Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize

Background and aims Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are unknown. The aims of this study were to compare Cd uptake, translocation and influx kinetics between rice, wheat and maize and to investigate...

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Published inPlant and soil Vol. 433; no. 1/2; pp. 377 - 389
Main Authors Sui, Fu-Qing, Chang, Jia-Dong, Tang, Zhong, Liu, Wen-Ju, Huang, Xin-Yuan, Zhao, Fang-Jie
Format Journal Article
LanguageEnglish
Published Cham Springer 01.12.2018
Springer International Publishing
Springer Nature B.V
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Abstract Background and aims Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are unknown. The aims of this study were to compare Cd uptake, translocation and influx kinetics between rice, wheat and maize and to investigate whether the expression and functionality of Nramp5 genes differ between the three crop species. Methods Two cultivars each of rice, wheat and maize were grown hydroponically and exposed to a range of Cd concentrations. Nramp5 genes were cloned from the three plants and their expression levels determined. The Cd transport activities of Nramp5 proteins were tested in yeast. Results Under hydroponic conditions, Cd uptake in rice was 2.5–8.1 and 1.1–3.6 times that of wheat and maize, respectively. The maximum Cd influx velocity of rice was 6.5 and 2.2 times that in wheat and maize, respectively. Wheat showed the lowest Cd uptake but the highest Cd root-to-shoot translocation. The absolute expression level of OsNramp5 in rice roots was 4–5 times that of TaNramp5A and TaNramp5D in wheat or ZmNramp5 in maize. All Nramp5 proteins were localized to the plasma membrane. When expressed in yeast, OsNramp5 showed a greater Cd transport activity than wheat or maize Nramp5. Conclusions Rice has a greater Cd uptake ability than wheat or maize, likely because OsNramp5 is more highly expressed and the protein has a higher Cd transport activity than wheat or maize Nramp5.
AbstractList Background and aimsCereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are unknown. The aims of this study were to compare Cd uptake, translocation and influx kinetics between rice, wheat and maize and to investigate whether the expression and functionality of Nramp5 genes differ between the three crop species.MethodsTwo cultivars each of rice, wheat and maize were grown hydroponically and exposed to a range of Cd concentrations. Nramp5 genes were cloned from the three plants and their expression levels determined. The Cd transport activities of Nramp5 proteins were tested in yeast.ResultsUnder hydroponic conditions, Cd uptake in rice was 2.5–8.1 and 1.1–3.6 times that of wheat and maize, respectively. The maximum Cd influx velocity of rice was 6.5 and 2.2 times that in wheat and maize, respectively. Wheat showed the lowest Cd uptake but the highest Cd root-to-shoot translocation. The absolute expression level of OsNramp5 in rice roots was 4–5 times that of TaNramp5A and TaNramp5D in wheat or ZmNramp5 in maize. All Nramp5 proteins were localized to the plasma membrane. When expressed in yeast, OsNramp5 showed a greater Cd transport activity than wheat or maize Nramp5.ConclusionsRice has a greater Cd uptake ability than wheat or maize, likely because OsNramp5 is more highly expressed and the protein has a higher Cd transport activity than wheat or maize Nramp5.
Background and aims Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are unknown. The aims of this study were to compare Cd uptake, translocation and influx kinetics between rice, wheat and maize and to investigate whether the expression and functionality of Nramp5 genes differ between the three crop species. Methods Two cultivars each of rice, wheat and maize were grown hydroponically and exposed to a range of Cd concentrations. Nramp5 genes were cloned from the three plants and their expression levels determined. The Cd transport activities of Nramp5 proteins were tested in yeast. Results Under hydroponic conditions, Cd uptake in rice was 2.5–8.1 and 1.1–3.6 times that of wheat and maize, respectively. The maximum Cd influx velocity of rice was 6.5 and 2.2 times that in wheat and maize, respectively. Wheat showed the lowest Cd uptake but the highest Cd root-to-shoot translocation. The absolute expression level of OsNramp5 in rice roots was 4–5 times that of TaNramp5A and TaNramp5D in wheat or ZmNramp5 in maize. All Nramp5 proteins were localized to the plasma membrane. When expressed in yeast, OsNramp5 showed a greater Cd transport activity than wheat or maize Nramp5. Conclusions Rice has a greater Cd uptake ability than wheat or maize, likely because OsNramp5 is more highly expressed and the protein has a higher Cd transport activity than wheat or maize Nramp5.
Background and aims Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are unknown. The aims of this study were to compare Cd uptake, translocation and influx kinetics between rice, wheat and maize and to investigate whether the expression and functionality of Nramp5 genes differ between the three crop species. Methods Two cultivars each of rice, wheat and maize were grown hydroponically and exposed to a range of Cd concentrations. Nramp5 genes were cloned from the three plants and their expression levels determined. The Cd transport activities of Nramp5 proteins were tested in yeast. Results Under hydroponic conditions, Cd uptake in rice was 2.5–8.1 and 1.1–3.6 times that of wheat and maize, respectively. The maximum Cd influx velocity of rice was 6.5 and 2.2 times that in wheat and maize, respectively. Wheat showed the lowest Cd uptake but the highest Cd root-to-shoot translocation. The absolute expression level of OsNramp5 in rice roots was 4–5 times that of TaNramp5A and TaNramp5D in wheat or ZmNramp5 in maize. All Nramp5 proteins were localized to the plasma membrane. When expressed in yeast, OsNramp5 showed a greater Cd transport activity than wheat or maize Nramp5. Conclusions Rice has a greater Cd uptake ability than wheat or maize, likely because OsNramp5 is more highly expressed and the protein has a higher Cd transport activity than wheat or maize Nramp5.
Author Chang, Jia-Dong
Tang, Zhong
Liu, Wen-Ju
Zhao, Fang-Jie
Sui, Fu-Qing
Huang, Xin-Yuan
Author_xml – sequence: 1
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  givenname: Xin-Yuan
  surname: Huang
  fullname: Huang, Xin-Yuan
– sequence: 6
  givenname: Fang-Jie
  surname: Zhao
  fullname: Zhao, Fang-Jie
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Issue 1/2
Keywords Cadmium
Maize
Nramp5
Wheat
Uptake
Rice
Language English
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PublicationSubtitle An International Journal on Plant-Soil Relationships
PublicationTitle Plant and soil
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Springer International Publishing
Springer Nature B.V
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EhrnstorferIAGeertsmaERPardonESteyaertJDutzlerRCrystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transportNat Struct Mol Biol2014219909961:CAS:528:DC%2BC2cXhslOisrjP10.1038/nsmb.2904
UraguchiSKamiyaTSakamotoTKasaiKSatoYNagamuraYYoshidaAKyozukaJIshikawaSFujiwaraTLow-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grainsProc Natl Acad Sci U S A201110820959209641:CAS:528:DC%2BC38XnvVCqsw%3D%3D10.1073/pnas.1116531109
IshimaruYTakahashiRBashirKShimoHSenouraTSugimotoKOnoKYanoMIshikawaSAraoTNakanishiHNishizawaNKCharacterizing the role of rice NRAMP5 in manganese, iron and cadmium transportSci Rep2012228610.1038/srep00286
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TangLMaoBLiYLvQZhangLChenCHeHWangWZengXShaoYPanYHuYPengYFuXLiHXiaSZhaoBKnockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yieldSci Rep2017710.1038/s41598-017-14832-9
Satoh-NagasawaNMoriMNakazawaNKawamotoTNagatoYSakuraiKTakahashiHWatanabeAAkagiHMutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmiumPlant Cell Physiol2012532132241:CAS:528:DC%2BC38XosFGksw%3D%3D10.1093/pcp/pcr166
SasakiAYamajiNYokoshoKMaJFNramp5 is a major transporter responsible for manganese and cadmium uptake in ricePlant Cell201224215521671:CAS:528:DC%2BC38XhtVOktbzP10.1105/tpc.112.096925
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ZhuHHChenCXuCZhuQHHuangDYEffects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical ChinaEnviron Pollut2016219991061:CAS:528:DC%2BC28XhslGrtbfE10.1016/j.envpol.2016.10.043
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References_xml – reference: European Food Safety AuthorityCadmium dietary exposure in the European populationEFSA J2012102551258810.2903/j.efsa.2012.2551
– reference: IshikawaSIshimaruYIguraMKuramataMAbeTSenouraTHaseYAraoTNishizawaNKNakanishiHIon-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium riceProc Natl Acad Sci U S A201210919166191711:CAS:528:DC%2BC38XhvVagtrjN10.1073/pnas.1211132109
– reference: IARC (International Agency for Research on Cancer) (1993) Beryllium, cadmium, mercury and exposures in the glass manufacturing industry. IARC monographs on the evaluation of carcinogenic risk of chemicals to humans, vol. 58. L. IARC, Lyon, France. 444 p
– reference: YanJLWangPTWangPYangMLianXMTangZHuangCFSaltDEZhaoFJA loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of japonica rice cultivarsPlant Cell Environ201639194119541:CAS:528:DC%2BC28Xhtlamt7zE10.1111/pce.12747
– reference: MiyadateHAdachiSHiraizumiATezukaKNakazawaNKawamotoTKatouKKodamaISakuraiKTakahashiHSatoh-NagasawaNWatanabeAFujimuraTAkagiHOsHMA3, a P-1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuolesNew Phytol20111891901991:CAS:528:DC%2BC3MXltlGgtQ%3D%3D10.1111/j.1469-8137.2010.03459.x
– reference: LuoJ-SHuangJZengD-LPengJ-SZhangG-BMaH-LGuanYYiH-YFuY-LHanBLinH-XQianQGongJ-MA defensin-like protein drives cadmium efflux and allocation in riceNat Commun2018964510.1038/s41467-018-03088-0
– reference: SongYWangYMaoWSuiHYongLYangDJiangDZhangLGongYDietary cadmium exposure assessment among the Chinese populationPLoS One201712e017797810.1371/journal.pone.0177978
– reference: HartJJWelchRMNorvellWAClarkeJMKochianLVZinc effects on cadmium accumulation and partitioning in near-isogenic lines of durum wheat that differ in grain cadmium concentrationNew Phytol20051673914011:CAS:528:DC%2BD2MXpt1ersLs%3D10.1111/j.1469-8137.2005.01416.x
– reference: Joint FAO/WHO Expert Committee on Food Additives (2010) Joint FAO/WHO Expert Committee on Food Additives seventy-third meeting, http://www.who.int/foodsafety/publications/chem/summary73.pdf. World Health Organization, Geneva
– reference: ZhuHHChenCXuCZhuQHHuangDYEffects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical ChinaEnviron Pollut2016219991061:CAS:528:DC%2BC28XhslGrtbfE10.1016/j.envpol.2016.10.043
– reference: YangMZhangYYZhangLHuJZhangXLuKDongHWangDZhaoFJHuangCFLianXMOsNRAMP5 contributes to manganese translocation and distribution in rice shootsJ Exp Bot201465484948611:CAS:528:DC%2BC2MXitl2gtbg%3D10.1093/jxb/eru259
– reference: UenoDYamajiNKonoIHuangCFAndoTYanoMMaJFGene limiting cadmium accumulation in riceProc Natl Acad Sci U S A201010716500165051:CAS:528:DC%2BC3cXht1WrsrzN10.1073/pnas.1005396107
– reference: ClemensSAartsMGMThomineSVerbruggenNPlant science: the key to preventing slow cadmium poisoningTrends Plant Sci20131892991:CAS:528:DC%2BC38XhtlGqt7%2FK10.1016/j.tplants.2012.08.003
– reference: European Food Safety AuthorityScientific opinion of the panel on contaminants in the food chain on a request from the European Commission on cadmium in foodEFSA J20099801139
– reference: SasakiAYamajiNYokoshoKMaJFNramp5 is a major transporter responsible for manganese and cadmium uptake in ricePlant Cell201224215521671:CAS:528:DC%2BC38XhtVOktbzP10.1105/tpc.112.096925
– reference: WangPKopittkePMMcGrathSPZhaoFJSinghBRMcLaughlinMJBrevikECadmium transfer from soil to plants and its potential risk to human healthThe Nexus of soils, plants, animals and human health2017StuttgartCatena- Schweizerbart138147
– reference: IshimaruYTakahashiRBashirKShimoHSenouraTSugimotoKOnoKYanoMIshikawaSAraoTNakanishiHNishizawaNKCharacterizing the role of rice NRAMP5 in manganese, iron and cadmium transportSci Rep2012228610.1038/srep00286
– reference: TamuraKStecherGPetersonDFilipskiAKumarSMEGA6: molecular evolutionary genetics analysis version 6.0Mol Biol Evol201330272527291:CAS:528:DC%2BC3sXhvVKhurzP10.1093/molbev/mst197
– reference: TakahashiRIshimaruYSenouraTShimoHIshikawaSAraoTNakanishiHNishizawaNKThe OsNRAMP1 iron transporter is involved in Cd accumulation in riceJ Exp Bot201162484348501:CAS:528:DC%2BC3MXhtlejsrbP10.1093/jxb/err136
– reference: ChaneyRLHow does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmersCurrent Pollut Rep2015113221:CAS:528:DC%2BC2sXpt1Smt7c%3D10.1007/s40726-015-0002-4
– reference: WatanabeTZhangZWMoonCSShimboSNakatsukaHMatsuda-InoguchiNHigashikawaKIkedaMCadmium exposure of women in general populations in Japan during 1991-1997 compared with 1977-1981Int Arch Occup Environ Health20007326341:CAS:528:DC%2BD3cXht1Cmtr4%3D10.1007/PL00007934
– reference: UraguchiSMoriSKuramataMKawasakiAAraoTIshikawaSRoot-to-shoot cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in riceJ Exp Bot200960267726881:CAS:528:DC%2BD1MXntlGisb8%3D10.1093/jxb/erp119
– reference: TangLMaoBLiYLvQZhangLChenCHeHWangWZengXShaoYPanYHuYPengYFuXLiHXiaSZhaoBKnockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yieldSci Rep2017710.1038/s41598-017-14832-9
– reference: TangZCaiHLiJLvYZhangWZhaoFJAllelic variation of NtNramp5 associated with cultivar variation in cadmium accumulation in tobaccoPlant Cell Physiol201758158315931:CAS:528:DC%2BC1cXhs1Kqs7fJ10.1093/pcp/pcx087
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Snippet Background and aims Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are...
Background and aims Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are...
Background and aimsCereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are...
BACKGROUND AND AIMS: Cereals are the main dietary source of cadmium (Cd). Rice grains often contain higher levels of Cd than other cereals, but the reasons are...
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SubjectTerms Biomedical and Life Sciences
Cadmium
Cereals
Corn
crops
Cultivars
Ecology
Gene expression
Genes
Hydroponics
Life Sciences
Oryza
Plant Physiology
Plant Sciences
plasma membrane
Proteins
Regular Article
Rice
roots
Soil Science & Conservation
Translocation
Transport
Triticum
Wheat
Yeast
yeasts
Zea mays
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Title Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize
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