Skip to main content
Log in

The ethylene-responsive transcription factor of durum wheat, TdSHN1, confers cadmium, copper, and zinc tolerance to yeast and transgenic tobacco plants

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Cadmium (Cd), copper (Cu), and zinc (Zn) are among the most common heavy metals (HMs) present in polluted soils. While some HMs are required for key biological processes, they are toxic when present in excess. This toxicity damages plant health, decreases crop yields, and can impact human health via the food chain. For example, durum wheat is a staple food that is known to accumulate Cd when grown on polluted soils. Plant response to HM stress is complex and involves several transcription factors (TFs) among which members of the ERF family. Although roles of SHINE-type ERF transcription factors in abiotic stress tolerance have been thoroughly investigated, there is little information concerning their role in HM stress tolerance. In the present study, we investigated the role of durum wheat TdSHN1 TF in HM response and tolerance. Results showed that TdSHN1 expression was strongly induced by Cd, Cu, and Zn in durum wheat seedlings. In addition, TdSHN1 gene promoter directed HM-inducible GUS gene expression in transgenic tobacco. Overexpression of TdSHN1 encoding cDNA in transgenic yeast and tobacco conferred Cd, Cu, and Zn tolerances. Interestingly, transgenic tobacco lines exhibited longer roots and greater biomass accumulation, retained more chlorophyll, and produced less ROS than WT plants, when subjected to excess HMs. In addition, transgenic tobacco lines had higher activities of ROS-scavenging enzymes (SOD and CAT) which might have contributed to their HM tolerance. This study suggested that TdSHN1 is a potential candidate for improving HM tolerance in plants and phytoremediation of HM-contaminated soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ABRE:

ABA-responsive element

AP2/ERF:

APETALA2/ethylene-responsive element binding factor

CuRE:

Copper response element

CAT:

Catalase

DRE:

Dehydration-responsive factor

ERF:

Ethylene-responsive factor

HMs:

Heavy metals

MRE :

Metal-responsive element

MDA:

Malondialdehyde

NBT:

Azide-insensitive nitroblue tetrazolium

O2 :

Superoxide anion

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TF:

Transcription factor

References

  • Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working paper No. 12-03. Rome, FAO

  • Antosiewicz DM, Barabasz A, Siemianowski O (2014) Phenotypic and molecular consequences of overexpression of metal-homeostasis genes. Front Plant Sci 5:80

    Article  PubMed  PubMed Central  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species, metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Aprile A, Sabella E, Vergine M, Genga A, Siciliano M, Nutricati E, Rampino P, De Pascali M, Luvisi A, Negro C, De Bellis L (2018) Activation of a gene network in durum wheat roots exposed to cadmium. BMC Plant Biol 18:238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arteca RN, Arteca JM (2007) Heavy-metal-induced ethylene production in Arabidopsis thaliana. J Plant Physiol 164:1480–1488

    Article  CAS  PubMed  Google Scholar 

  • Asgher M, Khan NA, Khan MI, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61

    Article  CAS  PubMed  Google Scholar 

  • Ayangbenro AS, Babalola OO (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14:94

    Article  PubMed Central  Google Scholar 

  • Banerjee A, Roychoudhury A (2015) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17

    Article  Google Scholar 

  • Bertrand M, Poirier I (2005) Photosynthetic organisms and excess of metals. Photosynthetica 43:45–353

    Article  Google Scholar 

  • Broadley MR, Willey NJ, Wilkins JC, Baker AJM, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152:9–27

    Article  CAS  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Cao F, Chen F, Sun H, Zhang G, Chen ZH, Wu F (2014) Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genomics 15:611

    Article  PubMed  PubMed Central  Google Scholar 

  • Caspi V, Droppa M, Horváth G, Malkin S, Marder JB, Raskin VI (1999) The effect of copper on chlorophyll organization during greening of barley leaves. Photosynth Res 62:165–174

    Article  CAS  Google Scholar 

  • Chen Y, Yang X, Kun H, Liu M, Li J, Gao Z et al (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:124

    Google Scholar 

  • Cui J, Zhao Y, Lu Y, Chan T, Zhang L, Tsang DCW, Li X (2019) Distribution and speciation of copper in rice (Oryza sativa L.) from mining impacted paddy soil: Implications for copper uptake mechanisms. Environ Int 126:717–726

    Article  CAS  PubMed  Google Scholar 

  • Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Yvese G, Jana C, Jacoa V (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316

    Article  CAS  PubMed  Google Scholar 

  • Cuypers A, Bohler S, Opdenkker K, Remans T (2012) Cadmium and copper stress induce a cellular oxidative challenge leading to damage versus signaling. In: Gupta DK, Sandalio ML (eds) Metal toxicity in plants: perception, signaling and remediation. Springer- Verlag, Berlin, pp 65–90

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dey SK (2011) Alterations of antioxidative enzymes activities and induction of lipid peroxidation in germinating wheat seeds subjected to cadmium stress. J Life Sci 5:22–28

    CAS  Google Scholar 

  • Djemal R, Khoudi H (2015) Isolation and molecular characterization of a novel WIN1/SHN1 ethylene-responsive transcription factor TdSHN1 from durum wheat (Triticum turgidum. L. subsp. durum). Protoplasma 252:1461–1473

    Article  CAS  PubMed  Google Scholar 

  • Djemal R, Khoudi H (2016) TdSHN1, a WIN1/SHN1-type transcription factor, imparts multiple abiotic stress tolerance in transgenic tobacco. Environ Exp Bot 131:89–100

    Article  CAS  Google Scholar 

  • Djemal R, Khoudi H (2019) Combination of the endogenous promoter-intron significantly improves salt and drought tolerance conferred by TdSHN1 transcription factor in transgenic tobacco. Plant Physiol Biochem 139:435–445

    Article  CAS  PubMed  Google Scholar 

  • Djemal R, Mila I, Bouzayen M, Pirrello J, Khoudi H (2018) Molecular cloning and characterization of a novel WIN1/SHN1 ethylene-responsive transcription HvSHN1 in barley (Hordeum vulgare L.). J Plant Physiol 228:39–46

    Article  CAS  PubMed  Google Scholar 

  • Ebrahimi M, Khalili N, Razi S, Keshavarz-Fathi M, Khalili N, Rezaei N (2020) Effects of lead and cadmium on the immune system and cancer progression. J Environ Health Sci Eng 18:335–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emanuelli T, Milbradt BG, Callegaro MGK, Augusti PR (2014) Wheat bran and cadmium in human health. In: Watson RR, Preedy VR, Zibadi S (eds.) Wheat and Rice in Disease Prevention and Health. Academic Press, San Diego, 241-260

  • FAO and ITPS Status of the World’s Soil Resources (SWSR)-Technical Summary (2015) Food and agriculture organization of the united nations and intergovernmental technical panel on soils, Rome, Italy

  • Farinati S, DalCorso G, Varotto S, Furini A (2010) The Brassica juncea BjCdR15, an ortholog of Arabidopsis TGA3, is a regulator of cadmium uptake, transport and accumulation in shoots and confers cadmium tolerance in transgenic plants. New Phytol 185:964–978

    Article  CAS  PubMed  Google Scholar 

  • Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23:412–427

    Article  CAS  PubMed  Google Scholar 

  • Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534

  • Gibbs DJ, Conde JV, Berckhan S, Prasad G, Mendiondo GM, Holdsworth MJ (2015) Group VII ethylene response factors coordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiol 169:23–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giuntoli B, Perata P (2018) Group VII ethylene response factors in Arabidopsis: regulation and physiological roles. Plant Physiol 176:1143–1155

    Article  CAS  PubMed  Google Scholar 

  • Gouiaa S, Khoudi H (2019) Expression of V-PPase proton pump, singly or in combination with a NHX1 transporter, in transgenic tobacco improves copper tolerance and accumulation. Environ Sci Pollut Res 26:37037–37045

    Article  CAS  Google Scholar 

  • Groppa MD, Tomaro ML, Benavides MP (2001) Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci 161:481–488

    Article  CAS  Google Scholar 

  • Guan Z, Chai T, Zhang Y, Xu J, Wei W (2009) Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA. Chemosphere 76:623–630

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Hong C, Chen X, Xu Y, Liu Y, Jiang D, Zheng B (2016) Different growth and physiological responses to cadmium of the three Miscanthus species. PLoS One 11:e0153475

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall J, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613

    Article  CAS  PubMed  Google Scholar 

  • Hess N, Klode M, Anders M, Sauter M (2011) The hypoxia responsive transcription factor genes ERF71/HRE2 and ERF73/HRE1 of Arabidopsis are differentially regulated by ethylene. Physiol Plant 143:41–49

    Article  CAS  PubMed  Google Scholar 

  • Hollenbach B, Schreiber L, Hartung W, Dietz KJ (1997) Cadmium leads to stimulated expression of the lipid transfer protein genes in barley: implications for the involvement of lipid transfer proteins in wax assembly. Planta 203:9–19

    Article  CAS  PubMed  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycine betaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597

    Article  CAS  PubMed  Google Scholar 

  • Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136:3276–3283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabir AH, Rahman MM, Das U, Sarkar U, Roy NC, Reza MA, Talukder MR, Uddin MA (2019) Reduction of cadmium toxicity in wheat through plasma technology. PLoS One 14:e0214509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal induced oxidative stress and plant mitochondria. Int J Mol Sci 12:6894–6918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keunen E, Schellingen K, Vangronsveld J, Cuypers A (2016) Ethylene and metal stress: small molecules, big molecules. Front Plant Sci 7:23

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan MI, Khan NA (2014) Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma 251:1007–1019

    Article  CAS  PubMed  Google Scholar 

  • Khan A, Sardar K, Khan MA, Zahir Q, Waqas M (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res 22:13772–13799

    Article  CAS  Google Scholar 

  • Khoudi H, Maatar Y, Gouiaa S, Masmoudi K (2012) Transgenic tobacco plants expressing ectopically wheat H+-pyrophosphatase (H+-PPase) gene TaVP1 show enhanced accumulation and tolerance to cadmium. J Plant Physiol 169:98–103

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous over expression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    Article  CAS  PubMed  Google Scholar 

  • Li C, Yang X, Xu Y, Li L, Wang Y (2018) Cadmium detoxification induced by salt stress improves cadmium tolerance of multi-stress-tolerant Pichia kudriavzevii. Environ Pollut 242:845–854

    Article  CAS  PubMed  Google Scholar 

  • Lin CH, Peng PH, Ko CY, Markhart AH, Lin TY (2012) Characterization of a novel Y2K-type dehydrin VrDhn1 from Vigna radiata. Plant Cell Physiol 53:930–942

    Article  CAS  PubMed  Google Scholar 

  • Lin CY, Nam TN, Fu SF, Hsiung YC, Chia LC, Lin CW et al (2013) Comparison of early transcriptome responses to copper and cadmium in rice roots. Plant Mol Biol 81:507–522

    Article  CAS  PubMed  Google Scholar 

  • Lin T, Yang W, Lu W, Wang Y, Qi X (2017) Transcription factors PvERF15 and PvMTF-1 form a cadmium stress transcriptional pathway. Plant Physiol 173:1565–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, He X, Feng T, Renying Z, Wenmin Q, Han X, Qia G, Zhang D (2019) cDNA library for mining functional genes in Sedum alfredii Hance related to cadmium tolerance and characterization of the roles of a novel SaCTP2 gene in enhancing cadmium hyperaccumulation. Environ Sci Technol 53:10926–10940

    Article  CAS  PubMed  Google Scholar 

  • Manios T, Stentiford EI, Millner PA (2003) The effect of heavy metals accumulation on the chlorophyll concentration of Typha latifolia plants, growing in a substrate containing sewage sludge compost and watered with metaliferus water. Ecol Eng 20:65–74

    Article  Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ 35:524–533

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochem Biophys Acta 1819:86–96

    CAS  PubMed  Google Scholar 

  • Morina F, Jovanovic L, Mojovic M, Vidovic M, Pankovic D, Veljovic Jovanovic S (2010) Zinc-induced oxidative stress in Verbascum thapsus is caused by an accumulation of reactive oxygen species and quinhydrone in the cell wall. Physiol Plant 140:209–224

    CAS  PubMed  Google Scholar 

  • Müller M, Munné-Bosh S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 169:32–41

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Murtaza G, Javed W, Hussain A, Wahid A, Murtaza A, Owens G (2015) Metal uptake via phosphate fertilizer and city sewage in cereal and legume crops in Pakistan. Environ Sci Pollut Res 22:9136–9147

    Article  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Opdenakker K, Remans T, Keunen E, Vangronsveld J, Cuypers A (2012) Exposure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated alterations in MAPKinase transcript levels. Environ Exp Bot 83:53–61

    Article  CAS  Google Scholar 

  • Papdi C, Pérez-Salamó I, Joseph MP, Giuntoli B, Bögre L, Koncz C, Szabados L (2015) The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12, RAP2.2 and RAP2.3. Plant J 82:772–784

    Article  CAS  PubMed  Google Scholar 

  • Park HY, Seok HY, Woo DH, Lee SY, Tarte VN, Lee EH, Lee CH, Moon YH (2011) AtERF71/HRE2 transcription factor mediates osmotic stress response as well as hypoxia response in Arabidopsis. Biochem Biophys Res Commun 414:135–141

    Article  CAS  PubMed  Google Scholar 

  • Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Paunov M, Koleva L, Vassilev A, Vangronsveld J, Goltsev V (2018) Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. Int J Mol Sci 19:787

    Article  PubMed Central  Google Scholar 

  • Pietrini F, Zacchini M, Iori V, Pietrosanti L, Bianconi D, Massacci A (2009) Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. Inter J Phytoremed 12:105–120

    Article  Google Scholar 

  • Qiu CH, Li H, Li J, Qin RY, Xu RF, Yang YC, Ma H, Song FS, Li L, Wei PC, Yang JB (2015) Isolation and characterization of three cadmium-inducible promoters from Oryza sativa. J Biotechnol 216:11–19

    Article  CAS  PubMed  Google Scholar 

  • Repkina NS, Talanova VV, Topchieva LV, Batova YV, Titov AF (2012) Effect of cadmium on gene expression of the transcription factors CBF1 and DREB1 in wheat seedling leaves. Trudy Karel'skogo nauchnogo tsentra RAN Ser Eksperimental'naya biologiya 2:113–118

    Google Scholar 

  • Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gomez M, Del Rio LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357

    Article  CAS  PubMed  Google Scholar 

  • Ruduś I, Sasiak M, Kêpczyñski J (2012) Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylate oxidase (ACO) gene. Acta Physiol Plant 35:295–307

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Searle PF, Stuart GW, Palmiter R (1987) Metal regulatory elements of the mouse metallothionein-I gene. In: Kägi JR, Kojima Y (eds) MetallothioneinII. Birkhäuser, Basel, pp 407–414

    Chapter  Google Scholar 

  • Shahid M, Ferrand E, Schreck E, Dumat C (2013) Behavior and impact of zirconium in the soil-plant system: plant update and phytotoxicity. Rev Environ Contam Toxicol 221:107–127

    CAS  PubMed  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    Article  CAS  PubMed  Google Scholar 

  • Sharma A, Kumar V, Shahzad B, Ramakrishnan M, Singh Sidhu GP, Bali AS, Handa N, Kapoor D, Yadav P, Khanna K, Bakshi P, Rehman A, Kohli SK, Khan EA, Parihar RD, Yuan H, Thukral AK, Bhardwaj R, Zheng B (2020) Photosynthetic response of plants under different abiotic stresses: a review. J Plant Growth Regul 39:509–531

    Article  CAS  Google Scholar 

  • Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologues of the classA4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21:4031–4043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoji T, Mishima M, Hashimoto T (2013) Divergent DNA-binding specificities of a group of ethylene response factor transcription factors involved in plant defense. Plant Physiol 162:977–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh NK, Rai UN, Tewari A, Singh M (2010) Metal accumulation and growth response in Vigna radiata L. inoculated with chromate tolerant rhizobacteria and grown on tannery sludge amended soil. Bull Environ Contam Toxicol 84:118–124

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Parihar P, Singh R, Prasad SM (2016) An assessment to show toxic nature of beneficial trace metals: too much of good thing can be bad. Int J Curr Multidiscip Stud 2:141–144

    Google Scholar 

  • Singh H, Kumar D, Soni V (2020) Copper and mercury induced oxidative stresses and antioxidant responses of Spirodela polyrhiza (L.). Biochem Biophys Rep 23:100781

    PubMed  PubMed Central  Google Scholar 

  • Smeets K, Opdenakker K, Remans T, Forzani C, Hirt H, Vangronsveld J, Cuypers A (2013) The role of the kinase OXI1 in cadmium and copper-induced molecular responses in Arabidopsis thaliana. Plant Cell Environ 36:1228–1238

    Article  CAS  PubMed  Google Scholar 

  • Sun N, Liu M, Zhang W, Yang W, Bei X, Ma H, Qiao F, Qi X (2015) Bean metal-responsive element-binding transcription factor confers cadmium resistance in tobacco. Plant Physiol 167:1136–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617

    Article  CAS  PubMed  Google Scholar 

  • Tran LSP, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1:32–39

    Article  PubMed  Google Scholar 

  • Vaillant N, Monnet F, Hitmi A, Sallanon H, Coudret A (2005) Comparative study of responses in four Datura species to a zinc stress. Chemosphere 59:1005–1013

    Article  CAS  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Yang C, Gao C, Wang Y (2009a) Cloning and expression analysis of 14 lipid transfer protein genes from Tamarix hispida responding to different abiotic stresses. Tree Physiol 29:1607–1619

    Article  PubMed  Google Scholar 

  • Wang C, Zhang SH, Wang PF, Qian J, Hou J, Zhang WJ, Lu J (2009b) Excess Zn alters the nutrient uptake and induces the antioxidative responses in submerged plant Hydrilla verticillata (L.f.) Royle. Chemosphere 76:938–945

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Cui Y, Fan H, Huang Z, Yuan Y, Wu H, Ling HQ (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6:503–513

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang C, Sheng H, Wang Y, Zheng J, Kang H, Fan X, Sha L, Zhang H, Zhou Y (2017) Transcriptome-wide identification and expression analyses of ABC transporters in dwarf polish wheat under metal stresses. Biol Plant 61:293–304

    Article  CAS  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+ hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    Article  CAS  PubMed  Google Scholar 

  • Xian J, Wang Y, Niu K, Ma H, Ma X (2020) Transcriptional regulation and expression network responding to cadmium stress in a Cd-tolerant perennial grass Poa Pratensis. Chemosphere 250:126158

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Zhang YX, Wei W, Han L, Guan ZQ, Wang Z, Chai TY (2008) BjDHNs confer heavy-metal tolerance in plants. Mol Biotechnol 38:91–98

    Article  CAS  PubMed  Google Scholar 

  • Xynias IN, Mylonas I, Korpetis EG, Ninou E, Tsaballa A, Avdikos ID, Mavromatis AG (2020) Durum wheat breeding in the Mediterranean region: Current status and future prospects. Agronomy 10:432

  • Yang H, Yu C, Yan J, Wang X, Chen F, Zhao Y, Wei W (2014) Overexpression of the Jatropha curcas JcERF1 gene coding an AP2/ERF-type transcription factor increases tolerance to salt in transgenic tobacco. Biochemistry (Mosc) 79:1226–1236

    Article  CAS  Google Scholar 

  • Yang C, Lu X, Ma B, Chen SY, Zhang JS (2015) Ethylene signaling in rice and Arabidopsis: conserved and diverged aspects. Mol Plant 8:495–505

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Wu H, Ping J (2019) Simultaneous determination of Cd (II) and Pb (II) ions in honey and milk samples using a single-walled carbon nanohorns modified screen-printed electrochemical sensor. Food Chem 274:8–15

    Article  CAS  PubMed  Google Scholar 

  • Ying RR, Qiu RL, Tang YT, Hu PJ, Qiu H, Chen HR, Shi TH, Morel JL (2010) Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata. J Plant Physiol 167:81–87

    Article  CAS  PubMed  Google Scholar 

  • Youm JW, Jeon JH, Choi D, Yi SY, Joung H, Kim HS (2008a) Ectopic expression of pepper CaPF1 in potato enhances multiple stresses tolerance and delays initiation of in vitro tuberization. Planta 228:701–708

    Article  CAS  PubMed  Google Scholar 

  • Youm JW, Jeon JH, Choi D, Yi SY, Joung H, Kim HS (2008b) Ectopic expression of pepper CaPF1 in potato enhances multiple stresses tolerance and delays initiation of in vitro tuberization. Planta 228:701–708

    Article  CAS  PubMed  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430

    Article  CAS  PubMed  Google Scholar 

  • Yu Z, Wang X, Zhang L (2018) Structural and functional dynamics of dehydrins: a plant protector protein under abiotic stress. Int J Mol Sci 19:3420

    Article  PubMed Central  Google Scholar 

  • Yuan J, Bai Y, Chao Y, Sun X, He C, Liang X, Xie L, Han L (2018) Genome-wide analysis reveals four key transcription factors associated with cadmium stress in creeping bentgrass (Agrostis stolonifera L.). Peer J 6:e5191

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang P, Wang R, Ju Q, Li W, Tran LSP, Xu J (2019) The R2R3-MYB transcription factor MYB49 regulates cadmium accumulation. Plant Physiol 180:529–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by a grant from the Tunisian Ministry of Higher Education and Scientific Research (contrat programme LBAP).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Habib Khoudi.

Additional information

Handling Editor: Néstor Carrillo

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 15 kb)

ESM 2

(PPTX 170 kb)

ESM 3

(PPTX 94 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Djemal, R., Khoudi, H. The ethylene-responsive transcription factor of durum wheat, TdSHN1, confers cadmium, copper, and zinc tolerance to yeast and transgenic tobacco plants. Protoplasma 259, 19–31 (2022). https://doi.org/10.1007/s00709-021-01635-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-021-01635-z

Keywords

Navigation