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Overexpression of the maize phytochelatin synthase gene (ZmPCS1) enhances Cd tolerance in plants

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Abstract

Phytochelatin synthase (PCS) catalyzes the biosynthesis of phytochelatins (PCs), which play an essential role in detoxification of heavy metals in plants and other living organisms. In this study, we investigated the roles of the maize phytochelatin synthase gene ZmPCS1 in cadmium (Cd) tolerance. Induced expression results showed that expression of ZmPCS1 was upregulated under Cd stress in maize leaves and roots. Moreover, ZmPCS1 repaired the defective phenotypes resulting from heteroexpression of ZmPCS1 in the Cd-sensitive yeast mutant ∆ycf1 and Arabidopsis AtPCS1-deficent mutant atpcs1 under Cd stress. Moreover, overexpression in Arabidopsis also enhanced Cd tolerance and accumulation. Further analysis suggested that this increase in tolerance was due to increases in glutathione and PC contents, and a decrease in reactive oxygen species accumulation. Meanwhile, transient expression of ZmPCS1 in tobacco leaves was also found to cause a decrease in Cd toxicity. Taken together, these results suggest that the maize ZmPCS1 gene plays an important role in Cd tolerance in yeast and plants, and could, therefore, serve as a promising candidate in future breeding programs in crops.

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References

  • Agarwal P, Mitra M, Banerjee S, Roy S (2020) MYB4 transcription factor, a member of R2R3-subfamily of MYB domain protein, regulates cadmium tolerance via enhanced protection against oxidative damage and increases expression of PCS1 and MT1C in Arabidopsis. Plant Sci 297:110501

    Article  CAS  PubMed  Google Scholar 

  • Blum JK, Bommarius AS (2010) Amino ester hydrolase from Xanthomonas campestris pv. campestris, ATCC 33913 for enzymatic synthesis of ampicillin. J Mol Catal B Enzym 67:21–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunetti P, Zanella L, Proia A, Paolis AD, Falasca G, Altamura MM, Toppi LSd, Costantino P, Cardarelli M (2011) Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1. J Exp Bot 62:5509–5519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai Y, Cao FB, Cheng WD, Zhang GP, Wu FB (2011) Modulation of exogenous glutathione in phytochelatins and photosynthetic performance against Cd stress in the two rice genotypes differing in Cd tolerance. Biol Trace Elem Res 143:1159–1173

    Article  CAS  PubMed  Google Scholar 

  • Cazalé AC, Clemens S (2001) Arabidopsis thaliana expresses a second functional phytochelatin synthase. FEBS Lett 507:215–219

    Article  PubMed  Google Scholar 

  • Chen J, Yang L, Gu J, Bai X, Ren Y, Fan T, Han Y, Jiang L, Xiao F, Liu Y, Cao S (2015) MAN3 gene regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis thaliana. New Phytol 205:570–582

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Yang L, Yan X, Liu Y, Wang R, Fan T, Ren Y, Tang X, Xiao F, Liu Y (2016) Zinc-Finger Transcription Factor ZAT6 positively regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis. Plant Physiol 171:707–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  PubMed  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  PubMed  Google Scholar 

  • Dalcorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das N, Bhattacharya S, Bhattacharyya S, Maiti MK (2017) Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2 involved in mitigation of cadmium and arsenic stresses. Plant Mol Biol 94:167–183

    Article  CAS  PubMed  Google Scholar 

  • Erdei S (2002) Heavy metal induced physiological changes in the antioxidative response system. Acta Biol Szegediensis 46:89–90

    Google Scholar 

  • Francesca D, Maria DB, Alessandro P, Alberto M, Laura F, Sergio S, Adriana B, Luigi SdT (2014) A Cd/Fe/Zn-responsive phytochelatin synthase is constitutively present in the ancient liverwort lunularia cruciata (L.) dumort. Plant Cell Physio 55:1884–1891

    Article  Google Scholar 

  • Garnier L, Simon-Plas FO, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants: probing the role of sulfur. Plant Signal Behav 6:215–222

    Article  CAS  PubMed  Google Scholar 

  • Gong JM, Lee DA, Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci USA 100:10118–10123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Dai X, Xu W, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026

    Article  CAS  PubMed  Google Scholar 

  • Ha S-B (1999) Phytochelatin synthase genes from arabidopsis and the yeast. Plant Cell 11:1153–1164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Jiang YL, Zheng QQ, Chen L, Liang YL, Wu JD (2018) Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis. Acta Physiol Plant 40:1–12

    Article  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 13:3175–3145

    Article  Google Scholar 

  • Jozefczak M, Bohler S, Schat H, Horemans N, Guisez Y, Remans T, Vangronsveld J, Cuypers A (2015) Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium. Ann Botany 116(4):601–612

    Article  CAS  Google Scholar 

  • Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kováčik J (2019) Role of low molecular weight compounds in cadmium stress tolerance. In: Hasanuzzaman M, Prasad MNV, Nahar K (eds) Cadmium tolerance in plants: Agronomic, molecular, signaling, and omic approaches. Academic Press, pp 281–318

    Google Scholar 

  • Kováčik J, Babula P, Klejdus B, Hedbavny J, Jarošová M (2014) Unexpected behavior of some nitric oxide modulators under cadmium excess in plant tissue. PLoS ONE 9:e91685

    Article  PubMed  PubMed Central  Google Scholar 

  • Kováčik J, Klejdus B, Babula P, Hedbavny J (2016) Age affects not only metabolome but also metal toxicity in Scenedesmus quadricauda cultures. J Hazard Mater 306:58–66

    Article  PubMed  Google Scholar 

  • Lee S, Petros D, Moon JS, Ko TS, Goldsbrough PB, Korban SS (2003) Higher levels of ectopic expression of Arabidopsis phytochelatin synthase do not lead to increased cadmium tolerance and accumulation. Plant Physiol Biochem 41:903–910

    Article  CAS  Google Scholar 

  • Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YJ, Dhankher OP, Carreira L, Lee D, Chen A, Schroeder JI, Balish RS, Meagher RB (2004) Overexpression of phytochelatin synthase in arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol 45:1787–1797

    Article  CAS  PubMed  Google Scholar 

  • Li JC, Guo JB, Xu WZ, Ma M (2007) RNA interference-mediated silencing of phytochelatin synthase gene reduce cadmium accumulation in rice seeds. J Integr Plant Biol 49:1032–1037

    Article  CAS  Google Scholar 

  • Liang Y, Jiang Y, Du M, Li B, Wu J (2019) ZmASR3 from the maize ASR gene family positively regulates drought tolerance in transgenic arabidopsis. Int J Mol Sci 20:2278

    Article  CAS  PubMed Central  Google Scholar 

  • Lin YF, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mole Life Sci 69:3187–3206

    Article  CAS  Google Scholar 

  • Liu GY, Zhang YX, Chai TY (2011) Phytochelatin synthase of Thlaspi caerulescens enhanced tolerance and accumulation of heavy metals when expressed in yeast and tobacco. Plant Cell Rep 30:1067–1076

    Article  CAS  PubMed  Google Scholar 

  • María L, Flores-Cáceres S, Hattab S, Hattab H, Boussetta M (2015) Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants. Plant Sci 233:165–173

    Article  Google Scholar 

  • Mourato M, Reis R, Martins LL (2012) Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity. Adv Sel Plant Physiol Aspects 12:1–17

    Google Scholar 

  • Nahar N, Rahman A, Mos M, Warzecha T, Ghosh S, Hossain K, Nawani NN, Mandal A (2014) In silico and in vivo studies of molecular structures and mechanisms of AtPCS1 protein involved in binding arsenite and/or cadmium in plant cells. J Mol Model 20(3):1–16

    Article  CAS  Google Scholar 

  • Nalini P, Pathak GC, Pandey DK, Ritu P (2009) Heavy metals Co, Ni, Cu, Zn and Cd, produce oxidative damage and evoke differential antioxidant responses in spinach. Braz J Plant Physiol 21:103–111

    Article  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Pomponi M, Censi V, Di Girolamo V, De Paolis A, di Toppi LS, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd(2+) tolerance and accumulation but not translocation to the shoot. Planta 223:180–190

    Article  CAS  PubMed  Google Scholar 

  • Ramos J, Clemente MR, Naya L, Loscos J, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. a small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruotolo R, Peracchi A, Bolchi A, Infusini G, Amoresano A, Ottonello S (2004) Domain organization of phytochelatin synthase: functional properties of truncated enzyme species identified by limited proteolysis. J Bio Chem 279(15):14686–14693

    Article  CAS  Google Scholar 

  • Sauge-Merle S, Cuine S, Carrier P, Lecomte-Pradines C, Luu DT, Peltier G (2003) Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Appl Environ Microbiol 69:490–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semane B, Cuypers A, Smeets K, Belleghem FV, 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 

  • Shine AM, Shakya VP, Idnurm A (2015) Phytochelatin synthase is required for tolerating metal toxicity in a basidiomycete yeast and is a conserved factor involved in metal homeostasis in fungi. Fungal Biol Biotechnol 28:2–3

    Google Scholar 

  • Singh V, Tripathi BN, Sharma V (2016) Interaction of Mg with heavy metals (Cu, Cd) in T. aestivum with special reference to oxidative and proline metabolism. J Plant Res 129:487–497

    Article  CAS  PubMed  Google Scholar 

  • Vatamaniuk OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: Isolation and in vitro reconstitution. Proc Natl Acad Sci USA 96:7110–7115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Wang Z, Zhu C (2012) Heteroexpression of the wheat phytochelatin synthase gene (TaPCS1) in rice enhances cadmium sensitivity. Acta Biochim Biophys Sin 44:886–893

    Article  CAS  PubMed  Google Scholar 

  • Wojas C, Hennig S, Kopera S, Bal A, DM, (2008) Overexpression of phytochelatin synthase in tobacco: distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium. J EXP BOT 59:2205–2219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XX, Rui HY, Zhang FQ, Hu ZB, Xia Y, Shen ZG (2018) Overexpression of a functional Vicia sativa PCS1 homolog increases cadmium tolerance and phytochelatins synthesis in arabidopsis. Front Plant Sci 9:107–118

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu YL, Pilon-Smits EA, Jouanin L, Terry N (1999) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–80

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Anhui Provincial Natural Science Foundation of China (grant number 2008085MC70), the SRF of Anhui and AHAU (S202110364238, 202110364413) and the Special Project of Local Science and Technology Development Guided by the Central Government of Anhui Province, China (grant number 2019b12030007).

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  1. Demiao Jin, Qin Zhang and Yuqing Liu have contributed equally to this study.

Authors and Affiliations

  1. National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural University, Hefei, 230036, Anhui, China

    Demiao Jin, Qin Zhang, Yuqing Liu, Mengna Liang, Aiqi Li & Jiandong Wu

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  1. Demiao Jin
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  2. Qin Zhang
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Correspondence to Jiandong Wu.

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Table. S1 Primers used in this study

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Jin, D., Zhang, Q., Liu, Y. et al. Overexpression of the maize phytochelatin synthase gene (ZmPCS1) enhances Cd tolerance in plants. Acta Physiol Plant 44, 114 (2022). https://doi.org/10.1007/s11738-022-03451-1

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