{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T04:26:24Z","timestamp":1790396784675,"version":"4.1.0"},"reference-count":40,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,12,2]],"date-time":"2016-12-02T00:00:00Z","timestamp":1480636800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,12,2]],"date-time":"2016-12-02T00:00:00Z","timestamp":1480636800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Understanding Zn uptake dynamics is critical to rice grain Zn biofortification. Here we examined soil Zn availability and Zn uptake pathways as affected by genotype (high-grain Zn varieties IR69428 and IR68144), Zn fertilization and water management in two pot experiments. Results showed significant interactions (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.05) between genotypes and Zn fertilization on DTPA (diethylenetriaminepentaacetic acid)-extractable soil Zn from early tillering to flowering. DTPA-extractable Zn in soils grown with IR69428 was positively correlated with stem (<jats:italic>r<\/jats:italic>\u2009=\u20090.78, <jats:italic>P<\/jats:italic>\u2009&lt;\u20090.01), flagleaf (<jats:italic>r<\/jats:italic>\u2009=\u20090.60, <jats:italic>P<\/jats:italic>\u2009&lt;\u20090.01) and g<jats:italic>r<\/jats:italic>ain (<jats:italic>r<\/jats:italic>\u2009=\u20090.67, <jats:italic>P<\/jats:italic>\u2009&lt;\u20090.01) Zn concentrations, suggesting improved soil Zn availability and continued soil Zn uptake by IR69428 even at maturity. Conversely for IR68144, DTPA-extractable Zn was positively correlated only with leaf Zn uptake (<jats:italic>r<\/jats:italic>\u2009=\u20090.60, <jats:italic>P<\/jats:italic>\u2009&lt;\u20090.01) at active tillering, indicating dependence on remobilization for grain Zn loading. Furthermore, the highest grain Zn concentration (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.05) was produced by a combination of IR69428 and Zn fertilization applied at panicle initiation (38.5\u2009\u03bcg\u2009g<jats:sup>\u22121<\/jats:sup>) compared with other treatments (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.05). The results highlight that Zn uptake behavior of a rice genotype determines the fate of Zn from the soil to the grain. This has implications on overcoming Zn translocation barriers between vegetative parts and grains, and achieving grain Zn biofortification targets (30.0\u2009\u03bcg\u2009g<jats:sup>\u22121<\/jats:sup>).<\/jats:p>","DOI":"10.1038\/srep38301","type":"journal-article","created":{"date-parts":[[2016,12,2]],"date-time":"2016-12-02T10:09:55Z","timestamp":1480673395000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["Zn uptake behavior of rice genotypes and its implication on grain Zn biofortification"],"prefix":"10.1038","volume":"6","author":[{"given":"Sarah E.","family":"Johnson-Beebout","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johnvie Bayang","family":"Goloran","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francis H. C.","family":"Rubianes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jack D. C.","family":"Jacob","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oliver B.","family":"Castillo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,12,2]]},"reference":[{"key":"BFsrep38301_CR1","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":"BFsrep38301_CR2","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1016\/S0140-6736(13)60937-X","volume":"382","author":"RE Black","year":"2013","unstructured":"Black, R. E. et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382, 427\u201351 (2013).","journal-title":"Lancet"},{"key":"BFsrep38301_CR3","first-page":"94","volume":"25","author":"C Hotz","year":"2004","unstructured":"Hotz, C. & Brown, K. H. Assessment of the risk of zinc deficiency in populations and options 216 for its control. Food Nutr. Bull. 25, 94\u2013204 (2004).","journal-title":"Food Nutr. Bull."},{"key":"BFsrep38301_CR4","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1007\/s11104-007-9368-4","volume":"306","author":"M Wissuwa","year":"2008","unstructured":"Wissuwa, M., Ismail, A. B. & Graham, R. D. Rice grain zinc concentrations as affected by genotype, native soil-zinc availability, and zinc fertilization. Plant Soil 306, 37\u201348 (2008).","journal-title":"Plant Soil"},{"key":"BFsrep38301_CR5","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/S0378-4290(98)00130-0","volume":"60","author":"JG White","year":"1999","unstructured":"White, J. G. & Zasoski, R. J. Mapping soil micronutrients. Field Crops Res. 60, 11\u201326 (1999).","journal-title":"Field Crops Res"},{"key":"BFsrep38301_CR6","doi-asserted-by":"publisher","first-page":"1064","DOI":"10.1093\/jn\/136.4.1064","volume":"136","author":"P Nestel","year":"2006","unstructured":"Nestel, P., Bouis, H. E., Meenakshi, J. V. & Pfeiffer, W. Biofortification of staple food crops. J. Nutr. 136, 1064\u20131067 (2006).","journal-title":"J. Nutr."},{"key":"BFsrep38301_CR7","doi-asserted-by":"publisher","first-page":"S31","DOI":"10.1177\/15648265110321S105","volume":"32","author":"HE Bouis","year":"2011","unstructured":"Bouis, H. E., Hotz, C., McClafferty, B., Meenakshi, J. V. & Pfeiffer, W. H. Biofortification: a new tool to reduce micronutrient malnutrition. Food Nutr Bull 32, S31\u201340 (2011).","journal-title":"Food Nutr Bull"},{"key":"BFsrep38301_CR8","doi-asserted-by":"publisher","first-page":"6767","DOI":"10.1021\/jf100017e","volume":"58","author":"C Wu","year":"2010","unstructured":"Wu, C. et al. Uptake, translocation, and remobilization of zinc absorbed at different growth stages by rice genotypes of different Zn densities. J. Agric Food Chem. 58, 6767\u20136773 (2010).","journal-title":"J. Agric Food Chem."},{"key":"BFsrep38301_CR9","doi-asserted-by":"publisher","first-page":"2739","DOI":"10.1093\/jxb\/ert118","volume":"64","author":"SM Impa","year":"2013","unstructured":"Impa, S. M., Morete, M. J., Ismail, A. M., Schulin, R. & Johnson-Beebout, S. E. Zn uptake, translocation, and grain Zn loading in rice (Oryza sativa L.) genotypes selected for Zn deficiency tolerance and high grain Zn. J. Exp. Bot. 64, 2739\u20132751 (2013).","journal-title":"J. Exp. Bot."},{"key":"BFsrep38301_CR10","doi-asserted-by":"crossref","unstructured":"Tuyogon, D. S. J., Impa, S. M., Castillo, O. B., Larazo, W. & Johnson-Beebout, S. E. Enriching rice grain Zinc through Zinc fertilization and water management. Soil Fertility and Plant Nutrition. Soil Sci. Soc. Am. J. 80\u20131, 10.2136\/sssaj2015.07.0262 (2016).","DOI":"10.2136\/sssaj2015.07.0262"},{"key":"BFsrep38301_CR11","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1093\/aob\/mcs217","volume":"112","author":"TJ Rose","year":"2013","unstructured":"Rose, T. J. et al. Enhancing phosphorous and zinc acquisition efficiency in rice: acritical review of root traits and their potential utility in rice breeding. Ann. Bot. 112, 331\u2013345 doi: 10.1093\/aob\/mcs217 (2013).","journal-title":"Ann. Bot."},{"key":"BFsrep38301_CR12","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1111\/j.1365-3040.2009.02085.x","volume":"33","author":"T Arnold","year":"2010","unstructured":"Arnold, T. et al. Evidence for the mechanisms of zinc uptake by rice using isotope fractionation. Plant Cell Environ. 33, 370\u2013381 (2010).","journal-title":"Plant Cell Environ"},{"key":"BFsrep38301_CR13","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1111\/j.1469-8137.2009.03177.x","volume":"186","author":"B Widodo","year":"2010","unstructured":"Widodo, B. et al. Response to zinc deficiency of two rice lines with contrasting tolerance is determined by root growth maintenance and organic acid exudation rates, and not by zinc-transporter activity. New Phytol. 186, 400\u2013414 (2010).","journal-title":"New Phytol"},{"key":"BFsrep38301_CR14","doi-asserted-by":"publisher","first-page":"2038","DOI":"10.1111\/j.1365-3040.2011.02401.x","volume":"34","author":"M Ptashnyk","year":"2011","unstructured":"Ptashnyk, M., Rose, T., Jones, D. L. & Kirk, G. J. D. Enhanced zinc uptake by rice through phytosiderophore secretion: a modelling study. Plant, Cell Environ. 34, 2038\u20132046 (2011).","journal-title":"Plant, Cell Environ"},{"key":"BFsrep38301_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpls.2013.00464","volume":"4","author":"RA Sperotto","year":"2013","unstructured":"Sperotto, R. A. \u201cZn\/Fe remobilization from vegetative tissues to rice seeds: should I stay or should I go? Ask Zn\/Fe supply!\u201d Front Plant Sci. 4, 1\u20134, (2013).","journal-title":"Front Plant Sci"},{"key":"BFsrep38301_CR16","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1111\/j.1744-7348.2007.00138.x","volume":"150","author":"W Jiang","year":"2007","unstructured":"Jiang, W. et al. Uptake and distribution of root-applied or foliar-applied 65Zn after flowering in aerobic rice. Ann. Appl. Biol. 150, 383\u2013391 (2007).","journal-title":"Ann. Appl. Biol."},{"key":"BFsrep38301_CR17","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.tplants.2009.01.001","volume":"14","author":"TJ Stomph","year":"2009","unstructured":"Stomph, T. J., Jiang, W. & Struik, P. C. Zinc biofortification of cereals: rice differs from wheat and barley. Trends Plant Sci. 14, 23\u201324 (2009).","journal-title":"Trends Plant Sci"},{"key":"BFsrep38301_CR18","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1038\/nature11420","volume":"490","author":"ND Mueller","year":"2012","unstructured":"Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature, 490(7419), 254\u2013257 (2012).","journal-title":"Nature"},{"key":"BFsrep38301_CR19","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1016\/j.foodpol.2010.11.026","volume":"36","author":"RM Rejesus","year":"2011","unstructured":"Rejesus, R. M., Palis, F. G., Rodriguez, D. G. P., Lampayan, R. M. & Bouman, B. A. Impact of the alternate wetting and drying (AWD) water-saving irrigation technique: evidence from rice producers in the Philippines. Food Policy 36(2), 280\u2013288 (2011).","journal-title":"Food Policy"},{"key":"BFsrep38301_CR20","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1007\/s11104-012-1211-x","volume":"361","author":"N Phattarakul","year":"2012","unstructured":"Phattarakul, N. et al. Biofortification of rice grain with zinc through zinc fertilization in different countries. Plant Soil, 361(1\u20132), 131\u2013141 (2012).","journal-title":"Plant Soil"},{"key":"BFsrep38301_CR21","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/j.fcr.2013.05.012","volume":"149","author":"RL Mabesa","year":"2013","unstructured":"Mabesa, R. L., Impa, S. M., Grewal, D. & Johnson-Beebout, S. E. Contrasting grain-Zn response of biofortification rice (Oryza sativa L.) breeding lines to foliar Zn application. Field Crops Res. 149, 223\u2013233 (2013).","journal-title":"Field Crops Res"},{"key":"BFsrep38301_CR22","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/S0378-3774(00)00128-1","volume":"49","author":"BAM Bouman","year":"2001","unstructured":"Bouman, B. A. M. & Tuong, T. P. Field water management to save water and increase its productivity in irrigated lowland rice. Agri. Water Manage., 49(1), 11\u201330 (2001).","journal-title":"Agri. Water Manage."},{"key":"BFsrep38301_CR23","doi-asserted-by":"publisher","first-page":"e45428","DOI":"10.1371\/journal.pone.0045428","volume":"7","author":"Y Wei","year":"2012","unstructured":"Wei, Y., Shohag, M. J. I. & Yang, X. Biofortification and bioavailability of rice grain zinc as affected by different forms of foliar zinc fertilization. PloS One 79, e45428 (2012).","journal-title":"PloS One"},{"key":"BFsrep38301_CR24","doi-asserted-by":"crossref","unstructured":"Kirk, G. The biogeochemistry of submerged soils. Chichester. doi: 10.1002\/047086303X (John Wiley & Sons, Ltd. 2004).","DOI":"10.1002\/047086303X"},{"key":"BFsrep38301_CR25","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1111\/ejss.12303","volume":"67","author":"M Izquierdo","year":"2016","unstructured":"Izquierdo, M., Impa, S. M., Johnson\u2010Beebout, S. E., Weiss, D. J. & Kirk, G. J. D. Measurement of isotopically\u2010exchangeable Zn in Zn\u2010deficient paddy soil. Eur. J. Soil Sci. 67(1), 51\u201359 (2016).","journal-title":"Eur. J. Soil Sci."},{"key":"BFsrep38301_CR26","unstructured":"Dobermann, A. & Fairhusrt, A. Nutrient disorders and nutrient management. 84\u201385 (Potash and Phosphate Institute, 2000)."},{"key":"BFsrep38301_CR27","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/S0926-6690(98)00015-6","volume":"9","author":"K Brahim","year":"1998","unstructured":"Brahim, K., Ray, D. T. & Dierig, D. A. Growth and yield characteristics of Lesquerella fendleri as a function of plant density. Ind. Crops Prod. 9, 63\u201371, doi: 10.1016\/S0926-6690(98)00015-6 (1998).","journal-title":"Growth and yield characteristics of Lesquerella fendleri as a function of plant density. Ind. Crops Prod."},{"key":"BFsrep38301_CR28","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1007\/s11104-012-","volume":"361","author":"SM Impa","year":"2012","unstructured":"Impa, S. M. & Johnson-Beebout, S. E. Mitigating zinc deficiency and achieving high grain Zn in rice through integration of soil chemistry and plant physiology research. Plant Soil 361, 3\u201341, doi: 10.1007\/s11104-012- 1315\u20133.(2012).","journal-title":"Plant Soil"},{"key":"BFsrep38301_CR29","doi-asserted-by":"publisher","first-page":"19792","DOI":"10.1038\/srep19792","volume":"6","author":"KR Trijatmiko","year":"2016","unstructured":"Trijatmiko, K. R. et al. Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Sci Rep 6: 19792, doi: 10.1038\/srep19792 (2016).","journal-title":"Sci Rep"},{"key":"BFsrep38301_CR30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpls.2014.00008","volume":"5","author":"TJ Stomph","year":"2014","unstructured":"Stomph, T. J., Jiang, W., Van Der Putten, P. E. & Struik, P. C. Zinc allocation and re-allocation in rice. Front. Plant Sci. 5, 1\u20138 (2014).","journal-title":"Front. Plant Sci."},{"key":"BFsrep38301_CR31","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1016\/j.pbi.2006.03.015","volume":"9","author":"EP Colangelo","year":"2006","unstructured":"Colangelo, E. P. & Guerinot, M. L. Put the metal to the petal: metal uptake and transport throughout plants. Curr. Opin. Plant Biol. 9, 322\u2013330, doi: 10.1016\/j.pbi.2006.03.015 (2006).","journal-title":"Curr. Opin. Plant Biol."},{"key":"BFsrep38301_CR32","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.plantsci.2012.03.004","volume":"190","author":"RA Sperotto","year":"2012","unstructured":"Sperotto, R. A., Ricachenevsky, F. K., Waldow, V. A. & Fett, J. P. Iron biofortification in rice: it\u2019s a long way to the top. Plant Sci. 190, 24\u201339, doi: 10.1016\/j.plantsci.2012.03.004 (2012).","journal-title":"Plant Sci."},{"key":"BFsrep38301_CR33","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1097\/00010694-198011000-00004","volume":"130","author":"LN Mandal","year":"1980","unstructured":"Mandal, L. N. & Haldar, M. Influence of phosphorus and zinc application on the availability of zinc, copper, iron, manganese and phosphorus in waterlogged rice soil. Soil Sci. 130, 251\u2013257 (1980).","journal-title":"Soil Sci."},{"key":"BFsrep38301_CR34","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1100\/tsw.2005.63","volume":"5","author":"K Das","year":"2005","unstructured":"Das, K., Dang, R., Shivananda, T. N. & Sur, P. Interaction effect between phosphorus and zinc on their availability in soil in relation to their contents in stevia (Stevia rebaudiana). Sci. World J 5, 490\u2013495 (2005).","journal-title":"Sci. World J"},{"key":"BFsrep38301_CR35","doi-asserted-by":"crossref","unstructured":"Thomas, G. W. Soil pH and soil acidity in Methods of soil analysis : Part 3 (eds D. L. Sparks et al.) p. 475\u2013490, SSSA Book Series No. 5. SSSA, Madison, WI. (1996).","DOI":"10.2136\/sssabookser5.3.c16"},{"key":"BFsrep38301_CR36","doi-asserted-by":"publisher","first-page":"1004","DOI":"10.2136\/ sssaj1979.03615995004300050038x","volume":"43","author":"GW Gee","year":"1979","unstructured":"Gee, G. W. & Bauder J. W. Particle size analysis by hydrometer: A simplified method for routine textural analysis and a sensitivity test of measured parameters. Soil Sci. Soc. Am. J. 43, 1004\u20131007. doi: 10.2136\/ sssaj1979.03615995004300050038x (1979).","journal-title":"Soil Sci. Soc. Am. J"},{"key":"BFsrep38301_CR37","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1097\/00010694- 193401000-00003","volume":"37","author":"A Walkley","year":"1934","unstructured":"Walkley, A. & Black I. A. An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci. 37, 29\u201338, doi: 10.1097\/00010694- 193401000-00003 (1934).","journal-title":"Soil Sci."},{"key":"BFsrep38301_CR38","unstructured":"Olsen, S. R., Cole, C. V., F.S. Watanabe, F. S. & Dean, L. A. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circ. No. 939. U.S. Gov. Print. Office, Washington, DC (1954)."},{"key":"BFsrep38301_CR39","doi-asserted-by":"crossref","unstructured":"Sumner, M. E. & Miller, W. P. Cation exchange capacity and exchange coefficients. Methods of soil analysis : Part 3 (eds D. L. Sparks et al.) p. 1201\u20131229, SSSA Book Series No. 5. SSSA, Madison, WI. (1996).","DOI":"10.2136\/sssabookser5.3.c40"},{"key":"BFsrep38301_CR40","doi-asserted-by":"publisher","first-page":"1842","DOI":"10.1080\/00103620902896738","volume":"40","author":"SE Johnson-Beebout","year":"2009","unstructured":"Johnson-Beebout, S. E., Lauren, J. G. & Duxbury, J. M. Immobilization of zinc fertilizer in flooded soils monitored by adapted DTPA soil test. Commun. Soil Sci. Plant Anal. 40, 1842\u20131861, doi: 10.1080\/00103620902896738 (2009).","journal-title":"Commun. Soil Sci. Plant Anal."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep38301.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep38301","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep38301.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T01:12:59Z","timestamp":1672881179000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep38301"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,12,2]]},"references-count":40,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,12,23]]}},"alternative-id":["BFsrep38301"],"URL":"https:\/\/doi.org\/10.1038\/srep38301","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,12,2]]},"assertion":[{"value":"7 September 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 November 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 December 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"38301"}}