{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T01:56:30Z","timestamp":1791338190463,"version":"4.3.1"},"reference-count":46,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2021,9,27]],"date-time":"2021-09-27T00:00:00Z","timestamp":1632700800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100003086","name":"Basque Government","doi-asserted-by":"publisher","award":["IT932-16"],"award-info":[{"award-number":["IT932-16"]}],"id":[{"id":"10.13039\/501100003086","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Spanish Ministry of Economy and Competitiveness","award":["BIO2017-84035-R"],"award-info":[{"award-number":["BIO2017-84035-R"]}]},{"name":"Spanish Ministry of Economy and Competitiveness","award":["PID2020-113385RB-I00"],"award-info":[{"award-number":["PID2020-113385RB-I00"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,1,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Most plant species develop stress symptoms when exposed to high ammonium (NH4+) concentrations. The root is the first organ in contact with high NH4+ and therefore the first barrier to cope with ammonium stress. In this work, we focused on root adaptation to ammonium nutrition in the model plant Brachypodium distachyon. Proteome analysis revealed changes associated with primary metabolism, cell wall remodelling, and redox homeostasis. In addition, it showed a strong induction of proteins related to methionine (Met) metabolism and phytosiderophore (PS) synthesis in ammonium-fed plants. In agreement with this, we show how ammonium nutrition impacts Met\/S-adenosyl-Met and PS metabolic pathways together with increasing root iron content. Nevertheless, ammonium-fed plants displayed higher sensitivity to iron deficiency, suggesting that ammonium nutrition triggers impaired iron utilization and root to shoot transport, which entailed an induction in iron-related responses. Overall, this work demonstrates the importance of iron homeostasis during ammonium nutrition and paves a new way to better understand and improve ammonium use efficiency and tolerance.<\/jats:p>","DOI":"10.1093\/jxb\/erab427","type":"journal-article","created":{"date-parts":[[2021,9,16]],"date-time":"2021-09-16T19:16:36Z","timestamp":1631819796000},"page":"263-274","source":"Crossref","is-referenced-by-count":19,"title":["Ammonium nutrition interacts with iron homeostasis in <i>Brachypodium distachyon<\/i>"],"prefix":"10.1093","volume":"73","author":[{"given":"Marlon","family":"De la Pe\u00f1a","sequence":"first","affiliation":[{"name":"Department of Plant Biology and Ecology, University of the Basque Country (UPV\/EHU), E-48940, Leioa,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agust\u00edn Javier","family":"Mar\u00edn-Pe\u00f1a","sequence":"additional","affiliation":[{"name":"Department of Plant Biology and Ecology, University of the Basque Country (UPV\/EHU), E-48940, Leioa,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leyre","family":"Urmeneta","sequence":"additional","affiliation":[{"name":"Department of Plant Biology and Ecology, University of the Basque Country (UPV\/EHU), E-48940, Leioa,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Inmaculada","family":"Coleto","sequence":"additional","affiliation":[{"name":"Department of Plant Biology and Ecology, University of the Basque Country (UPV\/EHU), E-48940, Leioa,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jorge","family":"Castillo-Gonz\u00e1lez","sequence":"additional","affiliation":[{"name":"Department of Plant Nutrition, Aula Dei Experimental Station, Consejo Superior de Investigaciones Cient\u00edficas (EEAD-CSIC), E-50059, Zaragoza,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sebastiaan M","family":"van Liempd","sequence":"additional","affiliation":[{"name":"Metabolomics Platform, CIC bioGUNE-BRTA, Derio,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan M","family":"Falc\u00f3n-P\u00e9rez","sequence":"additional","affiliation":[{"name":"Metabolomics Platform, CIC bioGUNE-BRTA, Derio,Spain"},{"name":"Centro de Investigaci\u00f3n Biom\u00e9dica en Red de enfermedades hep\u00e1ticas y digestivas (CIBERehd), Madrid,Spain"},{"name":"Ikerbasque, Basque Foundation for Science, E-48011 Bilbao,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"\u00c1lvarez-Fern\u00e1ndez","sequence":"additional","affiliation":[{"name":"Department of Plant Nutrition, Aula Dei Experimental Station, Consejo Superior de Investigaciones Cient\u00edficas (EEAD-CSIC), E-50059, Zaragoza,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar\u00eda Bego\u00f1a","family":"Gonz\u00e1lez-Moro","sequence":"additional","affiliation":[{"name":"Department of Plant Biology and Ecology, University of the Basque Country (UPV\/EHU), E-48940, Leioa,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8788-6646","authenticated-orcid":false,"given":"Daniel","family":"Marino","sequence":"additional","affiliation":[{"name":"Department of Plant Biology and Ecology, University of the Basque Country (UPV\/EHU), E-48940, Leioa,Spain"},{"name":"Ikerbasque, Basque Foundation for Science, E-48011 Bilbao,Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,9,27]]},"reference":[{"key":"2022010519395368100_CIT0001","doi-asserted-by":"crossref","first-page":"1575","DOI":"10.1080\/01904169009364176","article-title":"Mineral nutrition of chickpea plants supplied with NO3","volume":"13","author":"Alloush","year":"1990","journal-title":"Journal of Plant Nutrition"},{"key":"2022010519395368100_CIT0002","first-page":"23","article-title":"Optimization of ammonium acquisition and metabolism by potassium in rice (Oryza sativa L. cv. IR-72)","volume":"33","author":"Balkos","year":"2010","journal-title":"Plant, Cell & Environment"},{"key":"2022010519395368100_CIT0003","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.copbio.2018.01.014","article-title":"Nitrification in agricultural soils: impact, actors and mitigation","volume":"50","author":"Beeckman","year":"2018","journal-title":"Current Opinion in Biotechnology"},{"key":"2022010519395368100_CIT0004","doi-asserted-by":"crossref","first-page":"1879532","DOI":"10.1080\/15592324.2021.1879532","article-title":"Arabidopsis MYB28 and MYB29 transcription factors are involved in ammonium-mediated alterations of root-system architecture","volume":"16","author":"Bejarano","year":"2021","journal-title":"Plant Signaling & Behavior"},{"key":"2022010519395368100_CIT0005","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1016\/j.tplants.2019.03.008","article-title":"Getting to the root of plant mineral nutrition: combinatorial nutrient stresses reveal emergent properties","volume":"24","author":"Bouain","year":"2019","journal-title":"Trends in Plant Science"},{"key":"2022010519395368100_CIT0006","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.tplants.2014.07.005","article-title":"Iron nutrition, biomass production, and plant product quality","volume":"20","author":"Briat","year":"2015","journal-title":"Trends in Plant Science"},{"key":"2022010519395368100_CIT0007","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1078\/0176-1617-0774","article-title":"NH4+ toxicity in higher plants: a critical review","volume":"584","author":"Britto","year":"2002","journal-title":"Journal of Plant Physiology"},{"key":"2022010519395368100_CIT0008","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1007\/978-94-011-0878-2_10","article-title":"Zinc phytotoxicity","volume-title":"Zinc in soils and plants","author":"Chaney","year":"1993"},{"key":"2022010519395368100_CIT0009","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1111\/nph.16918","article-title":"Arabidopsis thaliana transcription factors MYB28 and MYB29 shape ammonium stress responses by regulating Fe homeostasis","volume":"229","author":"Coleto","year":"2021","journal-title":"New Phytologist"},{"key":"2022010519395368100_CIT0010","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12870-017-1100-9","article-title":"Leaves play a central role in the adaptation of nitrogen and sulfur metabolism to ammonium nutrition in oilseed rape (Brassica napus)","volume":"17","author":"Coleto","year":"2017","journal-title":"BMC Plant Biology"},{"key":"2022010519395368100_CIT0011","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/ppl.12174","article-title":"The physiology of channel-mediated K+ acquisition in roots of higher plants","volume":"151","author":"Coskun","year":"2014","journal-title":"Physiologia Plantarum"},{"key":"2022010519395368100_CIT0012","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1038\/nbt.1511","article-title":"MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification","volume":"26","author":"Cox","year":"2008","journal-title":"Nature Biotechnology"},{"key":"2022010519395368100_CIT0013","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1021\/pr101065j","article-title":"Andromeda: a peptide search engine integrated into the MaxQuant environment","volume":"10","author":"Cox","year":"2011","journal-title":"Journal of Proteome Research"},{"key":"2022010519395368100_CIT0014","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1016\/j.bbrc.2018.11.118","article-title":"Nitrate transporter NPF7.3\/NRT1.5 plays an essential role in regulating phosphate deficiency responses in Arabidopsis","volume":"508","author":"Cui","year":"2019","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2022010519395368100_CIT0015","doi-asserted-by":"crossref","first-page":"plz029","DOI":"10.1093\/aobpla\/plz029","article-title":"Providing carbon skeletons to sustain amide synthesis in roots underlines the suitability of Brachypodium distachyon for the study of ammonium stress in cereals","volume":"11","author":"De la Pe\u00f1a","year":"2019","journal-title":"AoB Plants"},{"key":"2022010519395368100_CIT0016","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.3389\/fpls.2018.01190","article-title":"Iron and zinc in the embryo and endosperm of rice (Oryza sativa L.) seeds in contrasting 2\u2032-deoxymugineic acid\/nicotianamine scenarios","volume":"9","author":"D\u00edaz-Benito","year":"2018","journal-title":"Frontiers in Plant Science"},{"key":"2022010519395368100_CIT0017","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1002\/jpln.19971600218","article-title":"Physiological and biochemical processes related to ammonium toxicity in higher plants","volume":"160","author":"Gerend\u00e1s","year":"1997","journal-title":"Zeitschrift f\u00fcr Pflanzenern\u00e4hrung und Bodenkunde"},{"key":"2022010519395368100_CIT0018","doi-asserted-by":"crossref","first-page":"6461","DOI":"10.1093\/jxb\/erz388","article-title":"The source of inorganic nitrogen has distinct effects on cell wall composition in Brachypodium distachyon","volume":"70","author":"Glazowska","year":"2019","journal-title":"Journal of Experimental Botany"},{"key":"2022010519395368100_CIT0019","doi-asserted-by":"crossref","first-page":"632285","DOI":"10.3389\/fpls.2020.632285","article-title":"A multi-species analysis defines anaplerotic enzymes and amides as metabolic markers for ammonium nutrition","volume":"11","author":"Gonz\u00e1lez-Moro","year":"2021","journal-title":"Frontiers in Plant Science"},{"key":"2022010519395368100_CIT0020","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1105\/tpc.111.095042","article-title":"Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis","volume":"24","author":"Haydon","year":"2012","journal-title":"The Plant Cell"},{"key":"2022010519395368100_CIT0021","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1016\/j.bbamcr.2012.03.010","article-title":"Getting a sense for signals: regulation of the plant iron deficiency response","volume":"1823","author":"Hindt","year":"2012","journal-title":"Biochimica et Biophysica Acta"},{"key":"2022010519395368100_CIT0022","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/j.atmosenv.2018.05.065","article-title":"DMPSA and DMPP equally reduce N2O emissions from a maize\u2013ryegrass forage rotation under Atlantic climate conditions","volume":"187","author":"Hu\u00e9rfano","year":"2018","journal-title":"Atmospheric Environment"},{"key":"2022010519395368100_CIT0023","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev-genet-112414-055135","article-title":"Brachypodium distachyon as a genetic model system","volume":"49","author":"Kellogg","year":"2015","journal-title":"Annual Review of Genetics"},{"key":"2022010519395368100_CIT0024","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.freeradbiomed.2018.10.439","article-title":"Iron transport and its regulation in plants","volume":"133","author":"Kobayashi","year":"2019","journal-title":"Free Radical Biology & Medicine"},{"key":"2022010519395368100_CIT0025","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1093\/jxb\/eri131","article-title":"Expression of iron-acquisition-related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements","volume":"56","author":"Kobayashi","year":"2005","journal-title":"Journal of Experimental Botany"},{"key":"2022010519395368100_CIT0026","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1002\/jpln.19941570602","article-title":"Effect of various nitrogen forms on the pH in leaf apoplast and on iron chlorosis of Glycine max L","volume":"157","author":"Kosegarten","year":"1994","journal-title":"Zeitschrift f\u00fcr Pflanzenern\u00e4hrung und Bodenkunde"},{"key":"2022010519395368100_CIT0027","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.1080\/01904169809365499","article-title":"Comparative investigation on the susceptibility of faba bean (Vicia faba L.) and sunflower (Helianthus annuus L.) to iron chlorosis","volume":"21","author":"Kosegarten","year":"1998","journal-title":"Journal of Plant Nutrition"},{"key":"2022010519395368100_CIT0028","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1104\/pp.97.1.104","article-title":"Plant NAD(H)-glutamate dehydrogenase consists of two subunit polypeptides and their participation in the seven isoenzymes occurs in an ordered ratio","volume":"97","author":"Loulakakis","year":"1991","journal-title":"Plant Physiology"},{"key":"2022010519395368100_CIT0029","doi-asserted-by":"crossref","first-page":"16549","DOI":"10.1074\/jbc.270.28.16549","article-title":"Biosynthesis of phytosiderophores, mugineic acids, associated with methionine cycling","volume":"270","author":"Ma","year":"1995","journal-title":"Journal of Biological Chemistry"},{"key":"2022010519395368100_CIT0030","volume-title":"Marschner\u2019s mineral nutrition of higher plants","author":"Marschner","year":"2012"},{"key":"2022010519395368100_CIT0031","doi-asserted-by":"crossref","first-page":"6274","DOI":"10.1038\/ncomms7274","article-title":"AtNIGT1\/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip","volume":"6","author":"Medici","year":"2015","journal-title":"Nature Communications"},{"key":"2022010519395368100_CIT0032","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1111\/j.1399-3054.1988.tb09151.x","article-title":"Relationship between iron chlorosis and alkalinity in Zea mays","volume":"72","author":"Mengel","year":"1988","journal-title":"Physiologia Plantarum"},{"key":"2022010519395368100_CIT0033","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/j.1399-3054.2011.01516.x","article-title":"S-methylmethionine is involved in the salinity tolerance of Arabidopsis thaliana plants at germination and early growth stages","volume":"144","author":"Ogawa","year":"2012","journal-title":"Physiologia Plantarum"},{"key":"2022010519395368100_CIT0034","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.3389\/fpls.2017.01344","article-title":"Altered cell wall plasticity can restrict plant growth under ammonium nutrition","volume":"8","author":"Podg\u00f3rska","year":"2017","journal-title":"Frontiers in Plant Science"},{"key":"2022010519395368100_CIT0035","doi-asserted-by":"crossref","first-page":"189","DOI":"10.3389\/fpls.2014.00189","article-title":"There and back again, or always there? The evolution of rice combined strategy for Fe uptake","volume":"5","author":"Ricachenevsky","year":"2014","journal-title":"Frontiers in Plant Science"},{"key":"2022010519395368100_CIT0036","doi-asserted-by":"crossref","first-page":"1933","DOI":"10.1080\/01904160701629211","article-title":"Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants","volume":"30","author":"Roosta","year":"2007","journal-title":"Journal of Plant Nutrition"},{"key":"2022010519395368100_CIT0037","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.envexpbot.2019.02.010","article-title":"The proteome of Medicago truncatula in response to ammonium and urea nutrition reveals the role of membrane proteins and enzymes of root lignification","volume":"162","author":"Royo","year":"2019","journal-title":"Environmental and Experimental Botany"},{"key":"2022010519395368100_CIT0038","doi-asserted-by":"crossref","first-page":"29","DOI":"10.3389\/fpls.2016.00029","article-title":"Nitrogen source and external medium pH interaction differentially affects root and shoot metabolism in Arabidopsis","volume":"7","author":"Sarasketa","year":"2016","journal-title":"Frontiers in Plant Science"},{"key":"2022010519395368100_CIT0039","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1042\/BJ20121744","article-title":"Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis","volume":"451","author":"Sauter","year":"2013","journal-title":"The Biochemical Journal"},{"key":"2022010519395368100_CIT0040","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1080\/01904169309364548","article-title":"Effect of nitrogen fertilizer form on pH of the bulk soil and rhizosphere, and on the growth, phosphorus, and micronutrient uptake of bean","volume":"16","author":"Thomson","year":"1993","journal-title":"Journal of Plant Nutrition"},{"key":"2022010519395368100_CIT0041","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1038\/nmeth.3901","article-title":"The Perseus computational platform for comprehensive analysis of (prote)omics data","volume":"13","author":"Tyanova","year":"2016","journal-title":"Nature Methods"},{"key":"2022010519395368100_CIT0042","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1104\/pp.86.3.914","article-title":"Influence of nitrate and ammonium nutrition on the uptake, assimilation, and distribution of nutrients in Ricinus communis","volume":"86","author":"Van Beusichem","year":"1988","journal-title":"Plant Physiology"},{"key":"2022010519395368100_CIT0043","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.envexpbot.2018.03.018","article-title":"NH4+ facilitates iron reutilization in the cell walls of rice (Oryza sativa) roots under iron-deficiency conditions","volume":"151","author":"Zhu","year":"2018","journal-title":"Environmental and Experimental Botany"},{"key":"2022010519395368100_CIT0044","first-page":"1407","article-title":"Differential effects of nitrogen forms on cell wall phosphorus remobilization are mediated by nitric oxide, pectin content, and phosphate transporter expression","volume":"171","author":"Zhu","year":"2016","journal-title":"Plant Physiology"},{"key":"2022010519395368100_CIT0045","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1007\/s00425-019-03202-6","article-title":"Ammonium regulates Fe deficiency responses by enhancing nitric oxide signaling in Arabidopsis thaliana","volume":"250","author":"Zhu","year":"2019","journal-title":"Planta"},{"key":"2022010519395368100_CIT0046","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1023\/A:1011902320662","article-title":"Impact of nitrogen form on iron uptake and distribution in maize seedlings in solution culture","volume":"235","author":"Zou","year":"2001","journal-title":"Plant and Soil"}],"container-title":["Journal of Experimental Botany"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jxb\/advance-article-pdf\/doi\/10.1093\/jxb\/erab427\/40539713\/erab427.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jxb\/article-pdf\/73\/1\/263\/42074404\/erab427.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jxb\/article-pdf\/73\/1\/263\/42074404\/erab427.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,1,5]],"date-time":"2022-01-05T19:42:41Z","timestamp":1641411761000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jxb\/article\/73\/1\/263\/6376168"}},"subtitle":[],"editor":[{"given":"Stanislav","family":"Kopriva","sequence":"additional","affiliation":[{"name":"University of Cologne, Germany"}],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,9,27]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,9,27]]},"published-print":{"date-parts":[[2022,1,5]]}},"URL":"https:\/\/doi.org\/10.1093\/jxb\/erab427","relation":{},"ISSN":["0022-0957","1460-2431"],"issn-type":[{"value":"0022-0957","type":"print"},{"value":"1460-2431","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,1,5]]},"published":{"date-parts":[[2021,9,27]]}}}