{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,27]],"date-time":"2026-04-27T12:36:54Z","timestamp":1777293414939,"version":"3.51.4"},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2021,2,16]],"date-time":"2021-02-16T00:00:00Z","timestamp":1613433600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2021,2,16]],"date-time":"2021-02-16T00:00:00Z","timestamp":1613433600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat. Plants"],"DOI":"10.1038\/s41477-021-00856-7","type":"journal-article","created":{"date-parts":[[2021,2,20]],"date-time":"2021-02-20T01:27:36Z","timestamp":1613784456000},"page":"137-143","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":132,"title":["Arabidopsis bZIP19 and bZIP23 act as zinc sensors to control plant zinc status"],"prefix":"10.1038","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3360-9405","authenticated-orcid":false,"given":"Grmay H.","family":"Lilay","sequence":"first","affiliation":[]},{"given":"Daniel P.","family":"Persson","sequence":"additional","affiliation":[]},{"given":"Pedro Humberto","family":"Castro","sequence":"additional","affiliation":[]},{"given":"Feixue","family":"Liao","sequence":"additional","affiliation":[]},{"given":"Ross D.","family":"Alexander","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5257-0740","authenticated-orcid":false,"given":"Mark G. M.","family":"Aarts","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5562-6807","authenticated-orcid":false,"given":"Ana G. L.","family":"Assun\u00e7\u00e3o","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2021,2,16]]},"reference":[{"key":"856_CR1","doi-asserted-by":"publisher","first-page":"4682","DOI":"10.1021\/cr800556u","volume":"109","author":"W Maret","year":"2009","unstructured":"Maret, W. & Li, Y. Coordination dynamics of zinc in proteins. Chem. Rev. 109, 4682\u20134707 (2009).","journal-title":"Chem. Rev."},{"key":"856_CR2","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1093\/jxb\/erh064","volume":"55","author":"RM Welch","year":"2004","unstructured":"Welch, R. M. & Graham, R. D. Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot. 55, 353\u2013364 (2004).","journal-title":"J. Exp. Bot."},{"key":"856_CR3","doi-asserted-by":"publisher","first-page":"e50568","DOI":"10.1371\/journal.pone.0050568","volume":"7","author":"KR Wessells","year":"2012","unstructured":"Wessells, K. R. & Brown, K. H. Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS ONE 7, e50568 (2012).","journal-title":"PLoS ONE"},{"key":"856_CR4","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1007\/s004250000458","volume":"212","author":"S Clemens","year":"2001","unstructured":"Clemens, S. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212, 475\u2013486 (2001).","journal-title":"Planta"},{"key":"856_CR5","doi-asserted-by":"publisher","first-page":"3173","DOI":"10.1021\/pr0603699","volume":"5","author":"C Andreini","year":"2006","unstructured":"Andreini, C., Banci, L., Bertini, I. & Rosato, A. Zinc through the three domains of life. J. Proteome Res. 5, 3173\u20133178 (2006).","journal-title":"J. Proteome Res."},{"key":"856_CR6","doi-asserted-by":"crossref","unstructured":"Choi, S. & Bird, A. J. Zinc\u2019ing sensibly: controlling zinc homeostasis at the transcriptional level. Metallomics 6, 1198\u20131215 (2014).","DOI":"10.1039\/C4MT00064A"},{"key":"856_CR7","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1039\/b926662c","volume":"2","author":"RA Colvin","year":"2010","unstructured":"Colvin, R. A., Holmes, W. R., Fontaine, C. P. & Maret, W. Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis. Metallomics 2, 297\u2013356 (2010).","journal-title":"Metallomics"},{"key":"856_CR8","doi-asserted-by":"publisher","first-page":"1199","DOI":"10.1046\/j.1365-2958.1998.00883.x","volume":"28","author":"SI Patzer","year":"1998","unstructured":"Patzer, S. I. & Hantke, K. The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol. Microbiol. 28, 1199\u20131210 (1998).","journal-title":"Mol. Microbiol."},{"key":"856_CR9","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1023\/A:1012932712483","volume":"14","author":"GK Andrews","year":"2001","unstructured":"Andrews, G. K. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 14, 223\u2013237 (2001).","journal-title":"Biometals"},{"key":"856_CR10","doi-asserted-by":"publisher","first-page":"18565","DOI":"10.1074\/jbc.R900014200","volume":"284","author":"DJ Eide","year":"2009","unstructured":"Eide, D. J. Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J. Biol. Chem. 284, 18565\u201318569 (2009).","journal-title":"J. Biol. Chem."},{"key":"856_CR11","doi-asserted-by":"publisher","first-page":"10296","DOI":"10.1073\/pnas.1004788107","volume":"107","author":"AGL Assun\u00e7\u00e3o","year":"2010","unstructured":"Assun\u00e7\u00e3o, A. G. L. et al. Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc. Natl Acad. Sci. USA 107, 10296\u201310301 (2010).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"856_CR12","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1126\/science.2683088","volume":"246","author":"CR Vinson","year":"1989","unstructured":"Vinson, C. R., Sigler, P. B. & McKnight, S. L. Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science 246, 911\u2013916 (1989).","journal-title":"Science"},{"key":"856_CR13","doi-asserted-by":"publisher","first-page":"1480","DOI":"10.1093\/molbev\/msl022","volume":"23","author":"CD Deppmann","year":"2006","unstructured":"Deppmann, C. D., Alvania, R. S. & Taparowsky, E. J. Cross-species annotation of basic leucine zipper factor interactions: insight into the evolution of closed interaction networks. Mol. Biol. Evol. 23, 1480\u20131492 (2006).","journal-title":"Mol. Biol. Evol."},{"key":"856_CR14","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-03903-6","volume":"7","author":"PH Castro","year":"2017","unstructured":"Castro, P. H. et al. Phylogenetic analysis of F-bZIP transcription factors indicates conservation of the zinc deficiency response across land plants. Sci. Rep. 7, 3806 (2017).","journal-title":"Sci. Rep."},{"key":"856_CR15","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/S0005-2736(00)00138-3","volume":"1465","author":"M Guerinot","year":"2000","unstructured":"Guerinot, M. & Lou The ZIP family of metal transporters. Biochim. Biophys. Acta 1465, 190\u2013198 (2000).","journal-title":"Biochim. Biophys. Acta"},{"key":"856_CR16","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1007\/s10534-013-9643-1","volume":"26","author":"S Clemens","year":"2013","unstructured":"Clemens, S., Deinlein, U., Ahmadi, H., H\u00f6reth, S. & Uraguchi, S. Nicotianamine is a major player in plant Zn homeostasis. BioMetals 26, 623\u2013632 (2013).","journal-title":"BioMetals"},{"key":"856_CR17","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1111\/tpj.12996","volume":"84","author":"S Inaba","year":"2015","unstructured":"Inaba, S. et al. Identification of putative target genes of bZIP19, a transcription factor essential for Arabidopsis adaptation to Zn deficiency in roots. Plant J. 84, 323\u2013334 (2015).","journal-title":"Plant J."},{"key":"856_CR18","doi-asserted-by":"publisher","first-page":"1955","DOI":"10.3389\/fpls.2018.01955","volume":"9","author":"GH Lilay","year":"2019","unstructured":"Lilay, G. H., Castro, P. H., Campilho, A. & Assun\u00e7\u00e3o, A. G. L. The Arabidopsis bZIP19 and bZIP23 activity requires zinc deficiency\u2014insight on regulation from complementation lines. Front. Plant Sci. 9, 1955 (2019).","journal-title":"Front. Plant Sci."},{"key":"856_CR19","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1039\/c3mt00070b","volume":"5","author":"AGL Assun\u00e7\u00e3o","year":"2013","unstructured":"Assun\u00e7\u00e3o, A. G. L. et al. Model of how plants sense zinc deficiency. Metallomics 5, 1110\u20131116 (2013).","journal-title":"Metallomics"},{"key":"856_CR20","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1039\/b905688b","volume":"1","author":"DP Persson","year":"2009","unstructured":"Persson, D. P., Hansen, T. H., Laursen, K. H., Schjoerring, J. K. & Husted, S. Simultaneous iron, zinc, sulfur and phosphorus speciation analysis of barley grain tissues using SEC-ICP-MS and IP-ICP-MS. Metallomics 1, 418\u2013426 (2009).","journal-title":"Metallomics"},{"key":"856_CR21","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1016\/j.gdata.2016.01.021","volume":"7","author":"H Azevedo","year":"2016","unstructured":"Azevedo, H. et al. Transcriptomic profiling of Arabidopsis gene expression in response to varying micronutrient zinc supply. Genom. Data 7, 256\u2013258 (2016).","journal-title":"Genom. Data"},{"key":"856_CR22","doi-asserted-by":"publisher","first-page":"82","DOI":"10.3945\/an.112.003038","volume":"4","author":"W Maret","year":"2013","unstructured":"Maret, W. Zinc Biochemistry: from a single zinc enzyme to a key element of life. Adv. Nutr. 4, 82\u201391 (2013).","journal-title":"Adv. Nutr."},{"key":"856_CR23","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.abb.2016.04.010","volume":"611","author":"A Kr\u0119\u017cel","year":"2016","unstructured":"Kr\u0119\u017cel, A. & Maret, W. The biological inorganic chemistry of zinc ions. Arch. Biochem. Biophys. 611, 3\u201319 (2016).","journal-title":"Arch. Biochem. Biophys."},{"key":"856_CR24","doi-asserted-by":"publisher","first-page":"2902","DOI":"10.1111\/pce.13627","volume":"42","author":"S Clemens","year":"2019","unstructured":"Clemens, S. Metal ligands in micronutrient acquisition and homeostasis. Plant Cell Environ. 42, 2902\u20132912 (2019).","journal-title":"Plant Cell Environ."},{"key":"856_CR25","doi-asserted-by":"publisher","DOI":"10.1038\/srep21437","volume":"6","author":"Y Kashiv","year":"2016","unstructured":"Kashiv, Y. et al. Imaging trace element distributions in single organelles and subcellular features. Sci. Rep. 6, 21437 (2016).","journal-title":"Sci. Rep."},{"key":"856_CR26","doi-asserted-by":"publisher","first-page":"28713","DOI":"10.1074\/jbc.273.44.28713","volume":"273","author":"H Zhao","year":"1998","unstructured":"Zhao, H. et al. Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J. Biol. Chem. 273, 28713\u201328720 (1998).","journal-title":"J. Biol. Chem."},{"key":"856_CR27","doi-asserted-by":"publisher","first-page":"7957","DOI":"10.1073\/pnas.97.14.7957","volume":"97","author":"TJ Lyons","year":"2000","unstructured":"Lyons, T. J. et al. Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc. Natl Acad. Sci. USA 97, 7957\u20137962 (2000).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"856_CR28","doi-asserted-by":"publisher","first-page":"5137","DOI":"10.1093\/emboj\/cdg484","volume":"22","author":"AJ Bird","year":"2003","unstructured":"Bird, A. J. et al. Zinc fingers can act as Zn2+ sensors to regulate transcriptional activation domain function. EMBO J. 22, 5137\u20135146 (2003).","journal-title":"EMBO J."},{"key":"856_CR29","doi-asserted-by":"publisher","first-page":"e22535","DOI":"10.1371\/journal.pone.0022535","volume":"6","author":"AG Frey","year":"2011","unstructured":"Frey, A. G. et al. Zinc-regulated DNA binding of the yeast Zap1 zinc-responsive activator. PLoS ONE 6, e22535 (2011).","journal-title":"PLoS ONE"},{"key":"856_CR30","doi-asserted-by":"publisher","first-page":"1440","DOI":"10.1093\/pcp\/pcz038","volume":"60","author":"T Kobayashi","year":"2019","unstructured":"Kobayashi, T. Understanding the complexity of iron sensing and signaling cascades in plants. Plant Cell Physiol. 60, 1440\u20131446 (2019).","journal-title":"Plant Cell Physiol."},{"key":"856_CR31","doi-asserted-by":"publisher","first-page":"24933","DOI":"10.1073\/pnas.1916892116","volume":"116","author":"SA Kim","year":"2019","unstructured":"Kim, S. A., LaCroix, I. S., Gerber, S. A. & Guerinot, M. Lou. The iron deficiency response in Arabidopsis thaliana requires the phosphorylated transcription factor URI. Proc. Natl Acad. Sci. USA 116, 24933\u201324942 (2019).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"856_CR32","doi-asserted-by":"crossref","unstructured":"Castro, P. H., Lilay, G. H. & Assuncao, A. G. L. in Plant Micronutrient Use Efficiency: Molecular and Genomic Perspectives in Crop Plants (eds Hossain M. A. et al.) Ch. 1, 1\u201310 (Academic Press Books, Elsevier, 2018).","DOI":"10.1016\/B978-0-12-812104-7.00002-2"},{"key":"856_CR33","doi-asserted-by":"publisher","first-page":"953","DOI":"10.1016\/j.molcel.2018.02.009","volume":"69","author":"G Dubeaux","year":"2018","unstructured":"Dubeaux, G., Neveu, J., Zelazny, E. & Vert, G. Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition. Mol. Cell 69, 953\u2013964 (2018).","journal-title":"Mol. Cell"},{"key":"856_CR34","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1111\/ejss.12437","volume":"69","author":"I Cakmak","year":"2018","unstructured":"Cakmak, I. & Kutman, U. B. Agronomic biofortification of cereals with zinc: a review. Eur. J. Soil Sci. 69, 172\u2013180 (2018).","journal-title":"Eur. J. Soil Sci."},{"key":"856_CR35","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1111\/j.1469-8137.2008.02738.x","volume":"182","author":"PJ White","year":"2009","unstructured":"White, P. J. & Broadley, M. R. Biofortification of crops with seven mineral elements often lacking in human diets\u2013iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 182, 49\u201384 (2009).","journal-title":"New Phytol."},{"key":"856_CR36","doi-asserted-by":"publisher","first-page":"2754","DOI":"10.1111\/pce.13045","volume":"40","author":"AZ Nazri","year":"2017","unstructured":"Nazri, A. Z., Griffin, J. H. C., Peaston, K. A., Alexander-Webber, D. G. A. & Williams, L. E. F-group bZIPs in barley\u2014a role in Zn deficiency. Plant. Cell Environ. 40, 2754\u20132770 (2017).","journal-title":"Plant. Cell Environ."},{"key":"856_CR37","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1111\/tpj.13655","volume":"92","author":"NP Evens","year":"2017","unstructured":"Evens, N. P., Buchner, P., Williams, L. E. & Hawkesford, M. J. The role of ZIP transporters and group F bZIP transcription factors in the Zn-deficiency response of wheat (Triticum aestivum). Plant J. 92, 291\u2013304 (2017).","journal-title":"Plant J."},{"key":"856_CR38","doi-asserted-by":"publisher","first-page":"3664","DOI":"10.1093\/jxb\/eraa115","volume":"71","author":"GH Lilay","year":"2020","unstructured":"Lilay, G. H. et al. Rice F-bZIP transcription factors regulate the zinc deficiency response. J. Exp. Bot. 71, 3664\u20133677 (2020).","journal-title":"J. Exp. Bot."},{"key":"856_CR39","doi-asserted-by":"publisher","first-page":"686","DOI":"10.1038\/nbt.2650","volume":"31","author":"Q Shan","year":"2013","unstructured":"Shan, Q. et al. Targeted genome modification of crop plants using a CRISPR\u2013Cas system. Nat. Biotechnol. 31, 686\u2013688 (2013).","journal-title":"Nat. Biotechnol."},{"key":"856_CR40","doi-asserted-by":"publisher","first-page":"616","DOI":"10.1111\/j.1365-313X.2005.02617.x","volume":"45","author":"KW Earley","year":"2006","unstructured":"Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616\u2013629 (2006).","journal-title":"Plant J."},{"key":"856_CR41","doi-asserted-by":"publisher","first-page":"3901","DOI":"10.1002\/j.1460-2075.1987.tb02730.x","volume":"6","author":"RA Jefferson","year":"1987","unstructured":"Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901\u20133907 (1987).","journal-title":"EMBO J."},{"key":"856_CR42","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","volume":"25","author":"KJ Livak","year":"2001","unstructured":"Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method. Methods 25, 402\u2013408 (2001).","journal-title":"Methods"},{"key":"856_CR43","doi-asserted-by":"crossref","unstructured":"Olsen, L. I. et al. Mother-plant-mediated pumping of zinc into the developing seed. Nat. Plants 2, 16036 (2016).","DOI":"10.1038\/nplants.2016.36"}],"container-title":["Nature Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41477-021-00856-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41477-021-00856-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41477-021-00856-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,2]],"date-time":"2022-12-02T14:50:02Z","timestamp":1669992602000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41477-021-00856-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,16]]},"references-count":43,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["856"],"URL":"https:\/\/doi.org\/10.1038\/s41477-021-00856-7","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.06.29.177287","asserted-by":"object"}]},"ISSN":["2055-0278"],"issn-type":[{"value":"2055-0278","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,16]]},"assertion":[{"value":"7 July 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 January 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 February 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}