Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid. Dorrell, R. G., Zhang, Y., Liang, Y., Gueguen, N., Nonoyama, T., Croteau, D., Penot-Raquin, M., Adiba, S., Bailleul, B., Gros, V., Pierella Karlusich, J. J., Zweig, N., Fernie, A. R., Jouhet, J., Marechal, E., & Bowler, C. Plant Cell, 36(9):3584-3610, 2024. Dorrell, Richard G Zhang, Youjun Liang, Yue Gueguen, Nolwenn Nonoyama, Tomomi Croteau, Dany Penot-Raquin, Mathias Adiba, Sandrine Bailleul, Benjamin Gros, Valerie Pierella Karlusich, Juan Jose Zweig, Nathanael Fernie, Alisdair R Jouhet, Juliette Marechal, Eric Bowler, Chris eng ANR-21-CE02-0014-01/ANR/ ANR-11-BTBR-0008/French Facility for Global Environment/ ANR-10-INBS-09-08/FRANCE GENOMIQUE/ ANR-10-LABX-54/MEMO LIFE/ ANR-11-IDEX-0001-02/PSL Research University/ ERC_/European Research Council/International 835067/European Union's Horizon 2020/ ANR-19-CE20-0020/ANR/ 22-PEBB-0002/PEPR AlgAdvance/ 10-LABX-0049/European Regional Development Fund/ University Grenoble Alpes/ ANR-17-EURE-0003/Ecoles Universitaires de Recherche/ 739582/European Union's Horizon 2020/ 715579/European Union's Horizon 2020/ England 2024/06/06 Plant Cell. 2024 Sep 3;36(9):3584-3610. doi: 10.1093/plcell/koae168.
Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid [link]Paper  doi  abstract   bibtex   1 download  
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.
@article{RN300,
   author = {Dorrell, R. G. and Zhang, Y. and Liang, Y. and Gueguen, N. and Nonoyama, T. and Croteau, D. and Penot-Raquin, M. and Adiba, S. and Bailleul, B. and Gros, V. and Pierella Karlusich, J. J. and Zweig, N. and Fernie, A. R. and Jouhet, J. and Marechal, E. and Bowler, C.},
   title = {Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid},
   journal = {Plant Cell},
   volume = {36},
   number = {9},
   pages = {3584-3610},
   note = {Dorrell, Richard G
Zhang, Youjun
Liang, Yue
Gueguen, Nolwenn
Nonoyama, Tomomi
Croteau, Dany
Penot-Raquin, Mathias
Adiba, Sandrine
Bailleul, Benjamin
Gros, Valerie
Pierella Karlusich, Juan Jose
Zweig, Nathanael
Fernie, Alisdair R
Jouhet, Juliette
Marechal, Eric
Bowler, Chris
eng
ANR-21-CE02-0014-01/ANR/
ANR-11-BTBR-0008/French Facility for Global Environment/
ANR-10-INBS-09-08/FRANCE GENOMIQUE/
ANR-10-LABX-54/MEMO LIFE/
ANR-11-IDEX-0001-02/PSL Research University/
ERC_/European Research Council/International
835067/European Union's Horizon 2020/
ANR-19-CE20-0020/ANR/
22-PEBB-0002/PEPR AlgAdvance/
10-LABX-0049/European Regional Development Fund/
University Grenoble Alpes/
ANR-17-EURE-0003/Ecoles Universitaires de Recherche/
739582/European Union's Horizon 2020/
715579/European Union's Horizon 2020/
England
2024/06/06
Plant Cell. 2024 Sep 3;36(9):3584-3610. doi: 10.1093/plcell/koae168.},
   abstract = {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.},
   keywords = {*Diatoms/metabolism/genetics
*Plastids/metabolism/genetics
*Glycolysis/genetics
*Gluconeogenesis/genetics
Phylogeny},
   ISSN = {1532-298X (Electronic)
1040-4651 (Print)
1040-4651 (Linking)},
   DOI = {10.1093/plcell/koae168},
   url = {https://www.ncbi.nlm.nih.gov/pubmed/38842420},
   year = {2024},
   type = {Journal Article}
}

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