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The redox state of the plastoquinone (PQ) pool is connected to thylakoid lipid saturation in a marine diatom

Abstract

The redox state of the plastoquinone (PQ) pool is a known sensor for retrograde signaling. In this paper, we asked, “does the redox state of the PQ pool modulate the saturation state of thylakoid lipids?” Data from fatty acid composition and mRNA transcript abundance analyses suggest a strong connection between these two aspects in a model marine diatom. Fatty acid profiles of Phaeodactylum tricornutum exhibited specific changes when the redox state of the PQ pool was modulated by light and two chemical inhibitors [3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) or 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB)]. Data from liquid chromatography with tandem mass spectrometry (LC–MS/MS) indicated a ca. 7–20% decrease in the saturation state of all four conserved thylakoid lipids in response to an oxidized PQ pool. The redox signals generated from an oxidized PQ pool in plastids also increased the mRNA transcript abundance of nuclear-encoded C16 fatty acid desaturases (FADs), with peak upregulation on a timescale of 6 to 12 h. The connection between the redox state of the PQ pool and thylakoid lipid saturation suggests a heretofore unrecognized retrograde signaling pathway that couples photosynthetic electron transport and the physical state of thylakoid membrane lipids.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

Not applicable.

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Acknowledgements

Funding was provided by the Bennett L. Smith endowment to PGF. We thank Nicole Waite and Grace Saba for assistance in HPLC analysis. We are grateful to Kevin Wyman for help in laboratory analyses. The LIPANG platform is supported by GRAL, financed within the University Grenoble Alpes graduate school (Ecole Universitaire de Recherche) CBH-EUR-GS (ANR-17-EURE-0003), and the Auvergne-Rhône-Alpes region with the European Union via the FEDER program.

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by KYC and JJ. The first draft of the manuscript was written by KYC, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Paul G. Falkowski.

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Cheong, K.Y., Jouhet, J., Maréchal, E. et al. The redox state of the plastoquinone (PQ) pool is connected to thylakoid lipid saturation in a marine diatom. Photosynth Res (2022). https://doi.org/10.1007/s11120-022-00914-x

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Keywords

  • Diatom
  • Lipid saturation
  • PQ pool
  • Redox state
  • Retrograde signaling
  • Thylakoid membrane