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Glutathione homeostasis and Cd tolerance in the Arabidopsis sultr1;1-sultr1;2 double mutant with limiting sulfate supply

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Cadmium sensitivity in sultr1;1 - sultr1;2 double mutant with limiting sulfate supply is attributed to the decreased glutathione content that affected oxidative defense but not phytochelatins’ synthesis.

Abstract

In plants, glutathione (GSH) homeostasis plays pivotal role in cadmium (Cd) detoxification. GSH is synthesized by sulfur (S) assimilation pathway. Many studies have tried to investigate the role of GSH homeostasis on Cd tolerance using mutants; however, most of them have focused on the last few steps of S assimilation. Until now, mutant evidence that explored the relationship between GSH homeostasis on Cd tolerance and S absorption is rare. To further reveal the role of GSH homeostasis on Cd stress, the wild-type and a sultr1;1-sultr1;2 double mutant which had a defect in two distinct high-affinity sulfate transporters were used in this study. Growth parameters, biochemical or zymological indexes and S assimilation-related genes’ expression were compared between the mutant and wild-type Arabidopsis plants. It was found that the mutations of SULTR1;1 and SULTR1;2 did not affect Cd accumulation. Compared to the wild-type, the double mutant was more sensitive to Cd under limited sulfate supply and suffered from stronger oxidative damage. More importantly, under the same condition, lower capacity of S assimilation resulted in decreased GSH content in mutant. Faced to the limited GSH accumulation, mutant seedlings consumed a large majority of GSH in pool for the synthesis of phytochelatins rather than participating in the antioxidative defense. Therefore, homeostasis of GSH, imbalance between antioxidative defense and severe oxidative damage led to hypersensitivity of double mutant to Cd under limited sulfate supply.

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References

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Ali M, Chun H, Kim B, Lee C (2002) Cadmium-induced changes in antioxidant enzyme activities in rice (Oryza sativa L. cv. Dongjin). J Plant Biol 45:134–140

    Article  CAS  Google Scholar 

  • Aravind P, Prasad MNV (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116

    Article  CAS  PubMed  Google Scholar 

  • Astolfi S, Zuchi S, Passera C (2004) Role of sulphur availability on cadmium-induced changes of nitrogen and sulphur metabolism in maize (Zea mays L.) leaves. J Plant Physiol 161:795–802

    Article  CAS  PubMed  Google Scholar 

  • Azpilicueta CE, Benavides MP, Tomaro ML, Gallego SM (2007) Mechanism of CATA3 induction by cadmium in sunflower leaves. Plant Physiol Biochem 45:589–595

    Article  CAS  PubMed  Google Scholar 

  • Baker A, Reeves R, Hajar A (2006) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. and C. Presl (Brassicaceae). New Phytol 127:61–68

    Article  Google Scholar 

  • Barberon M, Berthomieu P, Clairotte M, Shibagaki N, Davidian JC, Gosti F (2008) Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. New Phytol 180:608–619

    Article  CAS  PubMed  Google Scholar 

  • Bashir H, Ahmad J, Bagheri R, Nauman M, Qureshi MI (2013) Limited sulfur resource forces Arabidopsis thaliana to shift towards non-sulfur tolerance under cadmium stress. Environ Exp Bot 94:19–32

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2012a) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    Article  Google Scholar 

  • Chen J, Wu FH, Liu TW, Chen L, Xiao Q, Dong XJ, He JX, Pei ZM, Zheng HL (2012b) Emissions of nitric oxide from 79 plant species in response to simulated nitrogen deposition. Environ Pollut 160:192–200

    Article  CAS  PubMed  Google Scholar 

  • Cho UH, Seo NH (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120

    Article  CAS  Google Scholar 

  • Cho UH, Seo NH (2006) Changes of thiols and oxidative stress in tomato seedlings exposed to cadmium. J Ecol Field Biol 29:61–67

    Article  Google Scholar 

  • Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139:425–436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216

    Article  CAS  PubMed  Google Scholar 

  • Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J 16:73–78

    Article  CAS  PubMed  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Di Cagno R, Guidi L, De Gara L, Soldatini GF (2001) Combined cadmium and ozone treatments affect photosynthesis and ascorbate-dependent defences in sunflower. New Phytol 151:627–636

    Article  Google Scholar 

  • Ebbs S, Uchil S (2008) Cadmium and zinc induced chlorosis in Indian mustard [Brassica juncea (L.) Czern] involves preferential loss of chlorophyll b. Photosynthetica 46:49–55

    Article  CAS  Google Scholar 

  • El-Zohri M, Odjegba V, Ma L, Rathinasabapathi B (2015) Sulfate influx transporters in Arabidopsis thaliana are not involved in arsenate uptake but critical for tissue nutrient status and arsenate tolerance. Planta 241:1109–1118

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frachisse JM, Thomine S, Colcombet J, Guern J, Barbier-Brygoo H (1999) Sulfate is both a substrate and an activator of the voltage-dependent anion channel of Arabidopsis hypocotyl cells. Plant Physiol 121:253–262

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627–633

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120

    Article  CAS  PubMed  Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    Article  Google Scholar 

  • Guan C, Ji J, Jia C, Guan W, Li X, Jin C, Wang G (2015) A GSHS-like gene from Lycium chinense maybe regulated by cadmium-induced endogenous salicylic acid and overexpression of this gene enhances tolerance to cadmium stress in Arabidopsis. Plant Cell Rep 34:871–884

    Article  CAS  PubMed  Google Scholar 

  • Harada E, Choi YE, Tsuchisaka A, Obata H, Sano H (2001) Transgenic tobacco plants expressing a rice cysteine synthase gene are tolerant to toxic levels of cadmium. J Plant Physiol 158:655–661

    Article  CAS  Google Scholar 

  • Hawkesford MJ (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. J Exp Bot 51:131–138

    Article  CAS  PubMed  Google Scholar 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160:1085–1093

    Article  PubMed  Google Scholar 

  • Heiss S, Schäfer H, Haag-Kerwer A, Rausch T (1999) Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol Biol 39:847–857

    Article  CAS  PubMed  Google Scholar 

  • Hodges DM, Forney CF (2000) The effects of ethylene, depressed oxygen and elevated carbon dioxide on antioxidant profiles of senescing spinach leaves. J Exp Bot 51:645–655

    Article  CAS  PubMed  Google Scholar 

  • Hou W, Chen X, Song G, Wang Q, Chi Chang C (2007) Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). Plant Physiol Biochem 45:62–69

    Article  CAS  PubMed  Google Scholar 

  • Howden R, Andersen CR, Goldsbrough PB, Cobbett CS (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hsu YT, Kao CH (2007) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 298:231–241

    Article  CAS  Google Scholar 

  • Hubberten HM, Drozd A, Tran BV, Hesse H, Hoefgen R (2012) Local and systemic regulation of sulfur homeostasis in roots of Arabidopsis thaliana. Plant J 72:625–635

    Article  CAS  PubMed  Google Scholar 

  • Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koffler BE, Polanschütz L, Zechmann B (2014) Higher sensitivity of pad2-1 and vtc2-1 mutants to cadmium is related to lower subcellular glutathione rather than ascorbate contents. Protoplasma 251:755–769

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kopriva S, Mugford S, Matthewman C, Koprivova A (2009) Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep 28:1769–1780

    Article  CAS  PubMed  Google Scholar 

  • Lancilli C, Giacomini B, Lucchini G, Davidian JC, Cocucci M, Sacchi GA, Nocito FF (2014) Cadmium exposure and sulfate limitation reveal differences in the transcriptional control of three sulfate transporter (Sultr1; 2) genes in Brassica juncea. BMC Plant Biol 14:132

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee S, Leustek T (1999) The affect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci 141:201–207

    Article  CAS  Google Scholar 

  • Li JX, Gao LJ, Zheng L, Chen JH, Wang JT, Wang XR (2014) Determination of monobromobimane-labeled phytochelatins by high-performance liquid chromatography. Anal Lett 47:2148–2155

    Article  CAS  Google Scholar 

  • Lichtenthaler H (1987) Chlorophylls and carotenoids-pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu D, An Z, Mao Z, Ma L, Lu Z (2015) Enhanced heavy metal tolerance and accumulation by transgenic sugar beets expressing Streptococcus thermophilus STGCS-GS in the presence of Cd, Zn and Cu alone or in combination. PLoS One 10:e0128824

    Article  PubMed Central  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  CAS  PubMed  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Montagu MV, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    CAS  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MN (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37

    Article  CAS  PubMed  Google Scholar 

  • Momodu M, Anyakora C (2010) Heavy metal contamination of ground water: the surulere case study. Res J Environ Earth Sci 2:39–43

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in Spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nocito FF, Pirovano L, Cocucci M, Sacchi GA (2002) Cadmium-induced sulfate uptake in maize roots. Plant Physiol 129:1872–1879

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Paradiso A, Berardino R, de Pinto MC, Sanita di Toppi L, Storelli MM, Tommasi F, De Gara L (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362–374

    Article  CAS  PubMed  Google Scholar 

  • Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288

    Article  CAS  PubMed  Google Scholar 

  • Rea PA (2012) Phytochelatin synthase: of a protease a peptide polymerase made. Physiol Plant 145:154–164

    Article  CAS  PubMed  Google Scholar 

  • Ruiz J, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965–969

    Article  CAS  PubMed  Google Scholar 

  • Ryan KC, Johnson OE, Cabelli DE, Brunold TC, Maroney MJ (2010) Nickel superoxide dismutase: structural and functional roles of Cys2 and Cys6. J Biol Inorg Chem 15:795–807

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188–195

    Article  CAS  PubMed  Google Scholar 

  • Salin ML (2007) Toxic oxygen species and protective systems of the chloroplast. Physiol Plantarum 72:681–689

    Article  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  PubMed  Google Scholar 

  • Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Semane B, Cuypers A, Smeets K, Van Belleghem F, Horemans N, Schat H, Vangronsveld J (2007) Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiol Plant 129:519–528

    Article  CAS  Google Scholar 

  • Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1; 2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486

    Article  CAS  PubMed  Google Scholar 

  • Singh P, Tewari R (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–112

    CAS  PubMed  Google Scholar 

  • Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A, Vangronsveld J (2005) Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444

    Article  CAS  PubMed  Google Scholar 

  • Sneller FEC, van Heerwaarden LM, Koevoets PL, Vooijs R, Schat H, Verkleij JA (2000) Derivatization of phytochelatins from Silene vulgaris, induced upon exposure to arsenate and cadmium: comparison of derivatization with Ellman’s reagent and monobromobimane. J Agr Food Chem 48:4014–4019

    Article  CAS  Google Scholar 

  • Sobrino-Plata J, Meyssen D, Cuypers A, Escobar C, Hernández LE (2014) Glutathione is a key antioxidant metabolite to cope with mercury and cadmium stress. Plant Soil 377:369–381

    Article  CAS  Google Scholar 

  • Sun X, Lu B, Huang S, Mehta S, Xu L, Yang Z (2007) Coordinated expression of sulfate transporters and its relation with sulfur metabolites in Brassica napus exposed to cadmium. Bot Stud 48:43–54

    CAS  Google Scholar 

  • Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2001) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182

    Article  Google Scholar 

  • Talukdar D (2012) An induced glutathione-deficient mutant in grass pea (Lathyrus sativus L.): modifications in plant morphology, alteration in antioxidant activities and increased sensitivity to cadmium. Biorem Biodivers Bioavailab 6:75–86

    Google Scholar 

  • Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H, Amako K, Yamawaki K, Murata N (2006) Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184

    Article  CAS  PubMed  Google Scholar 

  • Vidmar JJ, Tagmount A, Cathala N, Touraine B, Davidian JCE (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett 475:65–69

    Article  CAS  PubMed  Google Scholar 

  • Vögeli-Lange R, Wagner GJ (1996) Relationship between cadmium, glutathione and cadmium-binding peptides (phytochelatins) in leaves of intact tobacco seedlings. Plant Sci 114:11–18

    Article  Google Scholar 

  • Xu J, Yin H, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Zhu Y, Ge Q, Li Y, Sun J, Zhang Y, Liu X (2012) Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. New Phytol 196:125–138

    Article  CAS  PubMed  Google Scholar 

  • Yan K, Chen W, Zhang G, Xu S, Liu Z, He X, Wang L (2010) Elevated CO2 ameliorated oxidative stress induced by elevated O3 in Quercus mongolica. Acta Physiol Plant 32:375–385

    Article  CAS  Google Scholar 

  • Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:378–388

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang ZC, Chen BX, Qiu BS (2010) Phytochelatin synthesis plays a similar role in shoots of the cadmium hyperaccumulator Sedum alfredii as in non-resistant plants. Plant Cell Environ 33:1248–1255

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Françoise Gosti from France for kindly providing sultr1;1-sultr1;2 double mutant seeds. This study was financially supported by the Natural Science Foundation of China (NSFC Nos. 30930076, 31260057, 31300505 and 31570586), Research Fund of State Key Laboratory of Soil and Sustainable Agriculture, Nanjing Institute of Soil Science, Chinese Academy of Science (Y412201449), China Postdoctoral Science Foundation (2012M521278).

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  1. Key Laboratory for Subtropical Wetland Ecosystem Research of MOE, College of the Environment and Ecology, Xiamen University, Xiamen, 361102, Fujian, People’s Republic of China

    Xiang Liu, Fei-Hua Wu, Juan Chen, Guang-Hui Wang, Wen-Jun Hu, Martin Simon & Hai-Lei Zheng

  2. Colleges of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 310036, Zhejiang, People’s Republic of China

    Fei-Hua Wu

  3. Marine Ecology Research Center, First Institute of Oceanography, State Oceanic Administration, Qingdao, 266061, Shandong, People’s Republic of China

    Jing-Xi Li, Li-Jie Gao, Zong-Ling Wang & Jun-Hui Chen

  4. Sericultural Research Institute, Zhejiang Academy of Agricultural Science, Hangzhou, 310021, Zhejiang, People’s Republic of China

    Wen-Jun Hu

  5. Fujian Key Laboratory of Subtropical Plant Physiology and Biochemistry, Fujian Institute of Subtropical Botany, Xiamen, 361005, Fujian, People’s Republic of China

    Wen-Hua Wang

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  1. Xiang Liu
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X.L., F.H.W. and H.L.Z. designed the experiments and wrote the manuscript. X.L., F.H.W., J.X.L., J.C., G.H.W., W.H.W., W.J.H., L.J.G., Z.L.W. and J.H.C. conducted experiments. X.L. and M.S. analyzed data. F.H.W. and W.H.W. provided technical assistance. All authors read and approved the manuscript.

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Supplementary Table S1. Lists of primers used in quantitative real-time PCR. Supplementary Table S2. Sulfate uptake or metabolism related genes expression in wild-type and double sultr1;1-sultr1;2 null mutant Arabidopsis seedlings under limited or sufficient sulfate conditions for two weeks. Supplementary Methods: Determination of phytochelatins (PCs). Supplementary Figure S1. The primary root length of ten-day-old wild-type and sultr1;1-sultr1;2 double mutant seedlings grown in 1/2 modified MS medium supplemented with 0, 25, 50, 100, 200, 400 and 1500 μM K2SO4 concentrations. 1/2 standard MS medium was chosen as control. Forty seedlings were used for each treatment. Data are mean ± SE. Supplementary Figure S2. The phenotype of wild-type and double sultr1;1-sultr1;2 null mutant of Arabidopsis seedlings under four treatment conditions for two weeks. (a) LS: 200 μM K2SO4, wild-type; (b) LS+Cd: 200 μM K2SO4 + 20 μM CdCl2, wild-type; (c) SS: 1500 μM K2SO4, wild-type; (d) SS+Cd: 1500 μM K2SO4 + 20 μM CdCl2, wild-type; (e) LS: 200 μM K2SO4 , double sultr1;1-sultr1;2 null mutant; (f) LS+Cd: 200 μM K2SO4 + 20 μM CdCl2, double mutant; (g) SS: 1500 μM K2SO4, double mutant; (h) SS+Cd: 1500 μM K2SO4 + 20 μM CdCl2, double mutant. (DOCX 2048 kb)

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Liu, X., Wu, FH., Li, JX. et al. Glutathione homeostasis and Cd tolerance in the Arabidopsis sultr1;1-sultr1;2 double mutant with limiting sulfate supply. Plant Cell Rep 35, 397–413 (2016). https://doi.org/10.1007/s00299-015-1892-8

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