{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T12:53:22Z","timestamp":1791982402124,"version":"4.4.0"},"reference-count":40,"publisher":"American Chemical Society (ACS)","issue":"40","license":[{"start":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T00:00:00Z","timestamp":1790640000000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T00:00:00Z","timestamp":1790640000000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T00:00:00Z","timestamp":1790640000000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"funder":[{"DOI":"10.13039\/501100013290","name":"Ministry of Science and Technology of the People's Republic of China","doi-asserted-by":"publisher","award":["2022YFD1400100"],"award-info":[{"award-number":["2022YFD1400100"]}],"id":[{"id":"10.13039\/501100013290","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010038","name":"Ministry of Agriculture of the People's Republic of China","doi-asserted-by":"publisher","award":["CARS-0329"],"award-info":[{"award-number":["CARS-0329"]}],"id":[{"id":"10.13039\/501100010038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,10,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Succinate dehydrogenase (Sdh) is a conserved mitochondrial complex linking the tricarboxylic acid cycle and electron transport chain and is the target of SDHI fungicides. However, the roles of individual Sdh subunits in fungal development and SDHI responses remain unclear. Here, we systematically characterized Sdh subunits in Fusarium verticillioides, the causal agent of maize ear rot. Deletion of FvSdhA, FvSdhB, or FvSdhD severely impaired fungal growth, conidiation, toxin production, pathogenicity, and concurrently reduced sensitivity to the SDHI fungicide pydiflumetofen. In contrast, the duplicated membrane-anchoring subunits FvSdhC1 and FvSdhC2 exhibited partial functional redundancy as deletion of FvSdhC1 led to a dramatic upregulation of FvSdhC2 transcript, and both could potentially support Sdh complex formation, while they exerted distinct effects on virulence and SDHI response. Together, these findings suggest functional specialization within the FvSdh complex and indicate that FvSdhC paralogs may contribute to adaptive fungicide responses through coordinated structural and transcriptional divergence.<\/jats:p>","DOI":"10.1021\/acs.jafc.6c07102","type":"journal-article","created":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T20:03:58Z","timestamp":1790712238000},"page":"31419-31428","source":"Crossref","is-referenced-by-count":0,"title":["Unraveling the Functional Diversity of Succinate Dehydrogenase\nSubunits in\n                    <i>Fusarium verticillioides<\/i>"],"prefix":"10.1021","volume":"74","author":[{"given":"Guiping","family":"Zhang","sequence":"first","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7671-637X","authenticated-orcid":true,"given":"Shuodan","family":"Hu","sequence":"additional","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiaowan","family":"Chen","sequence":"additional","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhankai","family":"Che","sequence":"additional","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongshou","family":"Wu","sequence":"additional","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5663-2352","authenticated-orcid":true,"given":"Yun","family":"Chen","sequence":"additional","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5426-0997","authenticated-orcid":true,"given":"Zhonghua","family":"Ma","sequence":"additional","affiliation":[{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Zhejiang University , , ,","place":["Hangzhou, China, 310058"]},{"name":"Yazhouwan National Laboratory , ,","place":["Sanya, China, 572025"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,9,29]]},"reference":[{"issue":"7","key":"2026101408091758900_cit1","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1016\/j.cell.2005.05.025","article-title":"Crystal structure of mitochondrial\nrespiratory membrane protein complex II","volume":"121","author":"Sun","year":"2005","journal-title":"Cell"},{"key":"2026101408091758900_cit2","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1146\/annurev.biochem.72.121801.161700","article-title":"Function and\nstructure of complex II of the respiratory chain","volume":"72","author":"Cecchini","year":"2003","journal-title":"Annu. Rev. Biochem."},{"issue":"5607","key":"2026101408091758900_cit3","doi-asserted-by":"publisher","first-page":"700","DOI":"10.1126\/science.1079605","article-title":"Architecture of succinate\ndehydrogenase and reactive oxygen species\ngeneration","volume":"299","author":"Yankovskaya","year":"2003","journal-title":"Science"},{"issue":"5","key":"2026101408091758900_cit4","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1038\/sj.ejhg.5200793","article-title":"Succinate\ndehydrogenase and human\ndiseases: New insights into a well\u2013known enzyme","volume":"10","author":"Rustin","year":"2002","journal-title":"Eur. J. Hum. Genet."},{"issue":"4","key":"2026101408091758900_cit5","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1016\/j.tibs.2017.01.003","article-title":"Mitochondrial\ncomplex II: At the crossroads","volume":"42","author":"Bezawork-Geleta","year":"2017","journal-title":"Trends Biochem.\nSci."},{"issue":"9","key":"2026101408091758900_cit6","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1094\/PHYTO-01-13-0009-RVW","article-title":"A review of current knowledge of\nresistance aspects\nfor the next\u2013generation succinate dehydrogenase inhibitor fungicides","volume":"103","author":"Sierotzki","year":"2013","journal-title":"Phytopathology"},{"key":"2026101408091758900_cit7","doi-asserted-by":"publisher","DOI":"10.1016\/j.envint.2023.108219","article-title":"SDHI fungicides: An example of mitotoxic pesticides\ntargeting the succinate dehydrogenase complex","volume":"180","author":"Duarte Hospital","year":"2023","journal-title":"Environ. Int."},{"key":"2026101408091758900_cit8","doi-asserted-by":"publisher","DOI":"10.1016\/j.bmc.2021.116476","article-title":"The research\nprogress\nin and perspective of potential fungicides: Succinate dehydrogenase\ninhibitors","volume":"50","author":"Li","year":"2021","journal-title":"Bioorg. Med. Chem."},{"issue":"7","key":"2026101408091758900_cit9","doi-asserted-by":"publisher","first-page":"2670","DOI":"10.1016\/j.jia.2024.08.017","article-title":"Amino acid\nsubstitutions in succinate dehydrogenase complex conferring resistance\nto the SDHI fungicide pydiflumetofen in Cochliobolus heterostrophus","volume":"24","author":"Sun","year":"2025","journal-title":"J. Integr. Agric."},{"issue":"8","key":"2026101408091758900_cit10","doi-asserted-by":"publisher","first-page":"3694","DOI":"10.1021\/acs.jafc.2c08023","article-title":"Multiple mutations\nin SDHB and SDHC2 subunits confer resistance to the succinate dehydrogenase\ninhibitor cyclobutrifluram in Fusarium fujikuroi","volume":"71","author":"Xue","year":"2023","journal-title":"J. Agric. Food Chem."},{"key":"2026101408091758900_cit11","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2023.103844","article-title":"Polymorphisms\nat amino acid positions 85 and 86 in succinate dehydrogenase subunit\nC of Colletotrichum siamense: Implications for fitness\nand intrinsic sensitivity to SDHI fungicides","volume":"169","author":"Qiu","year":"2023","journal-title":"Fungal Genet. Biol."},{"issue":"9","key":"2026101408091758900_cit12","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a011403","article-title":"Mitochondrial\nevolution","volume":"4","author":"Gray","year":"2012","journal-title":"Cold Spring Harbor Perspect. Biol."},{"key":"2026101408091758900_cit13","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1016\/S0005-2728(01)00238-9","article-title":"Succinate\ndehydrogenase and fumarate reductase from Escherichia coli","volume":"1553","author":"Cecchini","year":"2002","journal-title":"Biochim. Biophys. Acta,\nBioenerg."},{"key":"2026101408091758900_cit14","doi-asserted-by":"publisher","DOI":"10.3390\/biomedicines10081788","article-title":"Succinate dehydrogenase, succinate,\nand superoxides: a genetic, epigenetic, metabolic, environmental explosive\ncrossroad","volume":"10","author":"Be\u0301nit","year":"2022","journal-title":"Biomedicines"},{"key":"2026101408091758900_cit15","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1016\/j.pbi.2013.02.007","article-title":"Succinate dehydrogenase:\nthe complex roles of a simple\nenzyme","volume":"16","author":"Huang","year":"2013","journal-title":"Curr. Opin. Plant Biol."},{"key":"2026101408091758900_cit16","doi-asserted-by":"publisher","DOI":"10.3390\/plants12010068","article-title":"Effect\nof salt stress on the activity, expression, and promoter methylation\nof succinate dehydrogenase and succinic semialdehyde dehydrogenase\nin maize (Zea mays L.) leaves","volume":"12","author":"Fedorin","year":"2023","journal-title":"Plants"},{"key":"2026101408091758900_cit17","doi-asserted-by":"publisher","DOI":"10.1186\/s42483-024-00254-9","article-title":"Functional analysis of all succinate\ndehydrogenase subunits in Fusarium fujikuroi","volume":"6","author":"Fan","year":"2024","journal-title":"Phytopathol. Res."},{"key":"2026101408091758900_cit18","doi-asserted-by":"publisher","first-page":"1780","DOI":"10.1002\/ps.6795","article-title":"Fusarium graminearum FgSdhC1 point mutation A78V confers resistance\nto the succinate\ndehydrogenase inhibitor pydiflumetofen","volume":"78","author":"Shao","year":"2022","journal-title":"Pest\nManage. Sci."},{"key":"2026101408091758900_cit19","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1007780","article-title":"A dispensable paralog of succinate\ndehydrogenase subunit C mediates standing resistance towards a subclass\nof SDHI fungicides in Zymoseptoria tritici","volume":"15","author":"Steinhauer","year":"2019","journal-title":"PLoS Pathog."},{"key":"2026101408091758900_cit20","doi-asserted-by":"publisher","first-page":"1640","DOI":"10.1094\/Phyto-77-1640","article-title":"Nitrate non\u2013utilizing\nmutants\nof Fusarium oxysporum and their use in vegetative\ncompatibility tests","volume":"77","author":"Correll","year":"1987","journal-title":"Phytopathology"},{"key":"2026101408091758900_cit21","doi-asserted-by":"publisher","first-page":"1844","DOI":"10.1002\/ps.4216","article-title":"Efficacy of\nSDHI fungicides, including benzovindiflupyr, against Colletotrichum species","volume":"72","author":"Ishii","year":"2016","journal-title":"Pest Manage. Sci."},{"key":"2026101408091758900_cit22","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis\nof relative gene expression data using real\u2013time\nquantitative PCR and the 2-\u0394\u0394Ct method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"2026101408091758900_cit23","doi-asserted-by":"publisher","first-page":"2023","DOI":"10.1111\/1462-2920.12334","article-title":"The MAPKK\nFgMkk1 of Fusarium graminearum regulates vegetative\ndifferentiation, multiple stress response, and virulence via the cell\nwall integrity and high\u2013osmolarity glycerol signaling pathways","volume":"16","author":"Yun","year":"2014","journal-title":"Environ. Microbiol."},{"key":"2026101408091758900_cit24","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1094\/MPMI-8-0593","article-title":"Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic\ngene","volume":"8","author":"Proctor","year":"1995","journal-title":"Mol. Plant-Microbe Interact."},{"key":"2026101408091758900_cit25","doi-asserted-by":"publisher","DOI":"10.3390\/toxins9020043","article-title":"Involvement of FvSet1\nin Fumonisin B1 biosynthesis, vegetative growth, fungal\nvirulence, and environmental stress responses in Fusarium verticillioides","volume":"9","author":"Gu","year":"2017","journal-title":"Toxins"},{"key":"2026101408091758900_cit26","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.pmpp.2017.07.003","article-title":"Fumonisin B1 produced in planta by Fusarium verticillioides is associated with inhibition of maize \u03b2-1,3-glucanase\nactivity and increased aggressiveness","volume":"100","author":"Galeana-Sa\u0301nchez","year":"2017","journal-title":"Physiol.\nMol. Plant Pathol."},{"key":"2026101408091758900_cit27","doi-asserted-by":"publisher","first-page":"25848","DOI":"10.1021\/acs.jafc.5c07082","article-title":"Resistance evolution\nand fitness of Fusarium asiaticum from fields to\nsuccinate dehydrogenase inhibitor pydiflumetofen\nin China","volume":"73","author":"Yuan","year":"2025","journal-title":"J. Agric. Food Chem."},{"key":"2026101408091758900_cit28","doi-asserted-by":"publisher","first-page":"7039","DOI":"10.1021\/acs.jafc.2c02056","article-title":"Molecular mechanism\nof Sclerotinia sclerotiorum resistance\nto succinate dehydrogenase inhibitor fungicides","volume":"70","author":"Wang","year":"2022","journal-title":"J. Agric. Food Chem."},{"key":"2026101408091758900_cit29","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1021\/bi501350j","article-title":"Redox state of flavin adenine dinucleotide\ndrives substrate binding and product release in Escherichia coli succinate dehydrogenase","volume":"54","author":"Cheng","year":"2015","journal-title":"Biochemistry"},{"key":"2026101408091758900_cit30","doi-asserted-by":"publisher","first-page":"168","DOI":"10.3109\/10409238.2014.990556","article-title":"Protein-mediated\nassembly of succinate dehydrogenase and its cofactors","volume":"50","author":"Van Vranken","year":"2015","journal-title":"Crit. Rev. Biochem. Mol. Biol."},{"key":"2026101408091758900_cit31","doi-asserted-by":"publisher","DOI":"10.3389\/fchem.2017.00100","article-title":"Discovering novel Alternaria solani succinate dehydrogenase inhibitors by\nin silico modeling and virtual screening strategies to combat early\nblight","volume":"5","author":"Iftikhar","year":"2017","journal-title":"Front. Chem."},{"issue":"51","key":"2026101408091758900_cit32","doi-asserted-by":"publisher","first-page":"20643","DOI":"10.1021\/acs.jafc.3c06288","article-title":"FgSdhC paralog\nconfers natural resistance\ntoward SDHI fungicides in Fusarium graminearum","volume":"71","author":"Sun","year":"2023","journal-title":"J. Agric. Food Chem."},{"key":"2026101408091758900_cit33","doi-asserted-by":"publisher","first-page":"13006","DOI":"10.1021\/acs.jafc.1c04363","article-title":"Point mutations\nin FgSdhC2 or in\nthe 5\u2032 untranslated region of FgSdhC1 confer resistance to\na novel succinate dehydrogenase inhibitor flubeneteram in Fusarium graminearum","volume":"69","author":"Chen","year":"2021","journal-title":"J. Agric. Food\nChem."},{"key":"2026101408091758900_cit34","doi-asserted-by":"publisher","first-page":"14911","DOI":"10.1021\/acs.jafc.6c00040","article-title":"Succinate\ndehydrogenase subunits differentially regulate physiology,\nSDHI sensitivity, and DON biosynthesis in Fusarium pseudograminearum","volume":"74","author":"Li","year":"2026","journal-title":"J. Agric. Food Chem."},{"issue":"18","key":"2026101408091758900_cit35","doi-asserted-by":"publisher","first-page":"10314","DOI":"10.1021\/acs.jafc.4c02179","article-title":"Functional\ndifferentiation of the succinate dehydrogenase subunit\nSdhC governs the sensitivity to SDHI fungicides, ROS homeostasis,\nand pathogenicity in Fusarium asiaticum","volume":"72","author":"Chen","year":"2024","journal-title":"J.\nAgric. Food Chem."},{"key":"2026101408091758900_cit36","doi-asserted-by":"publisher","DOI":"10.1016\/j.jafr.2024.101587","article-title":"Succinate\ndehydrogenase governs the sensitivity to SDHI fungicides and fruit\npathogenicity of Colletotrichum gloeosporioides","volume":"19","author":"Zhang","year":"2025","journal-title":"J. Agric. Food Res."},{"issue":"44","key":"2026101408091758900_cit37","doi-asserted-by":"publisher","first-page":"28117","DOI":"10.1021\/acs.jafc.5c09818","article-title":"A83V mutation in FaSDHC2 confers\nhigh field resistance to pydiflumetofen and exhibits negative cross\u2013resistance\nto benzovindiflupyr in Fusarium asiaticum","volume":"73","author":"Li","year":"2025","journal-title":"J.\nAgric. Food Chem."},{"key":"2026101408091758900_cit38","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijbiomac.2024.139360","article-title":"The resistance\nmechanism of B_P225F and B_H272R mutations\nin succinate dehydrogenase in Botrytis cinerea","volume":"293","author":"Ma","year":"2025","journal-title":"Int. J. Biol. Macromol."},{"issue":"9","key":"2026101408091758900_cit39","doi-asserted-by":"publisher","first-page":"2723","DOI":"10.1007\/s11427-024-2899-1","article-title":"Phase separation\nof a master transcription factor targeted by a natural compound regulates\nfungal ergosterol homeostasis","volume":"68","author":"Wang","year":"2025","journal-title":"Sci. China Life\nSci."},{"issue":"1","key":"2026101408091758900_cit40","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-09145-6","article-title":"A phosphorylated transcription factor regulates sterol\nbiosynthesis in Fusarium graminearum","volume":"10","author":"Liu","year":"2019","journal-title":"Nat. Commun."}],"container-title":["Journal of Agricultural and Food Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jafc.6c07102","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/40\/31419\/68703253\/acs.jafc.6c07102.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/40\/31419\/68703253\/acs.jafc.6c07102.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T12:29:51Z","timestamp":1791980991000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jafcau\/article\/74\/40\/31419\/5441864\/Unraveling-the-Functional-Diversity-of-Succinate"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,29]]},"references-count":40,"journal-issue":{"issue":"40","published-online":{"date-parts":[[2026,9,29]]},"published-print":{"date-parts":[[2026,10,14]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jafc.6c07102","relation":{},"ISSN":["0021-8561","1520-5118"],"issn-type":[{"value":"0021-8561","type":"print"},{"value":"1520-5118","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,29]]}}}