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

doi:10.1093/plcell/koae168

	Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid
	Dorrell, Richard G.1,2,3; Zhang, Youjun 4,5,6; Liang, Yue 7,8; Gueguen, Nolwenn 9; Nonoyama, Tomomi 1,10; Croteau, Dany 11; Penot-Raquin, Mathias 1,2,3; Adiba, Sandrine 1; Bailleul, Benjamin 11; Gros, Valerie 9; Karlusich, Juan Jose Pierella 1,2; Zweig, Nathanael 1; Fernie, Alisdair R.4,5; Jouhet, Juliette 9; Marechal, Eric 9; Bowler, Chris 1,2
	2024-06-06
发表期刊	PLANT CELL
ISSN	1040-4651
页码	27
通讯作者	Dorrell, Richard G.([email protected])
摘要	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. Environmental and experimental methods reveal the importance of plastid-targeted Enolase and bis-phosphoglycerate mutase enzymes to diatoms, marine algae that contribute to global primary production.
DOI	10.1093/plcell/koae168
收录类别	SCI
语种	英语
资助项目	Agence Nationale de la Recherche (ANR) Jeune Chercheur/Jeune Chercheuse (JCJC) from 2021 to 2022[ANR-21-CE02-0014-01]; European Research Council (ERC) Starting Grant (ChloroMosaic) from 2023 to 2027[101039760]; Fonds Francais de l'Environnement Mondial (FFEM)/French Facility for Global Environment; French Government Investissements d'Avenir programs OCEANOMICS[ANR-11-BTBR-0008]; Organisation et Montee en Puissance d'une Infrastructure Nationale de Genomique (FRANCE GENOMIQUE)[ANR-10-INBS-0009]; Memory in Living Systems: An Integrative Approach (MEMOLIFE)[ANR-10-LABX-0054]; Paris Sciences et Lettres (PSL) Research University[ANR-11-IDEX-0001-02]; European Research Council (ERC) research and innovation program (Diatomic)[835067]; ANR BrownCut project[ANR-19-CE20-0020]; ANR DIM[ANR-21-CE02-0021]; Programmes et Equipements Prioritaires de la Recherche (PEPR) Novel Strategies for the Development of Microalgae as Renewable Biofuel Resources (AlgAdvance)[A-22-PEBB-0002]; European Regional Development Fund (ERDF); Labex GRAL[10-LABX-0049]; University Grenoble Alpes graduate school (Ecoles Universitaires de Recherche) Chimie-Biologie-Sante CBH-EUR-GS[A-17-EURE-0003]; European Research Council (ERC) research and innovation program[739582]; European Research Council (ERC) research and innovation program[66462]; European Regional Development Fund through the Bulgarian Science and Education for Smart Growth Operational Programme[BG05M2OP001-1.003-001-C01]; European Research Council (ERC) under the research and innovation program (PhotoPHYTOMIX project)[715579]; Centre National de la Recherche Scientifique (CNRS) Momentum Fellowship (The Carbon Cycle Revisited) 2019 to 2021
WOS研究方向	Biochemistry & Molecular Biology ; Plant Sciences ; Cell Biology
WOS类目	Biochemistry & Molecular Biology ; Plant Sciences ; Cell Biology
WOS记录号	WOS:001255673200001
出版者	OXFORD UNIV PRESS INC
WOS关键词	MARINE DIATOM ; PREDICTION ; ACID ; TOOL ; LOCALIZATION ; ORGANIZATION ; EVOLUTION ; BIOSYNTHESIS ; ASSIMILATION ; EXPRESSION
引用统计
文献类型	期刊论文
条目标识符	http://ir.qdio.ac.cn/handle/337002/186405
专题	深海极端环境与生命过程研究中心
通讯作者	Dorrell, Richard G.
作者单位	1.Univ PSL, INSERM, CNRS, Inst Biol ENS IBENS,Ecole Normale Super,Dept Biol, F-75005 Paris, France 2.CNRS, Res Federat Study Global Ocean Syst Ecol & Evolut, Tara Oceans GOSEE FR2022, F-75016 Paris, France 3.Sorbonne Univ, INSERM, CNRS, Inst Biol Paris Seine IBPS,Lab Computat & Quantita, F-75005 Paris, France 4.Ctr Plant Syst Biol & Biotechnol, Dept Plant Metabol, Plovdiv 4000, Bulgaria 5.Max Planck Inst Mol Plant Physiol, Cent Plant Metab Grp, D-14476 Potsdam, Germany 6.Chinese Acad Sci, Inst Genet & Dev Biol, Key Lab Seed Innovat, Beijing 100101, Peoples R China 7.Chinese Acad Sci, Inst Oceanol, Ctr Deep Sea Res, Ctr Ocean Mega Sci, Qingdao 266071, Peoples R China 8.Pilot Natl Lab Marine Sci & Technol, Lab Marine Mineral Resources, Qingdao 266237, Peoples R China 9.Univ Grenoble Alpes, CNRS, CEA, INRAE,IRIG,Lab Physiol Cellulaire & Vegetale, F-38000 Grenoble, France 10.Tokyo Univ Agr & Technol, Inst Engn, Div Biotechnol & Life Sci, Koganei, Tokyo 1848588, Japan 11.Univ PSL, Inst Biol Physico Chim IBPC, F-75005 Paris, France
推荐引用方式 GB/T 7714	Dorrell, Richard G.,Zhang, Youjun,Liang, Yue,et al. Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid[J]. PLANT CELL,2024:27.
APA	Dorrell, Richard G..,Zhang, Youjun.,Liang, Yue.,Gueguen, Nolwenn.,Nonoyama, Tomomi.,...&Bowler, Chris.(2024).Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid.PLANT CELL,27.
MLA	Dorrell, Richard G.,et al."Complementary environmental analysis and functional characterization of lower glycolysis-gluconeogenesis in the diatom plastid".PLANT CELL (2024):27.