratory of Biochemistry, Department of Biological Functions and Mechanisms, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan,
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  • Shusei Sato,

    1. Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan,
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  • Tomohiko Kato,

    1. Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan,
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  • Satoshi Tabata,

    1. Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan,
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  • Julio Sáez-Vasquez,

    1. Laboratoire Génome et Développement des Plantes, UMR CNRS-IRD 5096, Université de Perpignan, 66860 Perpignan Cedex, France, and
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  • Manuel Echeverría,

    1. Laboratoire Génome et Développement des Plantes, UMR CNRS-IRD 5096, Université de Perpignan, 66860 Perpignan Cedex, France, and
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  • Tsuyoshi Nakagawa,

    1. Research Institute of Molecular Genetics, Shimane University, Matsue, Shimane 690-8504, Japan
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  • Sumie Ishiguro,

    1. Laboratory of Biochemistry, Department of Biological Functions and Mechanisms, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan,
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  • Kenzo Nakamura

    Corresponding author
    1. Laboratory of Biochemistry, Department of Biological Functions and Mechanisms, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8601, Japan,
      (fax +81 52 789 4094; e-mail kenzo@agr.nagoya-u.ac.jp).
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(fax +81 52 789 4094; e-mail kenzo@agr.nagoya-u.ac.jp).

Summary

Animal and yeast nucleolin function as global regulators of ribosome synthesis, and their expression is tightly linked to cell proliferation. Although Arabidopsis contains two genes for nucleolin, AtNuc-L1 is the predominant if not only form of the protein found in most tissues, and GFP–AtNuc-L1 fusion proteins were targeted to the nucleolus. Expression of AtNuc-L1 was strongly induced by sucrose or glucose but not by non-metabolizable mannitol or 2-deoxyglucose. Sucrose also caused enhanced expression of genes for subunits of C/D and H/ACA small nucleolar ribonucleoproteins, as well as a large number of genes for ribosomal proteins (RPs), suggesting that carbohydrate availability regulates de novo ribosome synthesis. In sugar-starved cells, induction of AtNuc-L1 occurred with 10 mm glucose, which seemed to be a prerequisite for resumption of growth. Disruption of AtNuc-L1 caused an increased steady-state level of pre-rRNA relative to mature 25S rRNA, and resulted in various phenotypes that overlap those reported for several RP gene mutants, including a reduced growth rate, prolonged lifetime, bushy growth, pointed leaf, and defective vascular patterns and pod development. These results suggest that the rate of ribosome synthesis in the meristem has a strong impact not only on the growth but also the structure of plants. The AtNuc-L1 disruptant exhibited significantly reduced sugar-induced expression of RP genes, suggesting that AtNuc-L1 is involved in the sugar-inducible expression of RP genes.

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