Abstract
Aims
The contribution of sulphur (S)-induced responses to chromium (Cr) tolerance of rice plants is not yet fully elucidated. It is hypothesised that S nutrition mitigates the accumulation and toxicity of Cr through enhanced formation of iron plaque (IP) and S-containing chelators. This study aimed to investigate the responses of iron (Fe) and Cr availability and transfer in the hydroponic rice system to added S levels.
Methods
We explored the influence of S nutrition on Cr accumulation in rice under a combination of Cr (VI) (+Cr, –Cr) and S (0, 1.75, 3.5, 7 mM) treatments.
Results
S additions at rates of 1.75 and 3.5 mM gave the least decline in root and shoot growth of rice seedlings under Cr stress. Fe concentration in shoots was consistent with the level of Cr uptake. The subcellular distribution of Cr in roots and shoots differed with varying S supply levels. Our results also revealed that S treatment at a moderate level (3.5 mM) was more effective in suppressing the bioavailability of Cr in rice shoots than were the other levels.
Conclusions
S-induced reduction in shoot Cr concentration, particularly from 1.75 to 3.5 mM, was likely attributed to the enhanced biosynthesis of glutathione (GSH) and phytochelatins (PCs) in roots than the enhanced physical resistance of IP induced by S. The poor barrier capacity of IP to Cr absorption in rice plants primarily ascribed to the level of applied Cr concentration and partly to the competition between Cr and S at the absorbing sites.
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References
Aghajanzadeh TA, Reich M, Hawkesford MJ, Burow M (2019) Sulfur metabolism in Allium cepa is hardly affected by chloride and sulfate salinity. Arch Agron Soil Sci 65(7):945–956. https://doi.org/10.1080/03650340.2018.1540037
Amaral DC, Lopes G, Guilherme LRG, Seyferth AL (2017) A new approach to sampling intact Fe plaque reveals Si-induced changes in Fe mineral composition and shoot as in rice. Environ Sci Technol 51:38–45. https://doi.org/10.1021/acs.est.6b03558
Andrews M, Raven JA, Sprent J (2001) Environmental effects on dry matter partitioning between shoot and root of crop plants: relations with growth and shoot protein concentration. Ann Appl Biol 138(1):57–68. https://doi.org/10.1111/j.1744-7348.2001.tb00085.x
Andrews M, Raven JA, Lea PJ, Sprent JI (2006) A role for shoot protein in shoot–root dry matter allocation in higher plants. Ann Bot 97(1):3–10. https://doi.org/10.1093/aob/mcj009
Anjum NA, Umar S, Singh S, Nazar R, Khan NA (2008) Sulphur assimilation and cadmium tolerance in plants. In: Khan NA, Singh S, Umar S (eds) Abiotic stress and Sulphur assimilation in plants. Springer-Verlag, Berlin, pp 271–302
Bashir K, Nishizawa NK (2006) Deoxymugineic acid synthase; a gene important for Fe-acquisition and homeostasis. Plant Signal Behav 1:290–292. https://doi.org/10.4161/psb.1.6.3590
Bashir K, Ishimaru Y, Nishizawa NK (2010) Iron uptake and loading into rice grains. Rice 3:122–130. https://doi.org/10.1007/s12284-010-9042-y
Bazrkar-Khatibani L, Fakheri BA, Hosseini-Chaleshtori M, Mahender A, Mahdinejad N, Ali J (2019) Genetic mapping and validation of quantitative trait loci (QTL) for the grain appearance and quality traits in rice (Oryza sativa L.) by using recombinant inbred line (RIL) population. Int J Genomics 2019:3160275. https://doi.org/10.1155/2019/3160275
Blum R, Meyer KC, Wünschmann J, Lendzian KJ, Grill E (2010) Cytosolic action of phytochelatin synthase. Plant Physiol 153:159–169. https://doi.org/10.1104/pp.109.149922
Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20:33–40. https://doi.org/10.1016/j.tplants.2014.07.005
Cambui CA, Svennerstam H, Gruffman L, Nordin A, Ganeteg U, Näsholm T (2011) Patterns of plant biomass partitioning depend on nitrogen source. PLoS One 6(4):e19211. https://doi.org/10.1371/journal.pone.0019211
Cao ZZ, Qin ML, Lin XY, Zhu ZW, Chen MX (2018) Sulfur supply reduces cadmium uptake and translocation in rice grains (Oryza sativa L.) by enhancing iron plaque formation, cadmium chelation an vacuolar sequestration. Environ Pollut 238:76–84. https://doi.org/10.1016/j.envpol.2018.02.083
Carciochi WD, Divito GA, Fernández LA, Echeverría HE (2017) Sulfur affects root growth and improves nitrogen recovery and internal efficiency in wheat. J Plant Nutr 40(9):1231–1242. https://doi.org/10.1080/01904167.2016.1187740
Cheng H, Wang MY, Wong MH, Ye ZH (2014) Does radial oxygen loss and iron plaque formation on roots alter cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375(1–2):137–148. https://doi.org/10.1007/s11104-013-1945-0
Connorton JM, Balk J, Rodriguez-Celma J (2017) Iron homeostasis in plants – a brief overview. Metallomics 9(7):813–823. https://doi.org/10.1039/c7mt00136c
de Mendiburu F (2019) Agricolae: statistical procedures for agricultural research, R package version 1.3-1. https://CRAN.R-project.org/package=agricolae. Accessed 15 April 2020
de Oliveira LM, Ma LQ, Santos JA, Guilherme LR, Lessl JT (2014) Effects of arsenate, chromate, and sulfate on arsenic and chromium uptake and translocation by arsenic hyperaccumulator Pteris vittata L. Environ Pollut 184:187–192. https://doi.org/10.1016/j.envpol.2013.08.025
de Oliveira LM, Gress J, De J, Rathinasabapathi B, Marchi G, Chen Y, Ma LQ (2016) Sulfate and chromate increased each other's uptake and translocation in as-hyperaccumulator Pteris vittata. Chemosphere 147:36–43. https://doi.org/10.1016/j.chemosphere.2015.12.088
Fageria MK (2013) Mineral nutrition of rice. CRC Press, Boca Rotan
Fan JL, Hu ZY, Ziadi N, Xia X, Yang C, Wu H (2010) Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.). Environ Pollut 158:409–415. https://doi.org/10.1016/j.envpol.2009.08.042
Fan JL, Xia X, Hu ZY, Ziadi N, Liu C (2013) Excessive sulfur supply reduces arsenic accumulation in brown rice. Plant Soil Environ 59(4):169–174. https://doi.org/10.17221/882/2012-PSE
Flury B, Frommer J, Eggenberger U, Mader U, Nachtegaal M, Kretzschmar R (2009) Assessment of long-term performance and chromate reduction mechanisms in a field-scale permeable reactive barrier. Environ Sci Technol 43:6786–6792. https://doi.org/10.1021/es803526g
Gao Y, Xia J (2011) Chromium contamination accident in China: viewing environment policy of China. Environ Sci Technol 45(20):8605–8606. https://doi.org/10.1021/es203101f
Gao MX, Hu ZY, Wang GD, Xia X (2010) Effect of elemental sulfur supply on cadmium uptake into rice seedlings when cultivated in low and excess cadmium soils. Commun Soil Sci Plant Anal 41(8):990–1003. https://doi.org/10.1080/00103621003646071
Gao F, Robe K, Gaymard F, Izquierdo E, Dubos C (2019) The transcriptional control of Iron homeostasis in plants: a tale of bHLH transcription factors? Front Plant Sci 10:6. https://doi.org/10.3389/fpls.2019.00006
González PS, Talano MA, Wevar Oller AL, Ibañez SG, Medina MI, Agostini E (2014) Update on mechanisms involved in arsenic and chromium accumulation, translocation and homeostasis in plants. In: Kumar Gupta D, Chatterjee S (eds) Heavy metal remediation. Nova Science Publishers, New York, pp 45–72
Hakim MA, Juraimi AS, Begum M, Hanafi MM, Ismail MR, Selamat A (2010) Effect of salt stress on germination and early seedling growth of rice (Oryza sativa L.). Afr J Biotechnol 9(13):1911–1918. https://doi.org/10.5897/AJB09.1526
Hayat S, Khalique G, Irfan M, Wani AS, Tripathi BN, Ahmad A (2012) Physiological changes induced by chromium stress in plants: an overview. Protoplasma 249:599–611. https://doi.org/10.1007/s00709-011-0331-0
Holland SL, Avery SV (2011) Chromate toxicity and the role of sulfur. Metallomics 3:1119–1123. https://doi.org/10.1039/c1mt00059d
Honsel A, Kojima M, Haas R, Frank W, Sakakibara H, Herschbach C, Rennenberg H (2012) Sulphur limitation and early sulfur deficiency responses in poplar: the significance of gene expression, metabolites, and plant hormones. J Exp Bot 63(5):1873–1893. https://doi.org/10.1093/jxb/err365
Hu ZY, Xu CK (2002) Soil sulfur and environmental quality. In: Chen HM (ed) Behaviors of chemical substances in soils and environmental quality. Science Press, Beijing, pp 283–307 (in Chinese)
Hu ZY, Zhu YG, Li M, Zhang LG, Cao ZH, Smith FA (2007) Sulfur (S)-induced enhancement of iron plaque formation in the rhizosphere reduces arsenic accumulation in rice (Oryza sativa L.) seedlings. Environ Pollut 147:387–393. https://doi.org/10.1016/j.envpol.2006.06.014
Hu Y, Huang YZ, Liu YX (2014) Influence of iron plaque on chromium accumulation and translocation in three rice (Oryza sativa L.) cultivars grown in solution culture. Chem Ecol 30(1):29–38. https://doi.org/10.1080/02757540.2013.829050
Huang XY, Li M, Luo R, Zhao FJ, Salt DE (2019) Epigenetic regulation of sulfur homeostasis in plants. J Exp Bot 70(16):4171–4182. https://doi.org/10.1093/jxb/erz218
Huang G, Ding C, Li Y, Zhang T, Wang X (2020) Selenium enhances iron plaque formation by elevating the radial oxygen loss of roots to reduce cadmium accumulation in rice (Oryza sativa L.). J Hazard Mater 398:122860. https://doi.org/10.1016/j.jhazmat.2020.122860
Joseph MJ (2019) Structural biology of plant sulfur metabolism: from sulfate to glutathione. J Exp Bot 70:4089–4103. https://doi.org/10.1093/jxb/erz094
Kabata-Pendias A (2010) Trace elements in soils and plants. CRC press, Boca Raton
Khan N, Seshadri B, Bolan N, Saint CP, Kirkham NB, Chowdhury S, Yamaguchi N, Lee DY, Li G, Kunhikrishnan A, Qi F, Karunanithi R, Qiu R, Zhu YG, Syu CH (2016) Root iron plaque on wetland plants as a dynamic pool of nutrients and contaminants. Adv Agron 138:1–96. https://doi.org/10.1016/bs.agron.2016.04.002
Lešková A, Giehl RFH, Hartmann A, Fargašová A, Wirén NW (2017) Heavy metals induce iron-deficiency responses at different hierarchic and regulatory levels. Plant Physiol 174(3):1648–1668. https://doi.org/10.1104/pp.16.01916
Liu WJ, Zhu YG (2005) Iron and Mn plaques on the surface of roots of wetland plants. Acta Ecol Sin 25(2):358–363 (in Chinese)
Liu C, Gong X, Chen C, Yang J, Xu S (2016) The effect of iron plaque on lead translocation in soil- Carex cinerascens kukenth. system. Int J Phytorem 18(1):1–9. https://doi.org/10.1080/15226514.2015.1021954
Ma X, Liu J, Wang M (2013) Differences between rice cultivars in iron plaque formation on roots and plant lead tolerance. Adv J Food Sci Technol 5:160–163. https://doi.org/10.19026/ajfst.5.3237
Ma J, Lv C, Xu M, Chen G, Lv C, Gao Z (2016) Photosynthesis performance, antioxidant enzymes, and ultrastructural analyses of rice seedlings under chromium stress. Environ Sci Pollut Res 23:1768–1778. https://doi.org/10.1007/s11356-015-5439-x
Martínez-Trujillo M, Méndez-Bravo A, Ortiz-Castro R, Hernández-Madrigal F, Ibarra-Laclette E, Ruiz-Herrera LF, Long TA, Cervantes C, Herrera-Estrella L, López-Bucio J (2014) Chromate alters root system architecture and activates expression of genes involved in iron homeostasis and signalling in Arabidopsis thaliana. Plant Mol Biol 86(1–2):35–50. https://doi.org/10.1007/s11103-014-0210-0
Maruyama-Nakashita A, Watanabe-Takahashi A, Inoue E, Yamaya T, Saito K, Takahashi H (2015) Sulfur-responsive elements in the 3′-nontranscribed intergenic region are essential for the induction of SULFATE TRANSPORTER 2;1 gene expression in Arabidopsis roots under sulfur deficiency. Plant Cell 27(4):1279–1296. https://doi.org/10.1105/tpc.114.134908
Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus: a role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54(2):249–259. https://doi.org/10.1111/j.1365-313X.2008.03410.x
Mukta RH, Khatun MR, Nazmul Huda AKM (2019) Calcium induces phytochelatin accumulation to cope with chromium toxicity in rice (Oryza sativa L.). J Plant Interact 14(1):295–302. https://doi.org/10.1080/17429145.2019.1629034
Oliveira H (2012) Chromium as an environmental pollutant: insights on induced plant toxicity. J Bot 2012:375843–375848. https://doi.org/10.1155/2012/375843
Patsoukis N, Georgiou CD (2007) Thiol redox state and oxidative stress affect sclerotial differentiation of the phytopathogenic fungi Sclerotium rolfsii and Sclerotinia sclerotiorum. J Appl Microbiol 104:42–50. https://doi.org/10.1111/j.1365-2672.2007.03527.x
Perrier F, Yan B, Candaudap F, Pokrovsky OS, Gourdain E, Meleard B, Bussière S, Coriou C, Robert T, Nguyen C (2016) Variability in grain cadmium concentration among durum wheat cultivars: impact of aboveground biomass partitioning. Plant Soil 404:307–320. https://doi.org/10.1007/s11104-016-2847-8
Qiu B, Zeng F, Cai S, Wu X, Haider SI, Wu F, Zhang G (2013) Alleviation of chromium toxicity in rice seedlings by applying exogenous glutathione. J Plant Physiol 170(8):772–779. https://doi.org/10.1016/j.jplph.2013.01.016
Reich M, Aghajanzadeh T, Stuiver CEE, Koralewska A, De Kok LJ (2015) Impact of sulfate salinity on the uptake and metabolism of sulfur in Chinese cabbage. In: De Kok LJ, Hawkesford MJ, Rennenberg H, Saito K, Schnug E (eds) Molecular physiology and Ecophysiology of sulfur. Proceedings of the International Plant Sulfur Workshop. Springer, Cham, pp 227–238. https://doi.org/10.1007/978-3-319-20137-5_25
Reich M, Aghajanzadeh T, Parmar S, Hawkesfordc MJ, De Kok LJ (2018) Calcium ameliorates the toxicity of sulfate salinity in Brassica rapa. J Plant Physiol 231:1–8. https://doi.org/10.1016/j.jplph.2018.08.014
Resurreccion AP, Makino A, Bennett J, Mae T (2001) Effects of sulfur nutrition on the growth and photosynthesis of rice. Soil Sci Plant Nutr 47(3):611–620. https://doi.org/10.1080/00380768.2001.10408424
Rumble J (2019) Handbook of chemistry and physics, 100st edn. CRC Press, Boston
Sayantan D, Shardendu N (2013) Amendment in phosphorus levels moderates the chromium toxicity in Raphanus sativus L. as assayed by antioxidant enzymes activities. Ecotoxicol Environ Saf 95:161–170. https://doi.org/10.1016/j.ecoenv.2013.05.037
Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi R, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533. https://doi.org/10.1016/j.chemosphere.2017.03.074
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31(5):739–753. https://doi.org/10.1016/j.envint.2005.02.003
Shanker AK, Djanaguiraman M, Venkateswarlu B (2009) Chromium interactions in plants: current status and future strategies. Metallomics 1(5):375–383. https://doi.org/10.1039/b904571f
Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11(3):229–254. https://doi.org/10.1007/s10311-013-0407-5
Stein RJ, Duarte GL, Scheunemann L, Spohr MG, de Araújo Júnior AT, Ricachenevsky FK, Rosa LMG, Zanchin NIT, Santos RP, Fett JP (2019) Genotype variation in Rice (Oryza sativa L.) tolerance to Fe toxicity might be linked to root cell wall lignification. Front Plant Sci 10:746. https://doi.org/10.3389/fpls.2019.00746
Sun L, Zheng C, Yang J, Peng C, Xu C, Wang Y, Feng J, Shi J (2016) Impact of sulfur (S) fertilisation in paddy soils on copper (Cu) accumulation in rice (Oryza sativa L.) plants under flooding conditions. Biol Fertil Soils 52(1):31–39. https://doi.org/10.1007/s00374-015-1050-z
Sun L, Liu Q, Xue Y, Xue Y, Xu C, Peng C, Yuan X (2019) Dynamic influence of S fertiliser on cu bioavailability in rice (Oryza sativa L.) rhizosphere soil during the whole life cycle of rice plants. J Soils Sediments 19(1):198–210. https://doi.org/10.1007/s11368-018-2009-0
Sundaramoorthy P, Chidambaram A, Ganesh KS, Unnikannan P, Baskaran L (2010) Chromium stress in paddy: (i) nutrient status of paddy under chromium stress; (ii) phytoremediation of chromium by aquatic and terrestrial weeds. C R Biol 333(8):597–607. https://doi.org/10.1016/j.crvi.2010.03.002
Tausz M, Helena S, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55(404):1955–1962. https://doi.org/10.1093/jxb/erh194
Tripathi DK, Singh VP, Kumar D, Chauhan DK (2012) Impact of exogenous silicon addition on chromium uptake, growth, mineral elements, oxidative stress, antioxidant capacity, and leaf and root structures in rice seedlings exposed to hexavalent chromium. Acta Physiol Plant 34(1):279–289. https://doi.org/10.1007/s11738-011-0826-5
Tripathi RD, Tripathi P, Dwivedi S, Kumar A, Mishra A, Chauhan PS, Norton GJ, Nautiyal CS (2014) Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics 6:1789–1800. https://doi.org/10.1039/c4mt00111g
Vigani V, Zocchi Z, Bashir K, Philippar K, Briat JF (2013) Cellular iron homeostasis and metabolism in plant. Front Plant Sci 4:490. https://doi.org/10.3389/fpls.2013.00490
Wang YF, Wang SP, Cui XY, Chen ZZ, Schnug E, Haneklau S (2003) Effects of Sulphur supply on the morphology of shoots and roots of alfalfa (Medicago sativa L.). Grass Forage Sci 58(2):160–167. https://doi.org/10.1046/j.1365-2494.2003.00366.x
Wang D, Li X, Wang DC, Rao W, Du GH, Yang J, Hua DL (2015) Influence of sulfur on the formation of Fe-Mn plaque on root and uptake of cd by rice (Oryza sativa L.). Huan Jing Ke Xue 36(5):1877–1887. https://doi.org/10.13227/j.hjkx.2015.05.050
Wickham H (2016) Ggplot2: elegant graphics for data analysis. Springer-Verlag, New York https://ggplot2.tidyverse.org
Wu Z (2014) Influence of sulfur on the contents and distribution of iron, cadmium and related complexes in rice. PhD dissertation, Nanjing University, China
Wu CYH, Lu J, Hu ZY (2014a) Influence of sulfur supply on the iron accumulation in rice plants. Commun Soil Sci Plant Anal 45(8):1149–1161. https://doi.org/10.1080/00103624.2013.875189
Wu LB, Shhadi M, Gregorio G, Matthus E, Becker M, Frei M (2014b) Genetic and physiological analysis of tolerance to acute iron toxicity in rice. Rice 7:8. https://doi.org/10.1186/s12284-014-0008-3
Xu B, Wang F, Zhang Q, Lan Q, Liu C, Guo X, Cai Q, Chen Y, Wang G, Ding J (2018) Influence of iron plaque on the uptake and accumulation of chromium by rice (Oryza sativa L.) seedlings: insights from hydroponic and soil cultivation. Ecotoxicol Environ Saf 162:51–58. https://doi.org/10.1016/j.ecoenv.2018.06.063
Yamaguchi C, Maruyama-Nakashita A (2017) Sulfate transporters involved in cd-induced changes of sulfate uptake and distribution in Arabidopsis thaliana. In: De Kok LJ, Hawkesford MJ, Haneklaus SH, Schnug E (eds) Sulfur metabolism in higher plants - fundamental. Environmental and Agricultural Aspects. Springer, Cham, pp 199–205
Yamaguchi C, Takimoto Y, Ohkama-Ohtsu N, Hokura A, Shinano T, Nakamura T, Suyama A, Maruyama-Nakashita A (2016) Effects of cadmium treatment on the uptake and translocation of sulfate in Arab. Thaliana. Plant Cell Physiol 57:2353–2366. https://doi.org/10.1093/pcp/pcw156
Yamaguchi C, Khamsalath S, Takimoto Y, Suyama A, Mori Y, Ohkama-Ohtsu N, Maruyama-Nakashita A (2020) SLIM1 transcription factor promotes sulfate uptake and distribution to shoot, along with Phytochelatin accumulation, under cadmium stress in Arabidopsis thaliana. Plants 9:163. https://doi.org/10.3390/plants9020163
Yamazaki S, Ueda Y, Mukai A, Ochiai K, Matoh T (2018) Rice phytochelatin synthases OsPCS1 and OsPCS2 make different contributions to cadmium and arsenic tolerance. Plant Direct 2:1–15. https://doi.org/10.1002/pld3.34
Yang JX, Tam NFY, Ye ZH (2014) Root porosity, radial oxygen loss and iron plaque on roots of wetland plants in relation to zinc tolerance and accumulation. Plant Soil 374(1–2):815–828. https://doi.org/10.1007/s11104-013-1922-7
Yang J, Liu Z, Wan X, Zheng G, Yang J, Zhang H, Guo L, Wang X, Zhou X, Guo Q, Xu R, Zhou G, Peters M, Zhu G, Wei R, Tian L, Han X (2016) Interaction between sulfur and lead in toxicity, iron plaque formation and lead accumulation in rice plant. Ecotoxicol Environ Saf 128:206–212. https://doi.org/10.1016/j.ecoenv.2016.02.021
Yu XZ, Lu MR, Zhang XH (2017) The role of iron plaque in transport and distribution of chromium by rice seedlings. Cereal Res Commun 45(4):598–609. https://doi.org/10.1556/0806.45.2017.040
Zandi P, Yang JJ, Xin X, Yu T, Li Q, Możdżeń K, Yaosheng W (2020) Do sulfur addition and rhizoplane iron plaque affect chromium uptake by rice (Oryza sativa L.) seedlings in culture solution? J Hazard Mater 388:121803. https://doi.org/10.1016/j.jhazmat.2019.121803
Zeng FR, Chen S, Mao Y, Wu FB, Zhang GP (2008) Changes of organic acid exudation and rhizosphere pH in the rice plant under chromium stress. Environ Pollut 155(2):284–289. https://doi.org/10.1016/j.envpol.2007.11.019
Zeng F, Ali S, Qiu B, Wu F, Zhang G (2010) Effects of chromium stress on the subcellular distribution and chemical form of Ca, Mg, Fe, and Zn in two rice genotypes. J Plant Nutr Soil Sci 173(1):135–148. https://doi.org/10.1002/jpln.200900134
Zeng F, Qiu B, Wu X, Niu S, Wu F, Zhang G (2012) Glutathione-mediated alleviation of chromium toxicity in rice plants. Biol Trace Elem Res 148(2):255–263. https://doi.org/10.1007/s12011-012-9362-4
Zou JH, Wang M, Jiang WS, Liu DH (2006) Effect of hexavalent chromium (VI) on root growth and cell division in root tip cells of Amaranthus viridis L. Pak J Bot 38:673–681
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The work was supported by the National Key Research and Development Program of China (2016YFD0800400), National Natural Science Foundation of China (U1632134; 41877033), and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Science (2016-2018).
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JY: designed and coordinated the project. PZ: carried out greenhouse and lab experiments and wrote the manuscript (principal researcher). QL and PZ: provided the stock and working solutions. XX and SH: provided lab facilities. PZ, SMH and QL: performed data analysis and provided the required materials. PZ, SMH, SH, XX, BK, JP, YW, EB and KM: participated in the interpretation of the results and drafted the manuscript. PZ, BK, KM, JY, JP, SMH, BR, EB, and YW: improved the grammar and corrected spelling mistakes. PZ, JY, YW, BK, SMH, BR, EB and KM: edited and revised the manuscript. All authors read, corrected and approved the final manuscript.
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Zandi, P., Yang, J., Xia, X. et al. Sulphur nutrition and iron plaque formation on roots of rice seedlings and their consequences for immobilisation and uptake of chromium in solution culture. Plant Soil 462, 365–388 (2021). https://doi.org/10.1007/s11104-021-04870-8
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DOI: https://doi.org/10.1007/s11104-021-04870-8