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Although the evolutionary conservation of NDPK is well established, several aspects of its diversification and functional adaptation remain unclear. The central question of this work is how NDPK evolved across plant species, focusing on the Solanaceae family and how its evolutionary history relates to the diversification of its cellular functions. Phylogenetic and molecular dating analyses showed that the division between NDPK groups 1 and 2 predates the divergence of plants and animals, whereas plant-specific NDPK types (I\u2013IV) originated early in streptophyte evolution. Solanaceae species retain a conserved set of NDPK genes, including a type III isoform with features consistent with mitochondrial targeting. Functional assays in isolated potato tuber mitochondria revealed high NDPK activity in the intermembrane space, sustaining ADP supply to oxidative phosphorylation. Activation of mitochondrial NDPK induced a phosphorylative respiratory state, which partially dissipated the mitochondrial membrane potential and significantly reduced reactive oxygen species (ROS) production. GDP and UDP were preferentially phosphorylated, conferring a stronger antioxidant effect than other nucleotides. Consistently, the mitochondrial isoform StNDPK3 was upregulated during tuber development. Together, our results demonstrate that NDPKs are evolutionarily conserved yet functionally diversified enzymes in plants and identify mitochondrial NDPK as a key modulator of mitochondrial redox homeostasis. By linking nucleotide metabolism to \u0394\u03c8m control and ROS suppression, this study highlights a previously underappreciated antioxidant mechanism that integrates mitochondrial energy metabolism with developmental and stress-related processes in plants.<\/jats:p>","DOI":"10.3390\/plants15081156","type":"journal-article","created":{"date-parts":[[2026,4,9]],"date-time":"2026-04-09T09:46:23Z","timestamp":1775727983000},"page":"1156","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Nucleoside Diphosphate Kinase Family: Evolutionary Analysis and Protective Role in Mitochondrial ROS Production"],"prefix":"10.3390","volume":"15","author":[{"given":"Douglas","family":"Jardim-Messeder","sequence":"first","affiliation":[{"name":"Programa de Biologia Molecular e Biotecnologia, Instituto de Bioqu\u00edmica M\u00e9dica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil"},{"name":"Departamento de Gen\u00e9tica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-7095-5361","authenticated-orcid":false,"given":"Ygor","family":"de Souza-Vieira","sequence":"additional","affiliation":[{"name":"Departamento de Gen\u00e9tica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thais","family":"Felix-Cordeiro","sequence":"additional","affiliation":[{"name":"Departamento de Gen\u00e9tica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3153-4112","authenticated-orcid":false,"given":"R\u00e9gis L.","family":"Corr\u00eaa","sequence":"additional","affiliation":[{"name":"Departamento de Gen\u00e9tica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil"},{"name":"Institute for Integrative Systems Biology (I2SysBio), Consejo Superior de Investigaciones Cientificas (CSIC), Universitat de Val\u00e8ncia (UV), 46980 Valencia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4532-096X","authenticated-orcid":false,"given":"Gilberto","family":"Sachetto-Martins","sequence":"additional","affiliation":[{"name":"Departamento de Gen\u00e9tica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, 21941-902 Rio de Janeiro, RJ, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,4,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1023\/A:1023433504713","article-title":"Molecular Evolution of Nucleoside Diphosphate Kinase Genes: Conserved Core Structures and Multiple-Layered Regulatory Regions","volume":"35","author":"Ishikawa","year":"2003","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1023\/A:1005532912212","article-title":"The Catalytic Mechanism of Nucleoside Diphosphate Kinases","volume":"32","author":"Lascu","year":"2000","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3487","DOI":"10.1093\/jxb\/erx183","article-title":"Affinity Purification with Metabolomic and Proteomic Analysis Unravels Diverse Roles of Nucleoside Diphosphate Kinases","volume":"68","author":"Luzarowski","year":"2017","journal-title":"J. Exp. Bot."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Desvignes, T., Pontarotti, P., Fauvel, C., and Bobe, J. (2009). Nme Protein Family Evolutionary History, a Vertebrate Perspective. BMC Evol. Biol., 9.","DOI":"10.1186\/1471-2148-9-256"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s00210-014-1009-x","article-title":"Clues to the Functions of Plant NDPK Isoforms","volume":"388","author":"Dorion","year":"2015","journal-title":"Naunyn. Schmiedebergs Arch. Pharmacol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1007\/s10555-023-10118-x","article-title":"Mechanisms of Action of NME Metastasis Suppressors\u2014A Family Affair","volume":"42","author":"Prunier","year":"2023","journal-title":"Cancer Metast. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1510","DOI":"10.1126\/science.1253768","article-title":"Nucleoside Diphosphate Kinases Fuel Dynamin Superfamily Proteins with GTP for Membrane Remodeling","volume":"344","author":"Boissan","year":"2014","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1073\/pnas.1818629116","article-title":"Two Separate Functions of NME3 Critical for Cell Survival Underlie a Neurodegenerative Disorder","volume":"116","author":"Chen","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Chen, C.-W., Tsao, N., Zhang, W., and Chang, Z.-F. (2020). NME3 Regulates Mitochondria to Reduce ROS-Mediated Genome Instability. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21145048"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"26198","DOI":"10.1074\/jbc.M803132200","article-title":"The Nucleoside Diphosphate Kinase D (NM23-H4) Binds the Inner Mitochondrial Membrane with High Affinity to Cardiolipin and Couples Nucleotide Transfer with Respiration","volume":"283","author":"Boissan","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1038\/labinvest.2017.102","article-title":"Extracellular NME Proteins: A Player or a Bystander?","volume":"98","author":"Romani","year":"2018","journal-title":"Lab. Investig."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Adam, K., Ning, J., Reina, J., and Hunter, T. (2020). NME\/NM23\/NDPK and Histidine Phosphorylation. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21165848"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1038\/labinvest.2017.125","article-title":"The Actions of NME1\/NDPK-A and NME2\/NDPK-B as Protein Kinases","volume":"98","author":"Attwood","year":"2018","journal-title":"Lab. Investig."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1038\/labinvest.2017.109","article-title":"Nuclear Functions of NME Proteins","volume":"98","author":"Puts","year":"2018","journal-title":"Lab. Investig."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1007\/s00425-020-03355-9","article-title":"A Nucleoside Diphosphate Kinase Gene OsNDPK4 Is Involved in Root Development and Defense Responses in Rice (Oryza sativa L.)","volume":"251","author":"Ye","year":"2020","journal-title":"Planta"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1246","DOI":"10.1093\/pcp\/pci133","article-title":"A Possible Role for NDPK2 in the Regulation of Auxin-Mediated Responses for Plant Growth and Development","volume":"46","author":"Choi","year":"2005","journal-title":"Plant Cell Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1007\/s00425-005-0199-3","article-title":"Characterization of a Cytosolic Nucleoside Diphosphate Kinase Associated with Cell Division and Growth in Potato","volume":"224","author":"Dorion","year":"2006","journal-title":"Planta"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/S0014-5793(01)03069-1","article-title":"Nucleoside Diphosphate Kinase III Is Localized to the Inter-Membrane Space in Plant Mitochondria","volume":"508","author":"Sweetlove","year":"2001","journal-title":"FEBS Lett."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/j.1399-3054.2006.00794.x","article-title":"On the Phylogeny, Expression and Targeting of Plant Nucleoside Diphosphate Kinases","volume":"129","author":"Hammargren","year":"2007","journal-title":"Physiol. Plant."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"L\u00fcttge, U., Beyschlag, W., B\u00fcdel, B., and Francis, D. (2012). Role of Chloroplast Thylakoid Lumen in Photosynthetic Regulation and Plant Cell Signaling. Progress in Botany 73, Springer.","DOI":"10.1007\/978-3-642-22746-2"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e1475804","DOI":"10.1080\/15592324.2018.1475804","article-title":"Plant Nucleoside Diphosphate Kinase 1: A Housekeeping Enzyme with Moonlighting Activity","volume":"13","author":"Dorion","year":"2018","journal-title":"Plant Signal. Behav."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1111\/tpj.13431","article-title":"Engineering the Expression Level of Cytosolic Nucleoside Diphosphate Kinase in Transgenic Solanum tuberosum Roots Alters Growth, Respiration and Carbon Metabolism","volume":"89","author":"Dorion","year":"2017","journal-title":"Plant J."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1073\/pnas.252641899","article-title":"NDP Kinase 2 Interacts with Two Oxidative Stress-Activated MAPKs to Regulate Cellular Redox State and Enhances Multiple Stress Tolerance in Transgenic Plants","volume":"100","author":"Moon","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1038\/44176","article-title":"Phytochrome Signalling Is Mediated Through Nucleoside Diphosphate Kinase 2","volume":"401","author":"Choi","year":"1999","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5740","DOI":"10.1074\/jbc.M408965200","article-title":"NDPK2 as a Signal Transducer in the Phytochrome-Mediated Light Signaling","volume":"280","author":"Shen","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/s00425-014-2161-8","article-title":"Stress Signaling in Response to Polycyclic Aromatic Hydrocarbon Exposure in Arabidopsis thaliana Involves a Nucleoside Diphosphate Kinase, NDPK-3","volume":"241","author":"Liu","year":"2015","journal-title":"Planta"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1104\/pp.113.1.191","article-title":"Cooperation and Competition Between Adenylate Kinase, Nucleoside Diphosphokinase, Electron Transport, and ATP Synthase in Plant Mitochondria Studied by 31P-Nuclear Magnetic Resonance","volume":"113","author":"Roberts","year":"1997","journal-title":"Plant Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1042\/BJ20100026","article-title":"Intermolecular Phosphotransfer Is Crucial for Efficient Catalytic Activity of Nucleoside Diphosphate Kinase","volume":"430","author":"Dar","year":"2010","journal-title":"Biochem. J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3034","DOI":"10.1104\/pp.104.044040","article-title":"Structure and Mutational Analysis of a Plant Mitochondrial Nucleoside Diphosphate Kinase. Identification of Residues Involved in Serine Phosphorylation and Oligomerization","volume":"136","author":"Johansson","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1016\/j.tplants.2018.07.006","article-title":"Whole-Genome Duplication and Plant Macroevolution","volume":"23","author":"Clark","year":"2018","journal-title":"Trends Plant Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1113\/jphysiol.2003.049478","article-title":"Mitochondrial Formation of Reactive Oxygen Species","volume":"552","author":"Turrens","year":"2003","journal-title":"J. Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1042\/BJ20081386","article-title":"How Mitochondria Produce Reactive Oxygen Species","volume":"417","author":"Murphy","year":"2009","journal-title":"Biochem. J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1016\/j.exger.2010.01.003","article-title":"The Sites and Topology of Mitochondrial Superoxide Production","volume":"45","author":"Brand","year":"2010","journal-title":"Exp. Gerontol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0014-5793(97)01159-9","article-title":"High Protonic Potential Actuates a Mechanism of Production of Reactive Oxygen Species in Mitochondria","volume":"416","author":"Korshunov","year":"1997","journal-title":"FEBS Lett."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1146\/annurev.biochem.76.071905.090048","article-title":"The Machines That Divide and Fuse Mitochondria","volume":"76","author":"Hoppins","year":"2007","journal-title":"Annu. Rev. Biochem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/S0021-9258(19)57191-5","article-title":"Respiratory Enzymes in Oxidative Phosphorylation: III. The Steady State","volume":"217","author":"Chance","year":"1955","journal-title":"J. Biol. Chem."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1038\/191144a0","article-title":"Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic Type of Mechanism","volume":"191","author":"Mitchell","year":"1961","journal-title":"Nature"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1111\/j.1432-1033.1980.tb04792.x","article-title":"The Optimal Efficiency and the Economic Degrees of Coupling of Oxidative Phosphorylation","volume":"109","author":"Stucki","year":"1980","journal-title":"Eur. J. Biochem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1111\/j.1432-1033.1980.tb04791.x","article-title":"The Thermodynamic-Buffer Enzymes","volume":"109","author":"Stucki","year":"1980","journal-title":"Eur. J. Biochem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1023\/A:1010671129803","article-title":"Molecular Genetics of Nucleotide Sugar Interconversion Pathways in Plants","volume":"47","author":"Reiter","year":"2001","journal-title":"Plant Mol. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.pbi.2004.03.004","article-title":"Nucleotide Sugar Interconversions and Cell Wall Biosynthesis: How to Bring the inside to the Outside","volume":"7","author":"Seifert","year":"2004","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/BF00194429","article-title":"Sucrose Synthase Catalyses a Readily Reversible Reaction in Vivo in Developing Potato Tubers and Other Plant Tissues","volume":"189","author":"Geigenberger","year":"1993","journal-title":"Planta"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: Multiple Sequence Alignment with High Accuracy and High Throughput","volume":"32","author":"Edgar","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"msae263","DOI":"10.1093\/molbev\/msae263","article-title":"MEGA12: Molecular Evolutionary Genetic Analysis Version 12 for Adaptive and Green Computing","volume":"41","author":"Kumar","year":"2024","journal-title":"Mol. Biol. Evol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"msac174","DOI":"10.1093\/molbev\/msac174","article-title":"TimeTree 5: An Expanded Resource for Species Divergence Times","volume":"39","author":"Kumar","year":"2022","journal-title":"Mol. Biol. Evol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1101\/gr.092759.109","article-title":"Circos: An Information Aesthetic for Comparative Genomics","volume":"19","author":"Rzywinski","year":"2009","journal-title":"Genome Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e49","DOI":"10.1093\/nar\/gkr1293","article-title":"MCScanX: A Toolkit for Detection and Evolutionary Analysis of Gene Synteny and Collinearity","volume":"40","author":"Wang","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"W320","DOI":"10.1093\/nar\/gku316","article-title":"Deciphering Key Features in Protein Structures with the New ENDscript Server","volume":"42","author":"Robert","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"W202","DOI":"10.1093\/nar\/gkp335","article-title":"MEME Suite: Tools for Motif Discovery and Searching","volume":"37","author":"Bailey","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: An efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/0003-9861(82)90507-0","article-title":"Purification of Plant Mitochondria by Isopycnic Centrifugation in Density Gradients of Percoll","volume":"217","author":"Neuburger","year":"1982","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/0014-5793(76)80434-6","article-title":"Safranine as a Probe of the Mitochondrial Membrane Potential","volume":"68","year":"1976","journal-title":"FEBS Lett."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"51944","DOI":"10.1074\/jbc.M408920200","article-title":"Activation and Function of Mitochondrial Uncoupling Protein in Plants","volume":"279","author":"Smith","year":"2004","journal-title":"J. Biol. Chem."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/8\/1156\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,11]],"date-time":"2026-04-11T04:35:56Z","timestamp":1775882156000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/8\/1156"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,9]]},"references-count":58,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,4]]}},"alternative-id":["plants15081156"],"URL":"https:\/\/doi.org\/10.3390\/plants15081156","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,9]]}}}