Monogalactosyldiacylglycerol synthase isoforms play diverse roles inside and outside the diatom plastid

Diatoms derive from a secondary endosymbiosis event, which occurred when a eukaryotic host cell engulfed a red alga. This led to the formation of a complex plastid enclosed by four membranes: two innermost membranes originating from the red alga chloroplast envelope, and two additional peri- and epiplastidial membranes (PPM, EpM). The EpM is linked to the endoplasmic reticulum (ER). The most abundant membrane lipid in diatoms is monogalactosyldiacylglycerol (MGDG), synthesized by galactosyltransferases called MGDG synthases (MGDs), conserved in photosynthetic eukaryotes and considered to be specific to chloroplast membranes. Similar to angiosperms, a multigenic family of MGDs has evolved in diatoms, but through an independent process. We characterized MGDα, MGDβ and MGDγ in Phaeodactylum tricornutum, combining molecular analyses, heterologous expression in Saccharomyces cerevisiae, and studying overexpressing and CRISPR-Cas9-edited lines. MGDα localizes mainly to thylakoids, MGDβ to the PPM, and MGDγ to the ER and EpM. MGDs have distinct specificities for diacylglycerol, consistent with their localization. Results suggest that MGDα is required for thylakoid expansion under optimal conditions, while MGDβ and MGDγ play roles in plastid and non-plastid membranes and in response to environmental stress. Functional compensation among MGDs likely contributes to diatom resilience under adverse conditions and to their ecological success.

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Publication Details

Journal
The Plant Cell
Published
2024-10-09
DOI
https://doi.org/10.1093/plcell/koae275
Citations
6
Primary Topic
Photosynthetic Processes and Mechanisms
Type
article
Field-Weighted Citation Impact
1.40

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article

Monogalactosyldiacylglycerol synthase isoforms play diverse roles inside and outside the diatom plastid

Mathilde Cussac, Grégory Si Larbi, Juliette Salvaing, Juliette Jouhet et al.
6 citations
The Plant Cell
Photosynthetic Processes and Mechanisms
1.40
article

Monogalactosyldiacylglycerol synthase isoforms play diverse roles inside and outside the diatom plastid

Mathilde Cussac, Grégory Si Larbi, Juliette Salvaing, Juliette Jouhet, Damien Le Moigne, Dimitris Petroutsos, Éric Maréchal, Nolwenn Guéguen, Etienne Deragon, Yangmin Gong, Félix Cicéron, Valérie Gros, Marion Schilling, Alberto Amato, Morgane Michaud, Denis Falconet, Yannick Sérès, Siraba D Gueye, Hanhua Hu
article en
6 citations

Abstract

Diatoms derive from a secondary endosymbiosis event, which occurred when a eukaryotic host cell engulfed a red alga. This led to the formation of a complex plastid enclosed by four membranes: two innermost membranes originating from the red alga chloroplast envelope, and two additional peri- and epiplastidial membranes (PPM, EpM). The EpM is linked to the endoplasmic reticulum (ER). The most abundant membrane lipid in diatoms is monogalactosyldiacylglycerol (MGDG), synthesized by galactosyltransferases called MGDG synthases (MGDs), conserved in photosynthetic eukaryotes and considered to be specific to chloroplast membranes. Similar to angiosperms, a multigenic family of MGDs has evolved in diatoms, but through an independent process. We characterized MGDα, MGDβ and MGDγ in Phaeodactylum tricornutum, combining molecular analyses, heterologous expression in Saccharomyces cerevisiae, and studying overexpressing and CRISPR-Cas9-edited lines. MGDα localizes mainly to thylakoids, MGDβ to the PPM, and MGDγ to the ER and EpM. MGDs have distinct specificities for diacylglycerol, consistent with their localization. Results suggest that MGDα is required for thylakoid expansion under optimal conditions, while MGDβ and MGDγ play roles in plastid and non-plastid membranes and in response to environmental stress. Functional compensation among MGDs likely contributes to diatom resilience under adverse conditions and to their ecological success.

The Plant CellVol. 36(12)
Uppsala University (SE), Chinese Academy of Sciences (CN), Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR), CEA Grenoble (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Centre National pour la Recherche Scientifique et Technique (CNRST) (MA), Institute of Hydrobiology (CN), Chinese Academy of Agricultural Sciences (CN), Oil Crops Research Institute (CN), Université Grenoble Alpes (FR)
Agence Nationale de la Recherche, National Natural Science Foundation of China, Région Auvergne-Rhône-Alpes, Association Neurofibromatoses et Recklinghause, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Life in Land
Openalex Percentile: Top 19%
Photosynthetic Processes and Mechanisms
1.40
DOIOpen Access PDFOpenAlex
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