Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis

Koichi Kobayashi, Takafumi Narise, Kintake Sonoike, Haruki Hashimoto, Naoki Sato, Maki Kondo, Mikio Nishimura, Mayuko Sato, Kiminori Toyooka, Keiko Sugimoto, Hajime Wada, Tatsuru Masuda, Hiroyuki Ohta

    Research output: Contribution to journalArticle

    46 Citations (Scopus)

    Abstract

    The galactolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) are the predominant lipids in thylakoid membranes and indispensable for photosynthesis. Among the three isoforms that catalyze MGDG synthesis in Arabidopsis thaliana, MGD1 is responsible for most galactolipid synthesis in chloroplasts, whereas MGD2 and MGD3 are required for DGDG accumulation during phosphate (Pi) starvation. A null mutant of Arabidopsis MGD1 (mgd1-2), which lacks both galactolipids and shows a severe defect in chloroplast biogenesis under nutrient-sufficient conditions, accumulated large amounts of DGDG, with a strong induction of MGD2/3 expression, during Pi starvation. In plastids of Pi-starved mgd1-2 leaves, biogenesis of thylakoid-like internal membranes, occasionally associated with invagination of the inner envelope, was observed, together with chlorophyll accumulation. Moreover, the mutant accumulated photosynthetic membrane proteins upon Pi starvation, indicating a compensation for MGD1 deficiency by Pi stress-induced galactolipid biosynthesis. However, photosynthetic activity in the mutant was still abolished, and light-harvesting/photosystem core complexes were improperly formed, suggesting a requirement for MGDG for proper assembly of these complexes. During Pi starvation, distribution of plastid nucleoids changed concomitantly with internal membrane biogenesis in the mgd1-2 mutant. Moreover, the reduced expression of nuclear-and plastid-encoded photosynthetic genes observed in the mgd1-2 mutant under Pi-sufficient conditions was restored after Pi starvation. In contrast, Pi starvation had no such positive effects in mutants lacking chlorophyll biosynthesis. These observations demonstrate that galactolipid biosynthesis and subsequent membrane biogenesis inside the plastid strongly influence nucleoid distribution and the expression of both plastidand nuclear-encoded photosynthetic genes, independently of photosynthesis.

    Original languageEnglish
    Pages (from-to)250-261
    Number of pages12
    JournalPlant Journal
    Volume73
    Issue number2
    DOIs
    Publication statusPublished - 2013 Jan

    Fingerprint

    Galactolipids
    Photosynthetic Reaction Center Complex Proteins
    galactolipids
    Thylakoids
    Chloroplasts
    Starvation
    Arabidopsis
    thylakoids
    starvation
    Plastids
    chloroplasts
    biosynthesis
    mutants
    plastids
    Photosynthesis
    Chlorophyll
    Membranes
    photosynthesis
    chlorophyll
    synthesis

    Keywords

    • Arabidopsis thaliana
    • Chloroplast biogenesis
    • Digalactosyldiacylglycerol
    • Monogalactosyldiacylglycerol
    • Photosynthesis
    • Plastid nucleoid

    ASJC Scopus subject areas

    • Plant Science
    • Cell Biology
    • Genetics

    Cite this

    Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis. / Kobayashi, Koichi; Narise, Takafumi; Sonoike, Kintake; Hashimoto, Haruki; Sato, Naoki; Kondo, Maki; Nishimura, Mikio; Sato, Mayuko; Toyooka, Kiminori; Sugimoto, Keiko; Wada, Hajime; Masuda, Tatsuru; Ohta, Hiroyuki.

    In: Plant Journal, Vol. 73, No. 2, 01.2013, p. 250-261.

    Research output: Contribution to journalArticle

    Kobayashi, K, Narise, T, Sonoike, K, Hashimoto, H, Sato, N, Kondo, M, Nishimura, M, Sato, M, Toyooka, K, Sugimoto, K, Wada, H, Masuda, T & Ohta, H 2013, 'Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis', Plant Journal, vol. 73, no. 2, pp. 250-261. https://doi.org/10.1111/tpj.12028
    Kobayashi, Koichi ; Narise, Takafumi ; Sonoike, Kintake ; Hashimoto, Haruki ; Sato, Naoki ; Kondo, Maki ; Nishimura, Mikio ; Sato, Mayuko ; Toyooka, Kiminori ; Sugimoto, Keiko ; Wada, Hajime ; Masuda, Tatsuru ; Ohta, Hiroyuki. / Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis. In: Plant Journal. 2013 ; Vol. 73, No. 2. pp. 250-261.
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    abstract = "The galactolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) are the predominant lipids in thylakoid membranes and indispensable for photosynthesis. Among the three isoforms that catalyze MGDG synthesis in Arabidopsis thaliana, MGD1 is responsible for most galactolipid synthesis in chloroplasts, whereas MGD2 and MGD3 are required for DGDG accumulation during phosphate (Pi) starvation. A null mutant of Arabidopsis MGD1 (mgd1-2), which lacks both galactolipids and shows a severe defect in chloroplast biogenesis under nutrient-sufficient conditions, accumulated large amounts of DGDG, with a strong induction of MGD2/3 expression, during Pi starvation. In plastids of Pi-starved mgd1-2 leaves, biogenesis of thylakoid-like internal membranes, occasionally associated with invagination of the inner envelope, was observed, together with chlorophyll accumulation. Moreover, the mutant accumulated photosynthetic membrane proteins upon Pi starvation, indicating a compensation for MGD1 deficiency by Pi stress-induced galactolipid biosynthesis. However, photosynthetic activity in the mutant was still abolished, and light-harvesting/photosystem core complexes were improperly formed, suggesting a requirement for MGDG for proper assembly of these complexes. During Pi starvation, distribution of plastid nucleoids changed concomitantly with internal membrane biogenesis in the mgd1-2 mutant. Moreover, the reduced expression of nuclear-and plastid-encoded photosynthetic genes observed in the mgd1-2 mutant under Pi-sufficient conditions was restored after Pi starvation. In contrast, Pi starvation had no such positive effects in mutants lacking chlorophyll biosynthesis. These observations demonstrate that galactolipid biosynthesis and subsequent membrane biogenesis inside the plastid strongly influence nucleoid distribution and the expression of both plastidand nuclear-encoded photosynthetic genes, independently of photosynthesis.",
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    AU - Sato, Naoki

    AU - Kondo, Maki

    AU - Nishimura, Mikio

    AU - Sato, Mayuko

    AU - Toyooka, Kiminori

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