Absorption of cadmium accompanied by EDTA varies according to tomato cultivar
Shouping Zhao A , Qi Zhang A , Wendan Xiao A , De Chen A and Xuezhu Ye A B
+ Author Affiliations
- Author Affiliations
A Institute of Quality and Standard for Agro-products, Zhejiang Academy of Agricultural Sciences, State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Key Laboratory of Information Traceability for Agricultural Products, Ministry of Agriculture of China, Hangzhou, Zhejiang, 310021, China.
B Corresponding author. Email: rosecomepaper@163.com
Crop and Pasture Science 70(11) 981-989 https://doi.org/10.1071/CP19130
Submitted: 10 April 2019 Accepted: 23 August 2019 Published: 21 November 2019
Abstract
Two tomato (Lycopersicum solanum) varieties, one high (YSL189) and one low (HZ903) cadmium (Cd) accumulator, were used in our experiment. We detected cadmium (Cd ion/Cd-EDTA) uptake rates in roots and the corresponding expression of the Cd transport genes IRT1, IRT2, ZIP, Nramp1, Nramp2 and Nramp3. Our data proved that both cultivars – YSL189 and HZ903 – showed higher Cd accumulation in plants and a higher Cd uptake rate in roots supplied with Cd ion than with Cd-EDTA. In roots of YSL189, the expression levels of IRT1, IRT2, ZIP, Nramp1, Nramp3 and Nramp2 (5, 10 and 20 µmolc L–1 Cd) treated with Cd ion were higher than those treated with Cd-EDTA, whereas in roots of HZ903, only two genes, IRT1 and Nramp1 (5, 10, 100 µmolc L–1 Cd), showed higher expression levels in plants treated with Cd ion than in those treated with Cd-EDTA. When the difference between the cultivars was considered, the Cd concentration in the plant and the Cd uptake rate in the roots of YSL189 were higher than those of YZ903 under the same Cd treatments (i.e. Cd ion or Cd-EDTA). The expression of IRT2 and ZIP in the roots of YSL189 was higher than that observed in HZ903 treated with all levels of ion-Cd. We attribute the higher Cd uptake rate and greater accumulation of ion-Cd compared with EDTA-Cd in YSL189 than those found in HZ903 partly to the genes that had higher expression levels. Our results indicate that the roles of transporters in the absorption of different forms of Cd vary according to plant genotype.
Additional keyword: absorption, cadmium forms, transporter.
References
Chaffai R, Koyama H (2011) Chapter 1 – Heavy metal tolerance in Arabidopsis thaliana. Advances in Botanical Research 60, 1–49.| Chapter 1 – Heavy metal tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Cherif J, Derbel N, Nakkach M, Bergmann H, Jemal F, Lakhdar ZB (2012) Spectroscopic studies of photosynthetic responses of tomato plants to the interaction of zinc and cadmium toxicity. Journal of Photochemistry and Photobiology. B, Biology 111, 9–16.
| Spectroscopic studies of photosynthetic responses of tomato plants to the interaction of zinc and cadmium toxicity.Crossref | GoogleScholarGoogle Scholar | 22520862PubMed |
Conn S, Gilliham M (2010) Comparative physiology of elemental distributions in plants. Annals of Botany 105, 1081–1102.
| Comparative physiology of elemental distributions in plants.Crossref | GoogleScholarGoogle Scholar | 20410048PubMed |
Delpérée C, Lutts S (2008) Growth inhibition occurs independently of cell mortality in tomato (Solanum lycopersicum) exposed to high cadmium concentrations. Journal of Integrative Plant Biology 50, 300–310.
| Growth inhibition occurs independently of cell mortality in tomato (Solanum lycopersicum) exposed to high cadmium concentrations.Crossref | GoogleScholarGoogle Scholar | 18713362PubMed |
Fu XP, Dou CM, Chen YX, Chen XC, Shi JY, Yu MG (2011) Subcellular distribution and chemical forms of cadmium in Phytolacca americana. Journal of Hazardous Materials 186, 103–107.
| Subcellular distribution and chemical forms of cadmium in Phytolacca americana.Crossref | GoogleScholarGoogle Scholar |
Ghasemi E, Heydari A, Sillanpää M (2017) Superparamagnetic Fe3O4-EDTA nanoparticles as an efficient adsorbent for simultaneous removal of Ag(I), Hg(II), Mn(II), Zn(II), Pb(II) and Cd(II) from water and soil environmental samples. Microchemical Journal 131, 51–56.
| Superparamagnetic Fe3O4-EDTA nanoparticles as an efficient adsorbent for simultaneous removal of Ag(I), Hg(II), Mn(II), Zn(II), Pb(II) and Cd(II) from water and soil environmental samples.Crossref | GoogleScholarGoogle Scholar |
Gu YY, Yeung AT, Li HJ (2017) Enhanced electrokinetic remediation of cadmium-contaminated natural clay using organophosphonates in comparison with EDTA. Chinese Journal of Chemical Engineering 26, 1152–1159.
| Enhanced electrokinetic remediation of cadmium-contaminated natural clay using organophosphonates in comparison with EDTA.Crossref | GoogleScholarGoogle Scholar |
Hong CO, Chung DY, Lee DK, Kim PJ (2010) Comparison of phosphate materials for immobilizing cadmium in soil. Archives of Environmental Contamination and Toxicology 58, 268–274.
| Comparison of phosphate materials for immobilizing cadmium in soil.Crossref | GoogleScholarGoogle Scholar | 19633979PubMed |
Huang YX, Arturo AK (2015) EDTA functionalized magnetic nanoparticle sorbents for cadmium and lead contaminated water treatment. Water Research 80, 159–168.
| EDTA functionalized magnetic nanoparticle sorbents for cadmium and lead contaminated water treatment.Crossref | GoogleScholarGoogle Scholar |
Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa N (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Scientific Reports 2, 286
| Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport.Crossref | GoogleScholarGoogle Scholar | 22368778PubMed |
Kovács K, Kuzmann E, Vértes A, Lévai L, Cseh E, Fodor F (2010) Effect of cadmium on iron uptake in cucumber roots: a Mössbauer-spectroscopic study. Plant and Soil 327, 49–56.
| Effect of cadmium on iron uptake in cucumber roots: a Mössbauer-spectroscopic study.Crossref | GoogleScholarGoogle Scholar |
Lee S, An G (2009) Overexpression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant, Cell & Environment 32, 408–416.
| Overexpression of OsIRT1 leads to increased iron and zinc accumulations in rice.Crossref | GoogleScholarGoogle Scholar |
Li Z, Wu LH, Luo Y, Peter C (2018) Changes in metal mobility assessed by EDTA kinetic extraction in three polluted soils after repeated phytoremediation using a cadmium/zinc hyperaccumulator. Chemosphere 194, 432–440.
| Changes in metal mobility assessed by EDTA kinetic extraction in three polluted soils after repeated phytoremediation using a cadmium/zinc hyperaccumulator.Crossref | GoogleScholarGoogle Scholar | 29227891PubMed |
Luo BF, Shao TD, Lu KX, Liu WJ, Lin XY, Jin CW (2012) Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants. Journal of Experimental Botany 63, 3127–3136.
| Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants.Crossref | GoogleScholarGoogle Scholar | 22378950PubMed |
Meighan MM, Fenus T, Karey E, MacNeil J (2011) The impact of EDTA on the rate of accumulation and root/shoot partitioning of cadmium in mature dwarf sunflowers. Chemosphere 83, 1539–1545.
| The impact of EDTA on the rate of accumulation and root/shoot partitioning of cadmium in mature dwarf sunflowers.Crossref | GoogleScholarGoogle Scholar | 21306756PubMed |
Milner MJ (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. Journal of Experimental Botany 64, 369–381.
| Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis.Crossref | GoogleScholarGoogle Scholar | 23264639PubMed |
Monteiro CC, Carvalho RF, Gratão PL, Carvalho G, Tezotto T, Medici LO, Peres LE, Azevedo RA (2011) Biochemical responses of the ethylene-insensitive Never ripe tomato mutant subjected to cadmium and sodium stresses. Environmental and Experimental Botany 71, 306–320.
| Biochemical responses of the ethylene-insensitive Never ripe tomato mutant subjected to cadmium and sodium stresses.Crossref | GoogleScholarGoogle Scholar |
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Science and Plant Nutrition 52, 464–469.
| Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice.Crossref | GoogleScholarGoogle Scholar |
Peng F, Wang C, Cheng Y, Zeng J, Kang H, Fan X, Sha L, Zhang H, Zhou Y, Wang Y (2018a) Cloning and characterization of TpNRAMP3, a metal transporter from Polish wheat (Triticum polonicum L.). Frontiers in Plant Science 9, 1354
| Cloning and characterization of TpNRAMP3, a metal transporter from Polish wheat (Triticum polonicum L.).Crossref | GoogleScholarGoogle Scholar | 30294336PubMed |
Peng F, Wang C, Zhu J, Zeng J, Kang H, Fan X, Sha L, Zhang H, Zhou Y, Wang Y (2018b) Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 247, 1395–1406.
| Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 29523961PubMed |
Polettini A, Pomi R, Rolle E (2007) The effect of operating variables on chelant-assisted remediation of contaminated dredged sediment. Chemosphere 66, 866–877.
| The effect of operating variables on chelant-assisted remediation of contaminated dredged sediment.Crossref | GoogleScholarGoogle Scholar | 16860848PubMed |
Pottier M, Oomen R, Picco C, Giraudat J, Scholz-Starke J, Richaud P, Carpaneto A, Thomine S (2015) Identification of mutations allowing natural resistance associated macrophage proteins (NRAMP) to discriminate against cadmium. The Plant Journal 83, 625–637.
| Identification of mutations allowing natural resistance associated macrophage proteins (NRAMP) to discriminate against cadmium.Crossref | GoogleScholarGoogle Scholar | 26088788PubMed |
Radhouane C, Hiroyuki K (2011) Ch 1 - Heavy metal tolerance in Arabidopsis thaliana. Advances in Botanical Research 60, 1–49.
Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proceedings of the National Academy of Sciences of the United States of America 97, 12356–12360.
| Altered selectivity in an Arabidopsis metal transporter.Crossref | GoogleScholarGoogle Scholar | 11035780PubMed |
Saifullah ME, Qadir M, Caritat P, Tack FMG, Du-Laing G, Zia MH (2009) EDTA-assisted phytoextraction. Chemosphere 74, 1279–1291.
| EDTA-assisted phytoextraction.Crossref | GoogleScholarGoogle Scholar |
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. The Plant Cell 24, 2155–2167.
| Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice.Crossref | GoogleScholarGoogle Scholar | 22589467PubMed |
Seregin IV, Kozhevnikova AD (2008) Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 55, 1–22.
| Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium.Crossref | GoogleScholarGoogle Scholar |
Shibata M, Konno T, Akaike R, Xu Y, Shen R, Ma JF (2007) Phytoremediation of Pb contaminated soil with polymer-coated EDTA. Plant and Soil 290, 201–208.
| Phytoremediation of Pb contaminated soil with polymer-coated EDTA.Crossref | GoogleScholarGoogle Scholar |
Smeets K, Ruytinx J, Semane B, Belleghem FV, Remans T, Sanden SV, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environmental and Experimental Botany 63, 1–8.
| Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Su G, Li F, Lin J, Liu C, Shi G (2013) Peanut as a potential crop for bioenergy production via Cd-phytoextraction: a life-cycle pot experiment. Plant and Soil 365, 337–345.
| Peanut as a potential crop for bioenergy production via Cd-phytoextraction: a life-cycle pot experiment.Crossref | GoogleScholarGoogle Scholar |
Tan L, Zhu Y, Fan T, Peng C, Wang J, Sun L, Chen C (2019) OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice. Biochemical and Biophysical Research Communications 512, 112–118.
| OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice.Crossref | GoogleScholarGoogle Scholar | 30871778PubMed |
Tang M, Mao D, Xu L, Li D, Song S, Chen C (2014) Integrated analysis of miRNA and mRNA expression profiles in response to Cd exposure in rice seedlings. BMC Genomics 15, 835
| Integrated analysis of miRNA and mRNA expression profiles in response to Cd exposure in rice seedlings.Crossref | GoogleScholarGoogle Scholar | 25273267PubMed |
Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, He H, Wang W, Zeng X, Shao Y, Pan Y, Hu Y, Peng Y, Fu X, Li H, Xia S, Zhao B (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Scientific Reports 7, 14438
| Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield.Crossref | GoogleScholarGoogle Scholar | 29089547PubMed |
Tezotto T, Favarin JL, Azevedo RA, Alleoni LRF, Mazzafera P (2012) Coffee is highly tolerant to cadmium, nickel and zinc: plant and soil nutritional status, metal distribution and bean yield. Field Crops Research 125, 25–34.
| Coffee is highly tolerant to cadmium, nickel and zinc: plant and soil nutritional status, metal distribution and bean yield.Crossref | GoogleScholarGoogle Scholar |
Wang X, Liu Y, Zeng G, Chai L, Song X, Min Z (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Gaud. Environmental and Experimental Botany 62, 389–395.
| Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Gaud.Crossref | GoogleScholarGoogle Scholar |
Wang C, Chen X, Yao Q, Long D, Fan X, Kang HY, Zeng J, Sha L, Zhang HQ, Zhou YH, Wang Y (2019) Overexpression of TtNRAMP6 enhances the accumulation of Cd in Arabidopsis. Gene 696, 225–232.
| Overexpression of TtNRAMP6 enhances the accumulation of Cd in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30769144PubMed |
Weber M, Harada E, Vess C, Roepenack-Lahaye EV, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. The Plant Journal 37, 269–281.
| Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors.Crossref | GoogleScholarGoogle Scholar | 14690510PubMed |
Weng B, Xie X, Weiss DJ, Liu J, Lu H, Yan C (2012) Kandelia obovata (S., L.) Yong tolerance mechanisms to cadmium: subcellular distribution, chemical forms and thiol pools. Marine Pollution Bulletin 64, 2453–2460.
| Kandelia obovata (S., L.) Yong tolerance mechanisms to cadmium: subcellular distribution, chemical forms and thiol pools.Crossref | GoogleScholarGoogle Scholar | 22910331PubMed |
Wu D, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Ma JF (2016) The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiology 172, 1899–1910.
| The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron.Crossref | GoogleScholarGoogle Scholar | 27621428PubMed |
Wu X, Zhu ZB, Chen JH, Huang YF, Liu ZL, Zou JW, Chen YH, Su NN, Jin C (2019) Transcriptome analysis revealed pivotal transporters involved in the reduction of cadmium accumulation in pak choi (Brassica chinensis L.) by exogenous hydrogen-rich water. Chemosphere 216, 684–697.
| Transcriptome analysis revealed pivotal transporters involved in the reduction of cadmium accumulation in pak choi (Brassica chinensis L.) by exogenous hydrogen-rich water.Crossref | GoogleScholarGoogle Scholar | 30391890PubMed |
Xu WH, Li HG, He JP, Ma QF, Zhang XJ, Chen GQ, Wang HX, Zhang HB (2010) Cd uptake in rice cultivars treated with organic acids and EDTA. Journal of Environmental Sciences 22, 441–447.
| Cd uptake in rice cultivars treated with organic acids and EDTA.Crossref | GoogleScholarGoogle Scholar |
Yamaji N, Sasaki A, Xia J, Yokosho K, Ma J (2013) A node-based switch for preferential distribution of manganese in rice. Nature Communications 4, 2442
| A node-based switch for preferential distribution of manganese in rice.Crossref | GoogleScholarGoogle Scholar | 24048172PubMed |
Yang M, Zhang W, Dong H, Zhang Y, Lv K, Wang D, Lian X (2013) OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice. PLoS One 8, e83990
| OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice.Crossref | GoogleScholarGoogle Scholar | 24391994PubMed |
Yang Y, Xiong J, Chen R, Fu G, Chen T, Tao L (2016) Excessive nitrate enhances cadmium (Cd) uptake by up-regulating the expression of OsIRT1 in rice (Oryza sativa). Environmental and Experimental Botany 122, 141–149.
| Excessive nitrate enhances cadmium (Cd) uptake by up-regulating the expression of OsIRT1 in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |
Yang CH, Zhang Y, Huang CF (2019) Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5. Journal of Integrative Agriculture 18, 688–697.
| Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5.Crossref | GoogleScholarGoogle Scholar |
Zhao SP, Zhao XQ, Li SM, Shi WM (2006) Optimization and application of real-time PCR (RT-PCR) method for detecting nitrogen assimilation related genes expression levels in rice (Oryza sativa). Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 53, 560–569.
| Optimization and application of real-time PCR (RT-PCR) method for detecting nitrogen assimilation related genes expression levels in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |
Zhao SP, Zhang YZ, Ye XZ, Zhang Q, Xiao WD (2015) Responses to cadmium stress in two tomato genotypes differing in heavy metal accumulation. Turkish Journal of Botany 39, 615–624.
| Responses to cadmium stress in two tomato genotypes differing in heavy metal accumulation.Crossref | GoogleScholarGoogle Scholar |
