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Malate exudation chelates Al3+ in the rhizosphere and confers Al tolerance, yet its transcriptional control in potato remains uncharacterized. Here, StSTOP1\u20133 was identified as a direct activator of the malate transporter gene StALMT10. StALMT10 was root-predominant, encoded a plasma-membrane protein enriched in root tips, and its CRISPR\/Cas9 knockout caused Al3+ hypersensitivity, root-tip Al accumulation, and reduced malate exudation. Among three potato STOP1 paralogs, only StSTOP1\u20133 was rapidly induced by Al3+ and localized to the nucleus. Yeast one-hybrid, dual-luciferase, and DNA pull-down assays confirmed that StSTOP1\u20133 binds the StALMT10 promoter and activates its transcription. StSTOP1\u20133 knockout lines showed an even stronger malate-secretion defect than StALMT10 mutants, implying additional downstream targets. Thus, the StSTOP1\u20133\u2013StALMT10 module confers Al tolerance through root malate secretion, supporting marker-assisted breeding on acidic soils.<\/jats:p>","DOI":"10.1021\/acs.jafc.6c05554","type":"journal-article","created":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T19:01:38Z","timestamp":1790967698000},"page":"31343-31360","source":"Crossref","is-referenced-by-count":0,"title":["The Transcription\nFactor\n                    <i>StStop1\u20133<\/i>\n                    Activates\n                    <i>StALMT10<\/i>\n                    Expression to Enhance Aluminum\nTolerance by Promoting Malate Secretion in Potato (\n                    <i>Solanum tuberosum<\/i>\n                    L.)"],"prefix":"10.1021","volume":"74","author":[{"given":"Feng","family":"Zhang","sequence":"first","affiliation":[{"name":"Moutai Institute , , Luban Street , , ,","place":["Renhuai, Guizhou, P.R. China, 564502"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huaijuan","family":"Gou","sequence":"additional","affiliation":[{"name":"Moutai Institute , , Luban Street , , ,","place":["Renhuai, Guizhou, P.R. China, 564502"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anping","family":"Yuan","sequence":"additional","affiliation":[{"name":"Moutai Institute , , Luban Street , , ,","place":["Renhuai, Guizhou, P.R. China, 564502"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moli","family":"Chu","sequence":"additional","affiliation":[{"name":"Anhui Normal University , , , ,","place":["Wuhu, Anhui, China, 241000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haiyan","family":"Zhang","sequence":"additional","affiliation":[{"name":"Moutai Institute , , Luban Street , , ,","place":["Renhuai, Guizhou, P.R. China, 564502"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6718-6108","authenticated-orcid":true,"given":"Yanlin","family":"An","sequence":"additional","affiliation":[{"name":"Moutai Institute , , Luban Street , , ,","place":["Renhuai, Guizhou, P.R. China, 564502"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,10,2]]},"reference":[{"issue":"1\u20132","key":"2026101408091798000_cit1","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1007\/BF01734046","article-title":"The chemistry of aluminum in the environment","volume":"12","author":"Driscoll","year":"1990","journal-title":"Environ. Geochem. Health"},{"key":"2026101408091798000_cit2","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1016\/S0074-7696(07)64005-4","article-title":"Syndrome\nof aluminum toxicity and diversity of aluminum resistance in higher\nplants","volume":"264","author":"Ma","year":"2007","journal-title":"Int. Rev. Cytol."},{"issue":"1","key":"2026101408091798000_cit3","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1146\/annurev-arplant-043014-114822","article-title":"Plant Adaptation\nto Acid Soils: The Molecular Basis for Crop Aluminum Resistance","volume":"66","author":"Kochian","year":"2015","journal-title":"Annu. Rev. Plant Biol"},{"issue":"3","key":"2026101408091798000_cit4","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1111\/jipb.12162","article-title":"The role of aluminum sensing and\nsignaling in plant aluminum resistance","volume":"56","author":"Liu","year":"2014","journal-title":"J. Integr.\nPlant Biol."},{"issue":"5","key":"2026101408091798000_cit5","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1080\/07388551.2021.1874282","article-title":"Aluminum toxicity and\naluminum stress-induced physiological tolerance responses in higher\nplants","volume":"41","author":"Chauhan","year":"2021","journal-title":"Crit. Rev. Biotechnol."},{"issue":"2","key":"2026101408091798000_cit6","doi-asserted-by":"publisher","first-page":"101200","DOI":"10.1016\/j.xplc.2024.101200","article-title":"Aluminum resistance\nin plants: A critical review focusing on STOP1","volume":"6","author":"Huang","year":"2025","journal-title":"Plant Commun."},{"issue":"6","key":"2026101408091798000_cit7","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/S1360-1385(01)01961-6","article-title":"Aluminium tolerance in plants and\nthe complexing role of organic acids","volume":"6","author":"Ma","year":"2001","journal-title":"Trends\nPlant Sci."},{"issue":"5","key":"2026101408091798000_cit8","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1111\/j.1365-313X.2003.01991.x","article-title":"A wheat\ngene encoding\nan aluminum-activated malate transporter","volume":"37","author":"Sasaki","year":"2004","journal-title":"Plant\nJ."},{"issue":"42","key":"2026101408091798000_cit9","doi-asserted-by":"publisher","first-page":"15249","DOI":"10.1073\/pnas.0406258101","article-title":"Engineering\nhigh-level aluminum tolerance in barley\nwith the ALMT1 gene","volume":"101","author":"Delhaize","year":"2004","journal-title":"Proc. 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Acad. Sci. U. S. A."},{"issue":"3","key":"2026101408091798000_cit13","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1104\/pp.107.102335","article-title":"Characterization of\nAtALMT1 expression in aluminum-inducible malate release and its role\nfor rhizotoxic stress tolerance in Arabidopsis","volume":"145","author":"Kobayashi","year":"2007","journal-title":"Plant Physiol."},{"issue":"1","key":"2026101408091798000_cit14","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1534\/genetics.107.083451","article-title":"An ALMT1\ngene cluster controlling aluminum tolerance at the Alt4 locus of rye\n(Secale cereale L)","volume":"179","author":"Collins","year":"2008","journal-title":"Genetics"},{"issue":"2","key":"2026101408091798000_cit15","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1111\/j.1365-313X.2007.03344.x","article-title":"Not all\nALMT1-type transporters mediate aluminum-activated\norganic acid responses: the case of ZmALMT1 - an anion-selective transporter","volume":"53","author":"Pin\u0303eros","year":"2008","journal-title":"Plant J."},{"issue":"7","key":"2026101408091798000_cit16","doi-asserted-by":"publisher","first-page":"1185","DOI":"10.1111\/j.1365-3040.2011.02479.x","article-title":"Maize ZmALMT2\nis a root anion transporter that mediates constitutive root malate\nefflux","volume":"35","author":"Ligaba","year":"2012","journal-title":"Plant, Cell Environ."},{"issue":"3","key":"2026101408091798000_cit17","doi-asserted-by":"publisher","first-page":"1347","DOI":"10.1104\/pp.112.208934","article-title":"Low pH, aluminum, and phosphorus coordinately regulate malate exudation\nthrough GmALMT1 to improve soybean adaptation to acid soils","volume":"161","author":"Liang","year":"2013","journal-title":"Plant Physiol."},{"issue":"1","key":"2026101408091798000_cit18","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1111\/tpj.12266","article-title":"Adaptation to acidic soil is achieved by increased numbers of cis-acting\nelements regulating ALMT1 expression in Holcus lanatus","volume":"76","author":"Chen","year":"2013","journal-title":"Plant J."},{"issue":"3","key":"2026101408091798000_cit19","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1111\/ppl.12526","article-title":"Malate secretion from\nthe root system is an important reason for higher resistance of Miscanthus\nsacchariflorus to cadmium","volume":"159","author":"Guo","year":"2017","journal-title":"Physiol. Plant"},{"issue":"11","key":"2026101408091798000_cit20","doi-asserted-by":"publisher","first-page":"2367","DOI":"10.1093\/pcp\/pcw157","article-title":"Two Members of the Aluminum-Activated\nMalate Transporter Family, SlALMT4 and SlALMT5, are Expressed during\nFruit Development, and the Overexpression of SlALMT5 Alters Organic\nAcid Contents in Seeds in Tomato (Solanum lycopersicum)","volume":"57","author":"Sasaki","year":"2016","journal-title":"Plant Cell Physiol."},{"issue":"9","key":"2026101408091798000_cit21","doi-asserted-by":"publisher","first-page":"2249","DOI":"10.1105\/tpc.17.00211","article-title":"An InDel in the Promoter\nof Al-ACTIVATED MALATE TRANSPORTER9 Selected during Tomato Domestication\nDetermines Fruit Malate Contents and Aluminum Tolerance","volume":"29","author":"Ye","year":"2017","journal-title":"Plant Cell"},{"key":"2026101408091798000_cit22","doi-asserted-by":"publisher","first-page":"2156","DOI":"10.3389\/fpls.2017.02156","article-title":"BoALMT1, an Al-Induced\nMalate Transporter in Cabbage, Enhances Aluminum Tolerance in Arabidopsis\nthaliana","volume":"8","author":"Zhang","year":"2018","journal-title":"Front. Plant Sci."},{"issue":"1","key":"2026101408091798000_cit23","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1186\/s12870-022-03570-4","article-title":"Tea plant roots respond\nto aluminum-induced mineral nutrient imbalances by transcriptional\nregulation of multiple cation and anion transporters","volume":"22","author":"Hao","year":"2022","journal-title":"BMC Plant Biol."},{"issue":"23","key":"2026101408091798000_cit24","doi-asserted-by":"publisher","first-page":"9900","DOI":"10.1073\/pnas.0700117104","article-title":"Zinc finger\nprotein\nSTOP1 is critical for proton tolerance in Arabidopsis and coregulates\na key gene in aluminum tolerance","volume":"104","author":"Iuchi","year":"2007","journal-title":"Proc. Natl.\nAcad. Sci. U. S. A."},{"issue":"3","key":"2026101408091798000_cit25","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1111\/j.1365-313X.2008.03696.x","article-title":"Aluminum-activated\ncitrate and malate transporters from the MATE and ALMT families function\nindependently to confer Arabidopsis aluminum tolerance","volume":"57","author":"Liu","year":"2009","journal-title":"Plant J."},{"issue":"5","key":"2026101408091798000_cit26","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1111\/tpj.12337","article-title":"WRKY46\nfunctions as a transcriptional repressor of ALMT1, regulating aluminum-induced\nmalate secretion in Arabidopsis","volume":"76","author":"Ding","year":"2013","journal-title":"Plant J."},{"issue":"2","key":"2026101408091798000_cit27","doi-asserted-by":"publisher","first-page":"830","DOI":"10.1111\/nph.14420","article-title":"Loss-of-function mutation of the calcium sensor\nCBL1 increases aluminum sensitivity in Arabidopsis","volume":"214","author":"Ligaba-Osena","year":"2017","journal-title":"New Phytol."},{"key":"2026101408091798000_cit28","doi-asserted-by":"publisher","first-page":"118","DOI":"10.3389\/fpls.2018.00118","article-title":"The Cell\nCycle Checkpoint Regulator ATR Is Required for Internal Aluminum Toxicity-Mediated\nRoot Growth Inhibition in Arabidopsis","volume":"9","author":"Zhang","year":"2018","journal-title":"Front.\nPlant Sci."},{"issue":"19","key":"2026101408091798000_cit29","doi-asserted-by":"publisher","first-page":"5249","DOI":"10.1016\/j.cell.2025.06.034","article-title":"Ancient hybridization underlies tuberization and radiation\nof the potato lineage","volume":"188","author":"Zhang","year":"2025","journal-title":"Cell"},{"key":"2026101408091798000_cit30","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1016\/j.plaphy.2020.06.026","article-title":"Jasmonate and aluminum crosstalk in tomato:\nIdentification and expression analysis of WRKYs and ALMTs during JA\/Al-regulated\nroot growth","volume":"154","author":"Wang","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"2026101408091798000_cit31","doi-asserted-by":"publisher","first-page":"826954","DOI":"10.3389\/fpls.2022.826954","article-title":"The Tomato Transcription\nFactor SlNAC063 Is Required for Aluminum Tolerance by Regulating SlAAE3\u20131\nExpression","volume":"13","author":"Jin","year":"2022","journal-title":"Front. Plant Sci."},{"issue":"2","key":"2026101408091798000_cit32","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1111\/tpj.16054","article-title":"Involvement of SlSTOP1 regulated SlFDH expression\nin aluminum tolerance by reducing NAD+ to NADH in the tomato root\napex","volume":"113","author":"He","year":"2023","journal-title":"Plant J."},{"issue":"4","key":"2026101408091798000_cit33","doi-asserted-by":"publisher","first-page":"2654","DOI":"10.1093\/plphys\/kiae519","article-title":"Transcription factor\nSlSTOP1 regulates Small Auxin-Up RNA Genes for tomato root elongation\nunder aluminum stress","volume":"196","author":"Dong","year":"2024","journal-title":"Plant Physiol."},{"key":"2026101408091798000_cit34","doi-asserted-by":"publisher","first-page":"1274260","DOI":"10.3389\/fpls.2023.1274260","article-title":"Identification of the\nALMT gene family in the potato (Solanum tuberosum L.) and analysis of the function of StALMT6\/10 in response to aluminum\ntoxicity","volume":"14","author":"Zhang","year":"2023","journal-title":"Front. Plant Sci."},{"issue":"11","key":"2026101408091798000_cit35","doi-asserted-by":"publisher","first-page":"uhae282","DOI":"10.1093\/hr\/uhae282","article-title":"SlSTOP1-regulated SlHAK5 expression confers Al tolerance in tomato\nby facilitating citrate secretion from roots","volume":"11","author":"Zhu","year":"2024","journal-title":"Hortic. Res."},{"issue":"W1","key":"2026101408091798000_cit36","doi-asserted-by":"publisher","first-page":"W242","DOI":"10.1093\/nar\/gky354","article-title":"CRISPOR: intuitive\nguide selection for CRISPR\/Cas9\ngenome editing experiments and screens","volume":"46","author":"Concordet","year":"2018","journal-title":"Nucleic\nAcids Res."},{"issue":"4","key":"2026101408091798000_cit37","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1038\/nbt.3804","article-title":"GuideScan software for\nimproved single and paired CRISPR guide RNA design","volume":"35","author":"Perez","year":"2017","journal-title":"Nat. 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Protoc."},{"issue":"7","key":"2026101408091798000_cit47","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1071\/FP08021","article-title":"Arabidopsis thaliana\nMYB75\/PAP1 transcription factor induces anthocyanin production in\ntransgenic tomato plants","volume":"35","author":"Zuluaga","year":"2008","journal-title":"Funct. Plant Biol."},{"issue":"11","key":"2026101408091798000_cit48","doi-asserted-by":"publisher","first-page":"2078","DOI":"10.1111\/pbi.13123","article-title":"RrMYB5- and RrMYB10-regulated flavonoid biosynthesis\nplays a pivotal role in feedback loop responding to wounding and oxidation\nin Rosa rugosa","volume":"17","author":"Shen","year":"2019","journal-title":"Plant Biotechnol. J."},{"issue":"4","key":"2026101408091798000_cit49","doi-asserted-by":"publisher","first-page":"1937","DOI":"10.1104\/pp.113.218958","article-title":"Characterization of AtSTOP1 orthologous\ngenes in tobacco and other plant species","volume":"162","author":"Ohyama","year":"2013","journal-title":"Plant\nPhysiol."},{"issue":"2","key":"2026101408091798000_cit50","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.01720-16","article-title":"Visualizing the Essential\nRole of Complete Virion Assembly Machinery in Efficient Hepatitis\nC Virus Cell-to-Cell Transmission by a Viral Infection-Activated Split-Intein-Mediated\nReporter System","volume":"91","author":"Zhao","year":"2017","journal-title":"J. Virol."},{"issue":"1","key":"2026101408091798000_cit51","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1186\/s12870-021-02975-x","article-title":"Enhanced\naluminum tolerance\nin sugarcane: evaluation of SbMATE overexpression and genome-wide\nidentification of ALMTs in Saccharum spp","volume":"21","author":"Ribeiro","year":"2021","journal-title":"BMC\nPlant Biol."},{"key":"2026101408091798000_cit52","doi-asserted-by":"publisher","first-page":"115791","DOI":"10.1016\/j.ecoenv.2023.115791","article-title":"Aluminum\nphytotoxicity in acidic environments: A comprehensive review of plant\ntolerance and adaptation strategies","volume":"269","author":"Ur Rahman","year":"2024","journal-title":"Ecotoxicol.\nEnviron. Saf."},{"issue":"4","key":"2026101408091798000_cit53","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1111\/ppl.13214","article-title":"The role of solute transporters in\naluminum toxicity and tolerance","volume":"171","author":"Kar","year":"2021","journal-title":"Physiol. 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