Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid.

Publisher: Oxford University Press Country of Publication: England NLM ID: 9208688 Publication Model: Print Cited Medium: Internet ISSN: 1532-298X (Electronic) Linking ISSN: 10404651 NLM ISO Abbreviation: Plant Cell Subsets: MEDLINE

Publication: 2021- : [Oxford] : Oxford University Press
Original Publication: Rockville, MD : American Society of Plant Physiologists, c1989-

Diatoms*/metabolism ; Diatoms*/genetics ; Plastids*/metabolism ; Plastids*/genetics ; Glycolysis*/genetics ; Gluconeogenesis*/genetics; Phylogeny

Organic carbon fixed in chloroplasts through the Calvin-Benson-Bassham Cycle can be diverted toward different metabolic fates, including cytoplasmic and mitochondrial respiration, gluconeogenesis, and synthesis of diverse plastid metabolites via the pyruvate hub. In plants, pyruvate is principally produced via cytoplasmic glycolysis, although a plastid-targeted lower glycolytic pathway is known to exist in non-photosynthetic tissue. Here, we characterized a lower plastid glycolysis-gluconeogenesis pathway enabling the direct interconversion of glyceraldehyde-3-phosphate and phospho-enol-pyruvate in diatoms, ecologically important marine algae distantly related to plants. We show that two reversible enzymes required to complete diatom plastid glycolysis-gluconeogenesis, Enolase and bis-phosphoglycerate mutase (PGAM), originated through duplications of mitochondria-targeted respiratory isoforms. Through CRISPR-Cas9 mutagenesis, integrative 'omic analyses, and measured kinetics of expressed enzymes in the diatom Phaeodactylum tricornutum, we present evidence that this pathway diverts plastid glyceraldehyde-3-phosphate into the pyruvate hub, and may also function in the gluconeogenic direction. Considering experimental data, we show that this pathway has different roles dependent in particular on day length and environmental temperature, and show that the cpEnolase and cpPGAM genes are expressed at elevated levels in high-latitude oceans where diatoms are abundant. Our data provide evolutionary, meta-genomic, and functional insights into a poorly understood yet evolutionarily recurrent plastid metabolic pathway.
Competing Interests: Conflict of interest statement. None declared.
(© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

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Date Created: 20240606 Date Completed: 20240903 Latest Revision: 20240905

20240905

PMC11371179

10.1093/plcell/koae168

38842420