{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T23:26:29Z","timestamp":1787009189161,"version":"build-2736575974"},"reference-count":55,"publisher":"Oxford University Press (OUP)","issue":"18","license":[{"start":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T00:00:00Z","timestamp":1656979200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100007173","name":"Bio-oriented Technology Research Advancement Institution","doi-asserted-by":"publisher","award":["JPJ007097"],"award-info":[{"award-number":["JPJ007097"]}],"id":[{"id":"10.13039\/501100007173","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,10,18]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Decreasing cadmium (Cd) concentrations in rice grains can effectively reduce potential risks to human health because rice is the major contributor to Cd intake in many diets. Among several genes involved in rice Cd accumulation, the loss of function of OsNRAMP5 is known to be effective in reducing grain concentration by inhibiting root uptake. However, disruption of this gene simultaneously decreases manganese (Mn) uptake because OsNRAMP5 is a major Mn transporter. With the aim of improving Mn uptake in OsNRAMP5 mutants while still restricting the grain Cd concentration below the upper limit of international standards, we identified a novel OsNRAMP5 allele encoding a protein in which glutamine (Q) at position 337 was replaced by lysine (K). The mutant carrying the OsNRAMP5-Q337K allele showed intermediate Cd and Mn accumulation between that of the wild-type and OsNRAMP5-knockout lines, and exhibited more resistance to Mn deficiency than the knockout lines. Different amino acid substitutions at position Q337 significantly affected the Cd and Mn transport activity in yeast cells, indicating that it is one of the crucial sites for OsNRAMP5 function. Our results suggest that the OsNRAMP5-Q337K allele might be useful for reducing grain Cd concentrations without causing severe Mn deficiency in rice cultivars through DNA marker-assisted breeding.<\/jats:p>","DOI":"10.1093\/jxb\/erac302","type":"journal-article","created":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T10:27:27Z","timestamp":1657016847000},"page":"6475-6489","source":"Crossref","is-referenced-by-count":38,"title":["A weak allele of\n                    <i>OsNRAMP5<\/i>\n                    confers moderate cadmium uptake while avoiding manganese deficiency in rice"],"prefix":"10.1093","volume":"73","author":[{"given":"Masato","family":"Kuramata","sequence":"first","affiliation":[{"name":"Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO) , Tsukuba , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tadashi","family":"Abe","sequence":"additional","affiliation":[{"name":"Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO) , Tsukuba , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hachidai","family":"Tanikawa","sequence":"additional","affiliation":[{"name":"Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO) , Tsukuba , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kazuhiko","family":"Sugimoto","sequence":"additional","affiliation":[{"name":"Institute of Crop Sciences, NARO , Tsukuba , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6155-3050","authenticated-orcid":false,"given":"Satoru","family":"Ishikawa","sequence":"additional","affiliation":[{"name":"Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO) , Tsukuba , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,7,5]]},"reference":[{"key":"2022101813193536500_CIT0001","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1270\/jsbbr.19.109","article-title":"\u2018Koshihikari Kan No. 1\u2019, a new rice variety with nearly cadmium-free in grains.","volume":"19","author":"Abe","year":"2017","journal-title":"Breeding Research"},{"key":"2022101813193536500_CIT0002","author":"Bellinger","year":"2001"},{"key":"2022101813193536500_CIT0003","doi-asserted-by":"crossref","first-page":"1637","DOI":"10.1126\/science.8503008","article-title":"Structural basis of amino acid alpha helix propensity","volume":"260","author":"Blaber","year":"1993","journal-title":"Science"},{"key":"2022101813193536500_CIT0004","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/B978-0-12-384905-2.00007-8","article-title":"Function of nutrients: micronutrients.","volume-title":"Marschner\u2019s mineral nutrition of higher plants,","author":"Broadley","year":"2012","edition":"3"},{"key":"2022101813193536500_CIT0005","doi-asserted-by":"crossref","first-page":"2102","DOI":"10.1016\/j.str.2016.09.017","article-title":"Crystal structure and conformational change mechanism of a bacterial Nramp-family divalent metal transporter","volume":"24","author":"Bozzi","year":"2016","journal-title":"Structure"},{"key":"2022101813193536500_CIT0006","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1085\/jgp.201912428","article-title":"Unique structural features in an Nramp metal transporter impart substrate-specific proton cotransport and a kinetic bias to favor import","volume":"151","author":"Bozzi","year":"2019","journal-title":"Journal of General Physiology"},{"key":"2022101813193536500_CIT0007","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1016\/S0021-9258(17)49881-4","article-title":"Transmembrane helix 6b links proton and metal release pathways and drives conformational change in an Nramp-family transition metal transporter","volume":"295","author":"Bozzi","year":"2020","journal-title":"Journal of Biological Chemistry"},{"key":"2022101813193536500_CIT0008","doi-asserted-by":"crossref","first-page":"2476","DOI":"10.1111\/pce.13843","article-title":"OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice","volume":"43","author":"Chang","year":"2020","journal-title":"Plant, Cell & Environment"},{"key":"2022101813193536500_CIT0009","doi-asserted-by":"crossref","first-page":"5537","DOI":"10.1093\/jxb\/erz366","article-title":"Safer food through plant science: reducing toxic element accumulation in crops","volume":"70","author":"Clemens","year":"2019","journal-title":"Journal of Experimental Botany"},{"key":"2022101813193536500_CIT0010","author":"Codex","year":"2006"},{"key":"2022101813193536500_CIT0011","volume-title":"Rice. Nutrient disorders and nutrient management.","author":"Dobermann","year":"2000"},{"key":"2022101813193536500_CIT0012","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1038\/nsmb.2904","article-title":"Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport","volume":"21","author":"Ehrnstorfer","year":"2014","journal-title":"Nature Structural & Molecular Biology"},{"key":"2022101813193536500_CIT0013","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1038\/nprot.2007.13","article-title":"High-efficiency yeast transformation using the LiAc\/SS carrier DNA\/PEG method","volume":"2","author":"Gietz","year":"2007","journal-title":"Nature Protocols"},{"key":"2022101813193536500_CIT0014","doi-asserted-by":"crossref","first-page":"476","DOI":"10.3389\/fpls.2018.00476","article-title":"A node-expressed transporter OsCCX2 Is involved in grain cadmium accumulation of rice.","volume":"9","author":"Hao","year":"2018","journal-title":"Frontiers Plant Science"},{"key":"2022101813193536500_CIT0015","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1093\/nar\/gkq366","article-title":"Dali server: conservation mapping in 3D","volume":"38","author":"Holm","year":"2010","journal-title":"Nucleic Acids Research"},{"key":"2022101813193536500_CIT0016","first-page":"213","article-title":"Concentrations of nutrient content in rice variety Koshihikari Kan No.1 and risk estimation of incidence of brown spot disease in different paddy fields.","volume":"88","author":"Honma","year":"2017","journal-title":"Japanese Journal of Soil Science and Plant Nutrition"},{"key":"2022101813193536500_CIT0017","doi-asserted-by":"crossref","first-page":"19166","DOI":"10.1073\/pnas.1211132109","article-title":"Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice","volume":"109","author":"Ishikawa","year":"2012","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2022101813193536500_CIT0018","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1186\/1471-2229-11-172","article-title":"Real-time imaging and analysis of differences in cadmium dynamics in rice cultivars (Oryza sativa) using positron-emitting 107Cd tracer","volume":"11","author":"Ishikawa","year":"2011","journal-title":"BMC Plant Biology"},{"key":"2022101813193536500_CIT0019","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1038\/srep00286","article-title":"Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport","volume":"2","author":"Ishimaru","year":"2012","journal-title":"Scientific Reports"},{"key":"2022101813193536500_CIT0020","first-page":"1","article-title":"Health effects of cadmium exposure \u2013 a review of the literature and a risk estimate","volume":"24","author":"J\u00e4rup","year":"1998","journal-title":"Scandinavian Journal of Work, Environment & Health"},{"key":"2022101813193536500_CIT0021","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","article-title":"Highly accurate protein structure prediction with AlphaFold","volume":"596","author":"Jumper","year":"2021","journal-title":"Nature"},{"key":"2022101813193536500_CIT0022","doi-asserted-by":"crossref","first-page":"2577","DOI":"10.1002\/bip.360221211","article-title":"Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features","volume":"22","author":"Kabsch","year":"1983","journal-title":"Biopolymers"},{"key":"2022101813193536500_CIT0023","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1080\/19440049.2010.529620","article-title":"Probabilistic risk assessment of dietary cadmium in the South Korean population.","volume":"28","author":"Kim","year":"2011","journal-title":"Food Additives & Contaminants: Part A"},{"key":"2022101813193536500_CIT0024","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1186\/s12284-019-0349-z","article-title":"Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR\/Cas9-mediated mutagenesis for breeding low Cd rice","volume":"26","author":"Liu","year":"2019","journal-title":"Rice Science"},{"key":"2022101813193536500_CIT0025","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S1002-0160(20)60015-7","article-title":"Transport of cadmium from soil to grain in cereal crops: a review","volume":"31","author":"Ma","year":"2021","journal-title":"Pedosphere"},{"key":"2022101813193536500_CIT0026","author":"MAFF","year":"2018"},{"key":"2022101813193536500_CIT0027","first-page":"300","article-title":"Dietary exposure to essential and potentially toxic elements for the population of Hanoi, Vietnam","volume":"22","author":"Marcussen","year":"2013","journal-title":"Asia Pacific Journal of Clinical Nutrition"},{"key":"2022101813193536500_CIT0028","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1093\/bioinformatics\/17.7.646","article-title":"Evaluation of methods for the prediction of membrane spanning regions","volume":"17","author":"Moller","year":"2001","journal-title":"Bioinformatics"},{"key":"2022101813193536500_CIT0029","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1104\/pp.107.113613","article-title":"Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis","volume":"147","author":"Morgan","year":"2008","journal-title":"Plant Physiology"},{"key":"2022101813193536500_CIT0030","doi-asserted-by":"crossref","first-page":"4321","DOI":"10.1093\/nar\/8.19.4321","article-title":"Rapid isolation of high molecular weight plant DNA","volume":"8","author":"Murray","year":"1980","journal-title":"Nucleic Acids Research"},{"key":"2022101813193536500_CIT0031","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1016\/S0168-9525(02)02820-2","article-title":"Web-based primer design for single nucleotide polymorphism analysis","volume":"18","author":"Neff","year":"2002","journal-title":"Trends in Genetics"},{"key":"2022101813193536500_CIT0032","first-page":"133","article-title":"Current issues in low-dose cadmium toxicology: nephrotoxicity and carcinogenicity.","volume":"4","author":"Nordberg","year":"1996","journal-title":"Environmental Science"},{"key":"2022101813193536500_CIT0033","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1016\/S0006-3495(98)77529-0","article-title":"A helix propensity scale based on experimental studies of peptides and proteins","volume":"75","author":"Pace","year":"1998","journal-title":"Biophysical Journal"},{"key":"2022101813193536500_CIT0034","doi-asserted-by":"crossref","first-page":"100182","DOI":"10.1016\/j.xpro.2020.100182","article-title":"A quantitative imaging-based protocol for yeast growth and survival on agar plates","volume":"1","author":"Petropavlovskiy","year":"2020","journal-title":"STAR Protocols"},{"key":"2022101813193536500_CIT0035","doi-asserted-by":"crossref","first-page":"6194","DOI":"10.1038\/s41598-017-06446-y","article-title":"A novel proton transfer mechanism in the SLC11 family of divalent metal ion transporters","volume":"7","author":"Pujol-Gim\u00e9nez","year":"2017","journal-title":"Scientific Reports"},{"key":"2022101813193536500_CIT0036","doi-asserted-by":"crossref","first-page":"6013","DOI":"10.1093\/jxb\/eru340","article-title":"Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice","volume":"65","author":"Sasaki","year":"2014","journal-title":"Journal of Experimental Botany"},{"key":"2022101813193536500_CIT0037","doi-asserted-by":"crossref","first-page":"2155","DOI":"10.1105\/tpc.112.096925","article-title":"Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice","volume":"24","author":"Sasaki","year":"2012","journal-title":"The Plant Cell"},{"key":"2022101813193536500_CIT0038","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1093\/pcp\/pcr166","article-title":"Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium","volume":"53","author":"Satoh-Nagasawa","year":"2012","journal-title":"Plant & Cell Physiology"},{"key":"2022101813193536500_CIT0039","doi-asserted-by":"crossref","first-page":"e0177978","DOI":"10.1371\/journal.pone.0177978","article-title":"Dietary cadmium exposure assessment among the Chinese population","volume":"12","author":"Song","year":"2017","journal-title":"PLoS ONE"},{"key":"2022101813193536500_CIT0040","doi-asserted-by":"crossref","first-page":"1948","DOI":"10.1111\/j.1365-3040.2012.02527.x","article-title":"The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice","volume":"35","author":"Takahashi","year":"2012","journal-title":"Plant, Cell & Environment"},{"key":"2022101813193536500_CIT0041","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.bbrc.2019.03.024","article-title":"OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn\/Cd to grain in rice","volume":"512","author":"Tan","year":"2019","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2022101813193536500_CIT0042","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1080\/00380768.1966.10431958","article-title":"Interaction between iron and manganese in the rice plant","volume":"12","author":"Tanaka","year":"1966","journal-title":"Soil Science and Plant Nutrition"},{"key":"2022101813193536500_CIT0043","doi-asserted-by":"crossref","first-page":"14438","DOI":"10.1038\/s41598-017-14832-9","article-title":"Knockout of OsNramp5 using the CRISPR\/Cas9 system produces low Cd-accumulating indica rice without compromising yield","volume":"7","author":"Tang","year":"2017","journal-title":"Scientific Reports"},{"key":"2022101813193536500_CIT0044","first-page":"394","article-title":"Single-step protocol for preparation of plant tissue for analysis by PCR","volume":"19","author":"Thomson","year":"1995","journal-title":"Biotechniques"},{"key":"2022101813193536500_CIT0045","doi-asserted-by":"crossref","first-page":"16500","DOI":"10.1073\/pnas.1005396107","article-title":"Gene limiting cadmium accumulation in rice","volume":"107","author":"Ueno","year":"2010","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2022101813193536500_CIT0046","doi-asserted-by":"crossref","first-page":"20959","DOI":"10.1073\/pnas.1116531109","article-title":"Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains","volume":"108","author":"Uraguchi","year":"2011","journal-title":"Proceedings of the National Academy of Sciences,"},{"key":"2022101813193536500_CIT0047","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s11033-016-3950-x","article-title":"In silico analysis of Mn transporters (NRAMP1) in various plant species","volume":"43","author":"Vatansever","year":"2016","journal-title":"Molecular Biology Reports"},{"key":"2022101813193536500_CIT0048","doi-asserted-by":"crossref","first-page":"W430","DOI":"10.1093\/nar\/gkw306","article-title":"RaptorX-Property: a web server for protein structure property prediction","volume":"44","author":"Wang","year":"2016","journal-title":"Nucleic Acids Research"},{"key":"2022101813193536500_CIT0049","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.3389\/fpls.2019.01081","article-title":"Mutation at different sites of metal transporter gene OsNramp5 affects Cd accumulation and related agronomic traits in rice (Oryza sativa L.)","volume":"10","author":"Wang","year":"2019","journal-title":"Frontiers in Plant Science"},{"key":"2022101813193536500_CIT0050","first-page":"149","author":"WHO","year":"2011"},{"key":"2022101813193536500_CIT0051","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1104\/pp.113.216564","article-title":"Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2","volume":"162","author":"Yamaji","year":"2013","journal-title":"Plant Physiology"},{"key":"2022101813193536500_CIT0052","doi-asserted-by":"crossref","first-page":"4849","DOI":"10.1093\/jxb\/eru259","article-title":"OsNRAMP5 contributes to manganese translocation and distribution in rice shoots","volume":"65","author":"Yang","year":"2014","journal-title":"Journal of Experimental Botany"},{"key":"2022101813193536500_CIT0053","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1126\/science.1128186","article-title":"Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster","volume":"314","author":"Yano","year":"2006","journal-title":"Science"},{"key":"2022101813193536500_CIT0054","doi-asserted-by":"crossref","first-page":"2302","DOI":"10.1093\/nar\/gki524","article-title":"TM-align: a protein structure alignment algorithm based on the TM-score","volume":"33","author":"Zhang","year":"2005","journal-title":"Nucleic Acids Research"},{"key":"2022101813193536500_CIT0055","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11104-019-04374-6","article-title":"Arsenic and cadmium accumulation in rice and mitigation strategies","volume":"446","author":"Zhao","year":"2020","journal-title":"Plant and Soil"}],"container-title":["Journal of Experimental Botany"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jxb\/advance-article-pdf\/doi\/10.1093\/jxb\/erac302\/45479820\/erac302.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jxb\/article-pdf\/73\/18\/6475\/46559157\/erac302.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jxb\/article-pdf\/73\/18\/6475\/46559157\/erac302.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,18]],"date-time":"2022-10-18T09:27:27Z","timestamp":1666085247000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jxb\/article\/73\/18\/6475\/6631284"}},"subtitle":[],"editor":[{"given":"Karl-Josef","family":"Dietz","sequence":"additional","affiliation":[{"name":"Bielefeld University , Germany"}],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,7,5]]},"references-count":55,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2022,7,5]]},"published-print":{"date-parts":[[2022,10,18]]}},"URL":"https:\/\/doi.org\/10.1093\/jxb\/erac302","relation":{},"ISSN":["0022-0957","1460-2431"],"issn-type":[{"value":"0022-0957","type":"print"},{"value":"1460-2431","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,10,18]]},"published":{"date-parts":[[2022,7,5]]}}}