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Specific role of phosphatidylglycerol and functional overlaps with other thylakoid lipids in Arabidopsis chloroplast biogenesis

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Abstract

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With phosphate deficiency, the role of phosphatidylglycerol is compensated by increased glycolipid content in thylakoid membrane biogenesis but not photosynthetic electron transport in Arabidopsis chloroplasts.

Abstract

In plants and cyanobacteria, anionic phosphatidylglycerol (PG) is the only major phospholipid in thylakoid membranes, where neutral galactolipids monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) are predominant. In addition to provide a lipid bilayer matrix, PG plays a specific role in photosynthetic electron transport. Non-phosphorous sulfoquinovosyldiacylglycerol (SQDG) is another anionic lipid in thylakoids; it substitutes for PG under phosphate (Pi) deficiency to maintain proper balance of anionic charge in thylakoid membranes. Although the crucial role of PG in photosynthesis has been deeply analyzed in cyanobacteria, its physiological function in seed plants other than photosynthesis remains unclear. To reveal specific roles of PG and functional overlaps with other thylakoid lipids, we characterized a PG-deficient Arabidopsis mutant (pgp1-2) under Pi-controlled conditions. Under Pi-sufficient conditions, the proportion of PG and other thylakoid lipids was decreased in pgp1-2, which led to severe disruption of thylakoid membrane biogenesis. Under Pi-deficient conditions, the proportion of all glycolipids in the mutant was greatly increased, with that of PG further decreased. In Pi-deficient pgp1-2, thylakoid membranes remarkably developed, which was accompanied by a change in nucleoid morphology and restored expression of nuclear- and plastid-encoded photosynthesis genes. Increase in glycolipid content with Pi deficiency may compensate for the loss of PG in terms of thylakoid membrane biogenesis. Although Pi deficiency increased chlorophyll and photosynthesis protein content in pgp1-2, it critically decreased photochemical activity in PSII. Further deprivation of PG in photosynthesis complexes may abolish the PSII activity in Pi-deficient pgp1-2, which suggests that glycolipids cannot replace PG in photosynthesis.

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Acknowledgments

We thank Mayumi Wakazaki and Kei Hashimoto (CSRS, RIKEN, Yokaham, Japan) for electron microscopy. This work was supported by Grants-in-Aid for Scientific Research on Priority Areas (No. 24770055) and JST CREST from the Ministry of Education, Sports, Science and Culture in Japan.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo, 153-8902, Japan

    Koichi Kobayashi, Sho Fujii & Hajime Wada

  2. CREST, JST, 4-8-1 Honcho, Kawaguchi, Saitama, 332-0012, Japan

    Hajime Wada

  3. RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan

    Mayuko Sato & Kiminori Toyooka

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  1. Koichi Kobayashi
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  2. Sho Fujii
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  3. Mayuko Sato
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  4. Kiminori Toyooka
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  5. Hajime Wada
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Correspondence to Hajime Wada.

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Communicated by Mi Chung Suh.

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Kobayashi, K., Fujii, S., Sato, M. et al. Specific role of phosphatidylglycerol and functional overlaps with other thylakoid lipids in Arabidopsis chloroplast biogenesis. Plant Cell Rep 34, 631–642 (2015). https://doi.org/10.1007/s00299-014-1719-z

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  • DOI: https://doi.org/10.1007/s00299-014-1719-z

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