Rice alcohol dehydrogenase 1 promotes survival and has a major impact on carbohydrate metabolism in the embryo and endosperm when seeds are germinated in partially oxygenated water

H. Takahashi, Hendrik Greenway, H. Matsumura, N. Tsutsumi, M. Nakazono

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    21 Citations (Scopus)

    Abstract

    Background and AimsRice (Oryza sativa) has the rare ability to germinate and elongate a coleoptile under oxygen-deficient conditions, which include both hypoxia and anoxia. It has previously been shown that ALCOHOL DEHYDROGENASE 1 (ADH1) is required for cell division and cell elongation in the coleoptile of submerged rice seedlings by means of studies using a rice ADH1-deficient mutant, reduced adh activity (rad). The aim of this study was to understand how low ADH1 in rice affects carbohydrate metabolism in the embryo and endosperm, and lactate and alanine synthesis in the embryo during germination and subsequent coleoptile growth in submerged seedlings.MethodsWild-type and rad mutant rice seeds were germinated and grown under complete submergence. At 1, 3, 5 and 7 d after imbibition, the embryo and endosperm were separated and several of their metabolites were measured and compared.Key resultsIn the rad embryo, the rate of ethanol fermentation was halved, while lactate and alanine concentrations were 2·4-and 5·7-fold higher in the mutant than in the wild type. Glucose and fructose concentrations in the embryos increased with time in the wild type, but not in the rad mutant. The rad mutant endosperm had lower amounts of the α-amylases RAMY1A and RAMY3D, resulting in less starch degradation and lower glucose concentrations.ConclusionsThese results suggest that ADH1 is essential for sugar metabolism via glycolysis to ethanol fermentation in both the embryo and endosperm. In the endosperm, energy is presumably needed for synthesis of the amylases and for sucrose synthesis in the endosperm, as well as for sugar transport to the embryo. © 2014 The Author.
    Original languageEnglish
    Pages (from-to)851-859
    JournalAnnals of Botany
    Volume113
    Issue number5
    DOIs
    Publication statusPublished - 2014

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    alcohol dehydrogenase
    carbohydrate metabolism
    embryo (plant)
    endosperm
    rice
    seeds
    coleoptiles
    mutants
    water
    ethanol fermentation
    amylases
    alanine
    synthesis
    lactates
    hypoxia
    sugars
    glucose
    seedlings
    submergence
    imbibition

    Cite this

    @article{4454d93b33d24dd2b0922346f305664e,
    title = "Rice alcohol dehydrogenase 1 promotes survival and has a major impact on carbohydrate metabolism in the embryo and endosperm when seeds are germinated in partially oxygenated water",
    abstract = "Background and AimsRice (Oryza sativa) has the rare ability to germinate and elongate a coleoptile under oxygen-deficient conditions, which include both hypoxia and anoxia. It has previously been shown that ALCOHOL DEHYDROGENASE 1 (ADH1) is required for cell division and cell elongation in the coleoptile of submerged rice seedlings by means of studies using a rice ADH1-deficient mutant, reduced adh activity (rad). The aim of this study was to understand how low ADH1 in rice affects carbohydrate metabolism in the embryo and endosperm, and lactate and alanine synthesis in the embryo during germination and subsequent coleoptile growth in submerged seedlings.MethodsWild-type and rad mutant rice seeds were germinated and grown under complete submergence. At 1, 3, 5 and 7 d after imbibition, the embryo and endosperm were separated and several of their metabolites were measured and compared.Key resultsIn the rad embryo, the rate of ethanol fermentation was halved, while lactate and alanine concentrations were 2·4-and 5·7-fold higher in the mutant than in the wild type. Glucose and fructose concentrations in the embryos increased with time in the wild type, but not in the rad mutant. The rad mutant endosperm had lower amounts of the α-amylases RAMY1A and RAMY3D, resulting in less starch degradation and lower glucose concentrations.ConclusionsThese results suggest that ADH1 is essential for sugar metabolism via glycolysis to ethanol fermentation in both the embryo and endosperm. In the endosperm, energy is presumably needed for synthesis of the amylases and for sucrose synthesis in the endosperm, as well as for sugar transport to the embryo. {\circledC} 2014 The Author.",
    author = "H. Takahashi and Hendrik Greenway and H. Matsumura and N. Tsutsumi and M. Nakazono",
    year = "2014",
    doi = "10.1093/aob/mct305",
    language = "English",
    volume = "113",
    pages = "851--859",
    journal = "Annals of Botany",
    issn = "0305-7364",
    publisher = "OXFORD UNIV PRESS UNITED KINGDOM",
    number = "5",

    }

    Rice alcohol dehydrogenase 1 promotes survival and has a major impact on carbohydrate metabolism in the embryo and endosperm when seeds are germinated in partially oxygenated water. / Takahashi, H.; Greenway, Hendrik; Matsumura, H.; Tsutsumi, N.; Nakazono, M.

    In: Annals of Botany, Vol. 113, No. 5, 2014, p. 851-859.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Rice alcohol dehydrogenase 1 promotes survival and has a major impact on carbohydrate metabolism in the embryo and endosperm when seeds are germinated in partially oxygenated water

    AU - Takahashi, H.

    AU - Greenway, Hendrik

    AU - Matsumura, H.

    AU - Tsutsumi, N.

    AU - Nakazono, M.

    PY - 2014

    Y1 - 2014

    N2 - Background and AimsRice (Oryza sativa) has the rare ability to germinate and elongate a coleoptile under oxygen-deficient conditions, which include both hypoxia and anoxia. It has previously been shown that ALCOHOL DEHYDROGENASE 1 (ADH1) is required for cell division and cell elongation in the coleoptile of submerged rice seedlings by means of studies using a rice ADH1-deficient mutant, reduced adh activity (rad). The aim of this study was to understand how low ADH1 in rice affects carbohydrate metabolism in the embryo and endosperm, and lactate and alanine synthesis in the embryo during germination and subsequent coleoptile growth in submerged seedlings.MethodsWild-type and rad mutant rice seeds were germinated and grown under complete submergence. At 1, 3, 5 and 7 d after imbibition, the embryo and endosperm were separated and several of their metabolites were measured and compared.Key resultsIn the rad embryo, the rate of ethanol fermentation was halved, while lactate and alanine concentrations were 2·4-and 5·7-fold higher in the mutant than in the wild type. Glucose and fructose concentrations in the embryos increased with time in the wild type, but not in the rad mutant. The rad mutant endosperm had lower amounts of the α-amylases RAMY1A and RAMY3D, resulting in less starch degradation and lower glucose concentrations.ConclusionsThese results suggest that ADH1 is essential for sugar metabolism via glycolysis to ethanol fermentation in both the embryo and endosperm. In the endosperm, energy is presumably needed for synthesis of the amylases and for sucrose synthesis in the endosperm, as well as for sugar transport to the embryo. © 2014 The Author.

    AB - Background and AimsRice (Oryza sativa) has the rare ability to germinate and elongate a coleoptile under oxygen-deficient conditions, which include both hypoxia and anoxia. It has previously been shown that ALCOHOL DEHYDROGENASE 1 (ADH1) is required for cell division and cell elongation in the coleoptile of submerged rice seedlings by means of studies using a rice ADH1-deficient mutant, reduced adh activity (rad). The aim of this study was to understand how low ADH1 in rice affects carbohydrate metabolism in the embryo and endosperm, and lactate and alanine synthesis in the embryo during germination and subsequent coleoptile growth in submerged seedlings.MethodsWild-type and rad mutant rice seeds were germinated and grown under complete submergence. At 1, 3, 5 and 7 d after imbibition, the embryo and endosperm were separated and several of their metabolites were measured and compared.Key resultsIn the rad embryo, the rate of ethanol fermentation was halved, while lactate and alanine concentrations were 2·4-and 5·7-fold higher in the mutant than in the wild type. Glucose and fructose concentrations in the embryos increased with time in the wild type, but not in the rad mutant. The rad mutant endosperm had lower amounts of the α-amylases RAMY1A and RAMY3D, resulting in less starch degradation and lower glucose concentrations.ConclusionsThese results suggest that ADH1 is essential for sugar metabolism via glycolysis to ethanol fermentation in both the embryo and endosperm. In the endosperm, energy is presumably needed for synthesis of the amylases and for sucrose synthesis in the endosperm, as well as for sugar transport to the embryo. © 2014 The Author.

    U2 - 10.1093/aob/mct305

    DO - 10.1093/aob/mct305

    M3 - Article

    VL - 113

    SP - 851

    EP - 859

    JO - Annals of Botany

    JF - Annals of Botany

    SN - 0305-7364

    IS - 5

    ER -