{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,20]],"date-time":"2026-01-20T03:42:36Z","timestamp":1768880556938,"version":"3.49.0"},"reference-count":37,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T00:00:00Z","timestamp":1759881600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"name":"Environmental Radioactivity Research Network Center","award":["Y-22-27"],"award-info":[{"award-number":["Y-22-27"]}]},{"DOI":"10.13039\/501100002241","name":"Japan Science and Technology Agency","doi-asserted-by":"publisher","award":["JPMJFS2129"],"award-info":[{"award-number":["JPMJFS2129"]}],"id":[{"id":"10.13039\/501100002241","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science KAKENHI","doi-asserted-by":"crossref","award":["JP22H02230"],"award-info":[{"award-number":["JP22H02230"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science KAKENHI","doi-asserted-by":"crossref","award":["JP21H04717"],"award-info":[{"award-number":["JP21H04717"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,1,19]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Several plant species adapted to low-phosphorus (P) conditions develop cluster roots, specialized structures that release organic acids and acid phosphatases (APases) to increase inorganic phosphate (Pi) availability. White lupin (Lupinus albus L.) is used as a model for studying cluster root function. Using a positron-emitting tracer imaging system (PETIS), we previously observed spot-like carbon (C) secretion patterns in the cluster roots of white lupin, the amounts of which differed widely among spots, suggesting variation in secretion activity among cluster roots. Here, we combined PETIS with RNA-Seq to investigate transcriptomic differences between cluster roots with varying secretion activities. We identified 564 genes positively correlated and 135 genes negatively correlated with secretion levels. Among the positively correlated genes, we found three aluminum-activated malate transporter genes and two multidrug and toxic compound extrusion genes, likely involved respectively in malate and citrate secretion. Two APase genes encoding putative secreted enzymes were also upregulated. All Pi transporter genes except PHO1;6H were stably expressed, whereas PHO1;6H was significantly upregulated in high-C-secreting roots. Our findings highlight putative genes potentially involved in Pi mobilization, offering insights into plant adaptation to P deficiency.<\/jats:p>","DOI":"10.1093\/pcp\/pcaf127","type":"journal-article","created":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T11:41:57Z","timestamp":1759837317000},"page":"30-38","source":"Crossref","is-referenced-by-count":0,"title":["Genome-wide identification of genes associated with enhanced carbon secretion in cluster roots of\n                    <i>Lupinus albus<\/i>\n                    L"],"prefix":"10.1093","volume":"67","author":[{"given":"Kiyotoshi","family":"Hanashiro","sequence":"first","affiliation":[{"name":"Faculty of Agriculture, Saga University , 1 Honjo-machi, Saga 840-8502 ,","place":["Japan"]},{"name":"Graduate School of Integrated Sciences for Life, Hiroshima University , 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8157-4636","authenticated-orcid":false,"given":"Sho","family":"Nishida","sequence":"additional","affiliation":[{"name":"Faculty of Agriculture, Saga University , 1 Honjo-machi, Saga 840-8502 ,","place":["Japan"]},{"name":"The United Graduate School of Agricultural Sciences, Kagoshima University , 1-21-24 Korimoto, Kagoshima 890-0065 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2981-7041","authenticated-orcid":false,"given":"Takuo","family":"Enomoto","sequence":"additional","affiliation":[{"name":"Faculty of Agriculture, Saga University , 1 Honjo-machi, Saga 840-8502 ,","place":["Japan"]},{"name":"Institute of Fruit Tree and Tea Science, Division of Tea Research, National Agriculture and Food Research Organization , 2769 Kanaya-Shishidoi, Shimada 428-8501 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yong-Gen","family":"Yin","sequence":"additional","affiliation":[{"name":"Takasaki Institute for Advanced Quantum Science, National Institutes for Quantum Science and Technology (QST) , 1233 Watanuki-machi, Takasaki 370-1292 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1081-7578","authenticated-orcid":false,"given":"Nobuo","family":"Suzui","sequence":"additional","affiliation":[{"name":"Takasaki Institute for Advanced Quantum Science, National Institutes for Quantum Science and Technology (QST) , 1233 Watanuki-machi, Takasaki 370-1292 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuta","family":"Miyoshi","sequence":"additional","affiliation":[{"name":"Takasaki Institute for Advanced Quantum Science, National Institutes for Quantum Science and Technology (QST) , 1233 Watanuki-machi, Takasaki 370-1292 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yusaku","family":"Noda","sequence":"additional","affiliation":[{"name":"Takasaki Institute for Advanced Quantum Science, National Institutes for Quantum Science and Technology (QST) , 1233 Watanuki-machi, Takasaki 370-1292 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kazuyuki","family":"Enomoto","sequence":"additional","affiliation":[{"name":"Takasaki Institute for Advanced Quantum Science, National Institutes for Quantum Science and Technology (QST) , 1233 Watanuki-machi, Takasaki 370-1292 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3991-5035","authenticated-orcid":false,"given":"Naoki","family":"Kawachi","sequence":"additional","affiliation":[{"name":"Takasaki Institute for Advanced Quantum Science, National Institutes for Quantum Science and Technology (QST) , 1233 Watanuki-machi, Takasaki 370-1292 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yusuke","family":"Unno","sequence":"additional","affiliation":[{"name":"Institute for Environmental Sciences , Department of Radioecology, 1-7 Ienomae, Obuchi, Rokkasho-mura, Kamikita-gun 039-3212 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hayato","family":"Maruyama","sequence":"additional","affiliation":[{"name":"Research Faculty of Agriculture, Hokkaido University , Kita-9, Nishi-9, Kita-ku, Sapporo 060-8589 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Akiko","family":"Maruo","sequence":"additional","affiliation":[{"name":"Research Faculty of Agriculture, Hokkaido University , Kita-9, Nishi-9, Kita-ku, Sapporo 060-8589 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ayane","family":"Kan","sequence":"additional","affiliation":[{"name":"Research Faculty of Agriculture, Hokkaido University , Kita-9, Nishi-9, Kita-ku, Sapporo 060-8589 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takuro","family":"Shinano","sequence":"additional","affiliation":[{"name":"Research Faculty of Agriculture, Hokkaido University , Kita-9, Nishi-9, Kita-ku, Sapporo 060-8589 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8344-607X","authenticated-orcid":false,"given":"Jun","family":"Wasaki","sequence":"additional","affiliation":[{"name":"Graduate School of Integrated Sciences for Life, Hiroshima University , 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521 ,","place":["Japan"]},{"name":"Seto Inland Sea Carbon Neutral Research Center, Hiroshima University , 1-7-1 Kagamiyama, Higashi-Hiroshima 739-8521 ,","place":["Japan"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2025,10,8]]},"reference":[{"key":"2026011910065332200_ref1","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1038\/s41477-024-01895-6","article-title":"Structural mechanism underlying PHO1; H1-mediated phosphate transport in Arabidopsis","volume":"11","author":"Fang","year":"2025","journal-title":"Nat Plants"},{"key":"2026011910065332200_ref2","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1093\/pcp\/pcm091","article-title":"An aluminum-activated citrate transporter in barley","volume":"48","author":"Furukawa","year":"2007","journal-title":"Plant Cell Physiol."},{"key":"2026011910065332200_ref3","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1023\/A:1013351617532","article-title":"Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review","volume":"237","author":"Hinsinger","year":"2001","journal-title":"Plant Soil"},{"key":"2026011910065332200_ref4","doi-asserted-by":"crossref","first-page":"9738","DOI":"10.1073\/pnas.0602868103","article-title":"AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis","volume":"103","author":"Hoekenga","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2026011910065332200_ref5","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/s40538-023-00401-y","article-title":"Biotic and abiotic effects of soil organic matter on the phytoavailable phosphorus in soils: a review","volume":"10","author":"Jindo","year":"2023","journal-title":"Chem. Biol. Technol. Agric."},{"key":"2026011910065332200_ref6","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1080\/00380768.2021.1988829","article-title":"Comparative study of radioactive cesium transfer from soil to peanut and soybean","volume":"67","author":"Kubo","year":"2021","journal-title":"Soil Sci. Plant Nutr."},{"key":"2026011910065332200_ref7","doi-asserted-by":"crossref","first-page":"738172","DOI":"10.3389\/fpls.2021.738172","article-title":"Dynamic development of white lupin rootlets along a cluster root","volume":"12","author":"Le Thanh","year":"2021","journal-title":"Front. Plant Sci."},{"key":"2026011910065332200_ref8","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1111\/j.1365-313X.2008.03696.x","article-title":"Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance","volume":"57","author":"Liu","year":"2009","journal-title":"Plant J."},{"key":"2026011910065332200_ref9","doi-asserted-by":"crossref","first-page":"937940","DOI":"10.3389\/fmicb.2022.937940","article-title":"Root exudates contribute to belowground ecosystem hotspots: a review","volume":"13","author":"Ma","year":"2022","journal-title":"Front. Microbiol."},{"key":"2026011910065332200_ref10","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1038\/ng2074","article-title":"A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum","volume":"39","author":"Magalhaes","year":"2007","journal-title":"Nat. Genet."},{"key":"2026011910065332200_ref11","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1111\/j.1365-313X.2009.04103.x","article-title":"Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize","volume":"61","author":"Maron","year":"2010","journal-title":"Plant J."},{"key":"2026011910065332200_ref12","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1093\/pcp\/pcy190","article-title":"AtALMT3 is involved in malate efflux induced by phosphorus deficiency in Arabidopsis thaliana root hairs","volume":"60","author":"Maruyama","year":"2019","journal-title":"Plant Cell Physiol."},{"key":"2026011910065332200_ref13","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1104\/pp.010097","article-title":"Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin","volume":"127","author":"Miller","year":"2001","journal-title":"Plant Physiol."},{"key":"2026011910065332200_ref14","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/s004250050572","article-title":"Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin","volume":"208","author":"Neumann","year":"1999","journal-title":"Planta"},{"key":"2026011910065332200_ref15","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1093\/pcp\/pcr089","article-title":"AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana","volume":"52","author":"Nishida","year":"2011","journal-title":"Plant Cell Physiol."},{"key":"2026011910065332200_ref16","doi-asserted-by":"crossref","first-page":"329","DOI":"10.4161\/psb.19263","article-title":"Induction of IRT1 by the nickel-induced iron-deficient response in Arabidopsis","volume":"7","author":"Nishida","year":"2012","journal-title":"Plant Signal. 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The case of wild populations in central Italy","volume":"145","author":"Scoppola","year":"2011","journal-title":"Plant Biosyst."},{"key":"2026011910065332200_ref20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-15-230","article-title":"RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin","volume":"15","author":"Secco","year":"2014","journal-title":"BMC Genomics"},{"key":"2026011910065332200_ref21","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1093\/jexbot\/52.suppl_1.479","article-title":"Cluster roots: model experimental tools for key biological problems","volume":"52","author":"Skene","year":"2001","journal-title":"J. Exp. Bot."},{"key":"2026011910065332200_ref22","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1080\/00380768.1991.10415018","article-title":"Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions","volume":"37","author":"Tadano","year":"1991","journal-title":"Soil Sci. Plant Nutr."},{"key":"2026011910065332200_ref23","doi-asserted-by":"crossref","first-page":"1282","DOI":"10.1104\/pp.106.087171","article-title":"Biochemical and molecular characterization of AtPAP26, a vacuolar purple acid phosphatase up-regulated in phosphate-deprived Arabidopsis suspension cells and seedlings","volume":"142","author":"Veljanovski","year":"2006","journal-title":"Plant Physiol."},{"key":"2026011910065332200_ref24","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1111\/ppl.12187","article-title":"The regulatory network of cluster-root function and development in phosphate-deficient white lupin (Lupinus albus) identified by transcriptome sequencing","volume":"151","author":"Wang","year":"2014","journal-title":"Physiol. Plant."},{"key":"2026011910065332200_ref25","first-page":"865","article-title":"Vigorous root growth is a better indicator of early nutrient uptake than root hair traits in spring wheat grown under low fertility","volume":"7","author":"Wang","year":"2016","journal-title":"Front. Plant Sci."},{"key":"2026011910065332200_ref26","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1080\/00380768.1999.10409358","article-title":"Structure of a cDNA for an acid phosphatase from phosphate-deficient lupin (Lupinus albus L.) roots","volume":"45","author":"Wasaki","year":"1999","journal-title":"Soil Sci. Plant Nutr."},{"key":"2026011910065332200_ref27","first-page":"427","article-title":"Molecular cloning and root specific expression of secretory acid phosphatase from phosphate deficient lupin (Lupinus albus L.)","volume":"46","author":"Wasaki","year":"2000","journal-title":"Soil Sci. Plant Nutr."},{"key":"2026011910065332200_ref28","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1023\/A:1022332320384","article-title":"Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency","volume":"248","author":"Wasaki","year":"2003","journal-title":"Plant Soil"},{"key":"2026011910065332200_ref29","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1104\/pp.120.3.705","article-title":"Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration","volume":"120","author":"Watt","year":"1999","journal-title":"Plant Physiol."},{"key":"2026011910065332200_ref30","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1111\/j.1469-8137.2006.01776.x","article-title":"Isoflavonoid exudation from white lupin roots is influenced by phosphate supply, root type and cluster-root stage","volume":"171","author":"Weisskopf","year":"2006","journal-title":"New Phytol."},{"key":"2026011910065332200_ref31","doi-asserted-by":"crossref","first-page":"eabf2017","DOI":"10.1126\/sciadv.abf2017","article-title":"ETS1 acts as a regulator of human healthy aging via decreasing ribosomal activity","volume":"8","author":"Xiao","year":"2022","journal-title":"Sci. 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Plant Nutr."},{"key":"2026011910065332200_ref33","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1111\/nph.70010","article-title":"HalALMT1 mediates malate efflux in the cortex of mature cluster rootlets of Hakea laurina, occurring naturally in severely phosphorus-impoverished soil","volume":"246","author":"Yamada","year":"2025","journal-title":"New Phytol."},{"key":"2026011910065332200_ref34","doi-asserted-by":"crossref","first-page":"8446","DOI":"10.1038\/s41598-020-65668-9","article-title":"Visualising spatio-temporal distributions of assimilated carbon translocation and release in root systems of leguminous plants","volume":"10","author":"Yin","year":"2020","journal-title":"Sci. Rep."},{"key":"2026011910065332200_ref35","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1111\/j.1365-313X.2011.04757.x","article-title":"An Al-inducible MATE gene is involved in external detoxification of Al in rice","volume":"68","author":"Yokosho","year":"2011","journal-title":"Plant J."},{"key":"2026011910065332200_ref36","doi-asserted-by":"crossref","first-page":"1691","DOI":"10.1111\/pce.13762","article-title":"LaALMT1 mediates malate release from phosphorus-deficient white lupin root tips and metal root to shoot translocation","volume":"43","author":"Zhou","year":"2020","journal-title":"Plant Cell Environ."},{"key":"2026011910065332200_ref37","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1111\/ppl.13515","article-title":"Loss of LaMATE impairs isoflavonoid release from cluster roots of phosphorus-deficient white lupin","volume":"173","author":"Zhou","year":"2021","journal-title":"Physiol. Plant."}],"container-title":["Plant and Cell Physiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/pcp\/advance-article-pdf\/doi\/10.1093\/pcp\/pcaf127\/64549561\/pcaf127.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/pcp\/article-pdf\/67\/1\/30\/64549561\/pcaf127.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/pcp\/article-pdf\/67\/1\/30\/64549561\/pcaf127.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,19]],"date-time":"2026-01-19T15:07:02Z","timestamp":1768835222000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/pcp\/article\/67\/1\/30\/8277636"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,8]]},"references-count":37,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,10,8]]},"published-print":{"date-parts":[[2026,1,19]]}},"URL":"https:\/\/doi.org\/10.1093\/pcp\/pcaf127","relation":{},"ISSN":["0032-0781","1471-9053"],"issn-type":[{"value":"0032-0781","type":"print"},{"value":"1471-9053","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026,1]]},"published":{"date-parts":[[2025,10,8]]}}}