{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T01:27:46Z","timestamp":1789090066075,"version":"build-2803163510"},"reference-count":64,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2022,4,21]],"date-time":"2022-04-21T00:00:00Z","timestamp":1650499200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["16K18567"],"award-info":[{"award-number":["16K18567"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["17H03782"],"award-info":[{"award-number":["17H03782"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["17H06473"],"award-info":[{"award-number":["17H06473"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["18H02110"],"award-info":[{"award-number":["18H02110"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["18K05373"],"award-info":[{"award-number":["18K05373"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["19H00931"],"award-info":[{"award-number":["19H00931"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["20H05426"],"award-info":[{"award-number":["20H05426"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["20H05501"],"award-info":[{"award-number":["20H05501"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["20H05515"],"award-info":[{"award-number":["20H05515"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["20K05771"],"award-info":[{"award-number":["20K05771"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["21H05150"],"award-info":[{"award-number":["21H05150"]}]},{"name":"Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology","award":["21K19074"],"award-info":[{"award-number":["21K19074"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,6,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Nutrient distribution within the soil is generally heterogeneous. Plants, therefore, have evolved sophisticated systemic processes enabling them to optimize their nutrient acquisition efficiency. By organ-to-organ communication in Arabidopsis thaliana, for instance, iron (Fe) starvation in one part of a root drives the upregulation of a high-affinity Fe-uptake system in other root regions surrounded by sufficient levels of Fe. This compensatory response through Fe-starvation-triggered organ-to-organ communication includes the upregulation of Iron-regulated transporter 1 (IRT1) gene expression on the Fe-sufficient side of the root; however, the molecular basis underlying this long-distance signaling remains unclear. Here, we analyzed gene expression by RNA-seq analysis of Fe-starved split-root cultures. Genome-wide expression analysis showed that localized Fe depletion in roots upregulated several genes involved in Fe uptake and signaling, such as IRT1, in a distant part of the root exposed to Fe-sufficient conditions. This result indicates that long-distance signaling for Fe demand alters the expression of a subset of genes responsible for Fe uptake and coumarin biosynthesis to maintain a level of Fe acquisition sufficient for the entire plant. Loss of IRON MAN\/FE-UPTAKE-INDUCING PEPTIDE (IMA\/FEP) leads to the disruption of compensatory upregulation of IRT1 in the root surrounded by sufficient Fe. In addition, our split-root culture-based analysis provides evidence that the IMA3\/FEP1-MYB10\/72 pathway mediates long-distance signaling in Fe homeostasis through the regulation of coumarin biosynthesis. These data suggest that the signaling of IMA\/FEP, a ubiquitous family of metal-binding peptides, is critical for organ-to-organ communication in response to Fe starvation under heterogeneous Fe conditions in the surrounding environment.<\/jats:p>","DOI":"10.1093\/pcp\/pcac049","type":"journal-article","created":{"date-parts":[[2022,4,20]],"date-time":"2022-04-20T11:16:57Z","timestamp":1650453417000},"page":"842-854","source":"Crossref","is-referenced-by-count":31,"title":["Systemic Regulation of Iron Acquisition by <i>Arabidopsis<\/i> in Environments with Heterogeneous Iron Distributions"],"prefix":"10.1093","volume":"63","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8165-3430","authenticated-orcid":false,"given":"Ryo","family":"Tabata","sequence":"first","affiliation":[{"name":"Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa-ku, Nagoya, 464-8601 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3790-7119","authenticated-orcid":false,"given":"Takehiro","family":"Kamiya","sequence":"additional","affiliation":[{"name":"Graduate School of Agricultural and Life Sciences, The University of Tokyo , Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shunpei","family":"Imoto","sequence":"additional","affiliation":[{"name":"Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa-ku, Nagoya, 464-8601 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hana","family":"Tamura","sequence":"additional","affiliation":[{"name":"Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa-ku, Nagoya, 464-8601 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kumiko","family":"Ikuta","sequence":"additional","affiliation":[{"name":"Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa-ku, Nagoya, 464-8601 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michika","family":"Tabata","sequence":"additional","affiliation":[{"name":"Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa-ku, Nagoya, 464-8601 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tasuku","family":"Hirayama","sequence":"additional","affiliation":[{"name":"Laboratory of Pharmaceutical and Medicinal Chemistry, Gifu Pharmaceutical University , 1-25-4, Daigaku-nishi, Gifu, 501-1196 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hironaka","family":"Tsukagoshi","sequence":"additional","affiliation":[{"name":"Faculty of Agriculture, Meijo University , 1-501 Shiogamaguchi, Tempaku-ku, Nagoya, 468-8502 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keitaro","family":"Tanoi","sequence":"additional","affiliation":[{"name":"Isotope Facility for Agricultural Education and Research, Graduate School of Agricultural and Life Sciences, The University of Tokyo , Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1977-0510","authenticated-orcid":false,"given":"Takamasa","family":"Suzuki","sequence":"additional","affiliation":[{"name":"Department of Biological Chemistry, College of Bioscience and Biotechnology, Chubu University , 1200 Matsumoto-cho, Kasugai, Aichi, 478-8501 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3719-7620","authenticated-orcid":false,"given":"Takushi","family":"Hachiya","sequence":"additional","affiliation":[{"name":"Department of Molecular and Function Genomics, Interdisciplinary Center for Science Research, Shimane University , 1060 Nishikawatsu-cho, Matsue, 690-8504 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5449-6492","authenticated-orcid":false,"given":"Hitoshi","family":"Sakakibara","sequence":"additional","affiliation":[{"name":"Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa-ku, Nagoya, 464-8601 Japan"},{"name":"Center for Sustainable Resource Science, RIKEN , 1-7-22, Suehiro, Tsurumi, Yokohama, 230-0045 Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,4,21]]},"reference":[{"key":"2022061511093986000_R1","doi-asserted-by":"crossref","first-page":"3241","DOI":"10.1007\/s00018-009-0051-1","article-title":"Mammalian iron transport","volume":"66","author":"Anderson","year":"2009","journal-title":"Cell. Mol. Life Sci."},{"key":"2022061511093986000_R2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1100659108","article-title":"Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants","volume":"108","author":"Barberon","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2022061511093986000_R3","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1023\/A:1004375732137","article-title":"Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection","volume":"201","author":"Becana","year":"1998","journal-title":"Plant Soil"},{"key":"2022061511093986000_R4","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1016\/j.bbagen.2009.12.003","article-title":"Ferritins and iron storage in plants","volume":"1800","author":"Briat","year":"2010","journal-title":"Biochim. Biophys. Acta Gen. Subj."},{"key":"2022061511093986000_R5","doi-asserted-by":"crossref","first-page":"3400","DOI":"10.1105\/tpc.104.024315","article-title":"The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response","volume":"16","author":"Colangelo","year":"2004","journal-title":"Plant Cell"},{"key":"2022061511093986000_R6","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1039\/C7MT00136C","article-title":"Iron homeostasis in plants \u2013 a brief overview","volume":"9","author":"Connorton","year":"2017","journal-title":"Metallomics"},{"key":"2022061511093986000_R8","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1093\/nar\/gkq310","article-title":"agriGO: a GO analysis toolkit for the agricultural community","volume":"38","author":"Du","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"2022061511093986000_R9","doi-asserted-by":"crossref","first-page":"5624","DOI":"10.1073\/pnas.93.11.5624","article-title":"A novel iron-regulated metal transporter from plants identified by functional expression in yeast","volume":"93","author":"Eide","year":"1996","journal-title":"Proc. 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Rev. Plant Biol."},{"key":"2022061511093986000_R28","doi-asserted-by":"crossref","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","volume":"10","author":"Langmead","year":"2009","journal-title":"Genome Biol."},{"key":"2022061511093986000_R29","first-page":"1","article-title":"IRON MAN interacts with BRUTUS to maintain iron homeostasis in Arabidopsis","volume":"118","author":"Li","year":"2021","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2022061511093986000_R30","doi-asserted-by":"crossref","first-page":"2219","DOI":"10.1105\/tpc.110.074096","article-title":"The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots","volume":"22","author":"Long","year":"2010","journal-title":"Plant Cell"},{"key":"2022061511093986000_R31","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1104\/pp.87.1.167","article-title":"Characterization of phloem iron and its possible role in the regulation of Fe-efficiency reactions","volume":"87","author":"Maas","year":"1988","journal-title":"Plant Physiol."},{"key":"2022061511093986000_R32","volume-title":"Mineral Nutrition of Higher Plants","author":"Marschner","year":"1995","edition":"2nd"},{"key":"2022061511093986000_R33","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1111\/pce.12143","article-title":"Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability","volume":"37","author":"Mounier","year":"2014","journal-title":"Plant. Cell Environ."},{"key":"2022061511093986000_R34","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1016\/j.jplph.2010.11.020","article-title":"Arabidopsis CYP82C4 expression is dependent on Fe availability and circadian rhythm, and correlates with genes involved in the early Fe deficiency response","volume":"168","author":"Murgia","year":"2011","journal-title":"J. Plant Physiol."},{"key":"2022061511093986000_R35","doi-asserted-by":"crossref","DOI":"10.1038\/nplants.2017.29","article-title":"Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition","volume":"3","author":"Ohkubo","year":"2017","journal-title":"Nat. Plants"},{"key":"2022061511093986000_R36","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms3191","article-title":"Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase","volume":"4","author":"Okamoto","year":"2013","journal-title":"Nat. Commun."},{"key":"2022061511093986000_R37","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.pbi.2016.07.009","article-title":"Long-distance peptide signaling essential for nutrient homeostasis in plants","volume":"34","author":"Okamoto","year":"2016","journal-title":"Curr. Opin. Plant Biol."},{"key":"2022061511093986000_R38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-020-19037-9","article-title":"MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus","volume":"11","author":"Okuma","year":"2020","journal-title":"Nat. Commun."},{"key":"2022061511093986000_R39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-020-14440-8","article-title":"Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis","volume":"11","author":"Ota","year":"2020","journal-title":"Nat. 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Acta Bioenerg."},{"key":"2022061511093986000_R43","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1038\/s41589-018-0019-2","article-title":"Biosynthesis of redox-active metabolites in response to iron deficiency in plants","volume":"14","author":"Rajniak","year":"2018","journal-title":"Nat. Chem. Biol."},{"key":"2022061511093986000_R44","doi-asserted-by":"crossref","first-page":"19206","DOI":"10.1073\/pnas.0605275103","article-title":"The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches","volume":"103","author":"Remans","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. 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Plant Sci."},{"key":"2022061511093986000_R48","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1104\/pp.113.220426","article-title":"Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula","volume":"162","author":"Rodriguez-Celma","year":"2013","journal-title":"Plant Physiol."},{"key":"2022061511093986000_R49","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1111\/j.1399-3054.1987.tb06137.x","article-title":"Different strategies for iron acquisition in higher plants","volume":"70","author":"Romheld","year":"1987","journal-title":"Physiol. 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