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Mechanisms of cadmium-stress avoidance by selenium in tomato plants

Abstract

Cadmium (Cd) is probably the most damaging metal to plant species; with a long biological half-life, it can be taken up by plants, disrupting the cell homeostasis and triggering several metabolic pathways. Selenium (Se) improves plant defence systems against stressful conditions, but the biochemical antioxidant responses to Cd stress in tomato plants is poorly understood. To further address the relationship of Cd-stress responses with Se mineral uptake, Cd and Se concentration, proline content, MDA and H2O2 production, and the activity of SOD, APX, CAT and GR enzymes were analyzed in Micro-Tom (MT) plants submitted to 0.5 mM Cd. The results revealed different responses according to Se combination and Cd application. For instance, roots and leaves of MT plants treated with Se exhibited an increase in dry mass and nutritional status, exhibited lower proline content and higher APX and GR activities when compared with plants with no Se application. Plants submitted to 0.5 mM Cd, irrespective of Se exposure, exhibited lower proline, MDA and H2O2 content and higher SOD, CAT and GR activities. Selenium may improve tolerance against Cd, which allowed MT plants exhibited less oxidative damage to the cell, even under elevated Cd accumulation in their tissues. The results suggest that Se application is an efficient management technique to alleviate the deleterious effects of Cd-stress, enhancing the nutritional value and activity of ROS-scavenging enzymes in tomato plants.

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References

  • Abd AEF, Hashem A, Alqarawi AA (2016) Mitigation of cadmium induced stress in tomato. (Solanum lycopersicum L.) by selenium. Pak J Bot 48:953–961

    CAS  Google Scholar 

  • Alves LR, Monteiro CC, Carvalho RF, Cury PR, Tezotto T, Azevedo RA, Gratão PL (2017) Cadmium stress related to root-to-shoot communication depends on ethylene and auxin in tomato plants. Environ Exp Bot 134:102–115

    CAS  Article  Google Scholar 

  • Alves LR, Reis AR, Gratão PL (2016) Heavy metals in agricultural soils: from plants to our daily life(a review). Cientifica 44:346–361

    Article  Google Scholar 

  • Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R, Ahmad P (2018) Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255:459–469

    CAS  Article  Google Scholar 

  • Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Responses of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and catalase-deficient mutant of barley. Physiol Plant 104:280–292

    CAS  Article  Google Scholar 

  • Barbosa JC, Maldonado W Jr (2009) Software AgroEstat:Sistema de análises estatísticas de ensaios agronômicos. Universidade Estadual Paulista, Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal, SP, Brasil

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Article  Google Scholar 

  • Boaretto LF, Carvalho G, Borgo L, Creste S, Landell MGA, Mazzafera P, Azevedo RA (2014) Water stress reveals differential antioxidant responses of tolerant and non-tolerant sugarcane genotypes. Plant Physiol Biochem 74:165–75

    CAS  Article  Google Scholar 

  • Borges KLR, Hippler FWR, Carvalho MEA, Nalin RS, Matias FI, Azevedo RA (2019) Nutritional status and root morphology of tomato under Cd-induced stress: comparing contrasting genotypes for metal-tolerance. Sci Hortic 246:518–527

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Cartes P, Jara AA, Pinilla L, Rosas A, Mora ML (2010) Selenium improves the antioxidant ability against aluminium‐induced oxidative stress in ryegrass roots. Ann Appl Biol 156(2):297–307

    CAS  Article  Google Scholar 

  • Castillo-Godina RG, Foroughbakhch-Pournavab R, Benavies-Mendonza A (2016) Effect of selenium on elemental concentration and antioxidant enzymatic activity of tomato plants. J Agr Sci Technol 18:233–244

    Google Scholar 

  • Chmielowska-Bak J, Gzyl J, Rucinska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:1–13

    Google Scholar 

  • Chilimba ADC, Young SD, Black CR, Rogerson KB, Ander EL, Watts MJ, Lammel J, Broadley MR (2011) Maize grain and soil surveys reveal suboptimal dietary selenium intake is widespread in Malawi. Sci Rep 1:1–9

    Article  CAS  Google Scholar 

  • Clemens S, Feng MaJ (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:1–12

    Article  CAS  Google Scholar 

  • Edelstein M, Ben-Hur M (2018) Heavy metals and metalloids: sources, risks and strategies to reduce their accumulation in horticultural crops. Sci Hortic 234:431–444

    CAS  Article  Google Scholar 

  • Feng R, Wei C, Tu S (2013) The roles of selenium in protecting plants against abiotic stresses. Environ Exp Bot 87:58–68

    CAS  Article  Google Scholar 

  • Gratão PL, Monteiro CC, Carvalho RF, Tezotto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissection of diageotropica and Never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96

    Article  CAS  Google Scholar 

  • Gratão PL, Monteiro CC, Tezotto T, Carvalho RF, Alves LR, Peters LJ, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. BioMetals 28:803–816

    Article  CAS  Google Scholar 

  • Handa N, Kohli SK, Sharma A, Thukral AK, Bhardwaj R, Alyemeni MN, Wijaya L, Ahmad P (2018) Protective role of selenium against chromium stress involving metabolites and essential elements in Brassica juncea L. seedlings. 3Biotech 8:66

    Google Scholar 

  • Huang G, Ding C, Guo F, Li X, Zhang T, Wang X (2017) Underlying mechanisms and effects of hydrated lime and selenium application on cadmium uptake by rice (Oryza sativa L.) seedlings. Environ Sci Pollut Res 24:18926–18935

    CAS  Article  Google Scholar 

  • Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Bio Plant 59:609–619

    CAS  Article  Google Scholar 

  • Kaur S, Kaur N, Siddique KH, Nayyar H (2016) Beneficial elements for agricultural crops and their functional relevance in defence against stresses. Arch Agron Soil Sci 62:905–920

    Article  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    CAS  Article  Google Scholar 

  • Li HF, McGrath SP, Zhao FJ (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytol 178:92–102. https://doi.org/10.1111/j.1469-8137.2007.02343.x

    CAS  Article  Google Scholar 

  • Li X, Li B, Yang Y (2018) Effects of foliar selenite on the nutrient components of turnip (Brassica rapa var. rapa Linn.). Front Chem 6:42

    Article  CAS  Google Scholar 

  • Lichtentlaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1

    Article  Google Scholar 

  • Lin L, Zhou W, Dai H, Cao F, Zhang G, Wu F (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mater 235:343–351

    Article  CAS  Google Scholar 

  • Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    CAS  Article  Google Scholar 

  • Ma Q, Cao X, Tan X, Si L, Wu L (2017) Effects of cadmium stress on pakchoi (Brassica chinensis L.) growth and uptake of inorganic and organic nitrogenous compounds. Environ Exp Bot 137:49–57

    CAS  Article  Google Scholar 

  • Meissner R, Jacobson Y, Melamed S, Levyatuv S, Shalev G, Ashri A, Elkind Y, Levy A (1997) A new model system for tomato genetics. Plant J 12:1465–1472

    CAS  Article  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489

    Article  CAS  Google Scholar 

  • Noctor G, Foyer CH (2016) Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol 171:1581–1592

    CAS  Article  Google Scholar 

  • Noctor G, Reichheld JP, Foyer CH (2018) ROS-related redox regulation and signaling in plants. Semin Cell Dev Biol 80:3–12

    CAS  Article  Google Scholar 

  • Nogueirol RC, Monteiro FA, Gratão PL, Borgo L, Azevedo RA (2015) Tropical soils with high aluminum concentrations cause oxidative stress in two tomato genotypes. Environ Monit Assess 187:73

    Article  CAS  Google Scholar 

  • Pezzarossa B, Rosellini I, Borghesi E, Tonutti P, Malorgio F (2014) Effects of Se-enrichment on yield, fruit composition and ripening of tomato (Solanum lycopersicum) plants grown in hydroponics. Sci Hortic 165:106–110

    CAS  Article  Google Scholar 

  • Rabêlo FHS, Lux A, Rossi ML, Martinelli AP, Cuypers A, Lavres JJ (2018) Adequate S supply reduces the damage of high Cd exposure in roots and increases N, S and Mn uptake by Massaigrass grown in hydroponics. Environ Exp Bot 148:35–46

    Article  CAS  Google Scholar 

  • Reis AR, Barcelos JPQ, Osório CRWS, Santos E, Lisboa LAM, Santini JMK, Santos MJD, Furlani Jr E, Campos M, Figueiredo PAM, Lavres J, Gratão PL (2017) A glimpse into the physiological, biochemical and nutritional status of soybean plants under Ni-stress conditions. Environ Exp Bot 144:78–87

    Article  CAS  Google Scholar 

  • Reis HPG, Barcelos JPQ, Furlani Junior E, Santos EF, Silva VM, Moraes MF, Putti FF, Reis AR (2018) Agronomic biofortification of upland rice with selenium and nitrogen and its relation to grain quality. J Cereal Sci 79:508–515

    CAS  Article  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, delRío LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisumsativum L.) roots: imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544

    Article  CAS  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Saidi I, Nawel N, Djebali W (2014) Role of selenium in preventing manganese toxicity in sunflower (Helianthus annuus) seedling. S Afr J Bot 94:88–94

    CAS  Article  Google Scholar 

  • Santos EF, Macedo FG, Zanchim BJ, Lima GPP, Lavres J (2017) Prognosis of physiological disorders in physic nut to N, P, and K deficiency during initial growth. Plant Physiol Biochem 115:249–258

    CAS  Article  Google Scholar 

  • Schützendubel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898

    Article  Google Scholar 

  • Sebastian A, Prasad MNV (2015) Trace element management in rice. Agron 5:374–404

    CAS  Article  Google Scholar 

  • Seppänen M, Turakainen M, Hartikainen H (2003) Selenium effects on oxidative stress in potato. Plant Sci 165:311–319

    Article  CAS  Google Scholar 

  • Silva VM, Boleta EHM, Lanza MGDB, Lavres J, Martins JT, Santos EF, Broadley MR (2018) Physiological, biochemical, and ultrastructural characterization of selenium toxicity in cowpea plants. Environ Exp Bot 150:172–182

    CAS  Article  Google Scholar 

  • Sun H, Dai H, Wang X, Wang G (2016) Physiological and proteomic analysis of selenium-mediated tolerance to Cd stress in cucumber (Cucumis sativus L.). Ecotoxicol Environ Saf 133:114–126

    CAS  Article  Google Scholar 

  • Vincent JM (1975) Manual practico de rizobiologia, 1st ed. Hemisferio Sur, Buenos Aires

    Google Scholar 

  • Xue T, Hou S, Tan J, Liu GL (1993) The antioxidative function of selenium in higher plants: II. Non-enzymatic mechanisms. Chin Sci Bull 38:356–358

    Article  Google Scholar 

  • Wan Y, Yu Y, Wang Q, Qiao Y, Li H (2016) Cadmium uptake dynamics and translocation in rice seedling: influence of different forms of selenium. Ecotoxicol Environ Saf 133:127–134

    CAS  Article  Google Scholar 

  • Wu Z, Liu S, Zhao J, Wang F, Du Y, Zou S, Huang Y (2017) Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress. Environ Exp Bot 133:1–11

    Article  CAS  Google Scholar 

  • 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 Physiol 172:1899–1910

    CAS  Article  Google Scholar 

  • 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 Arabidopsis thaliana. Plant Cell Physiol 57:2353–2366

    CAS  Article  Google Scholar 

  • Yao X, Jianzhou C, Xueli H, Binbin L, Jingmin L, Zhaowei Y (2013) Effects of selenium on agronomical characters of winter wheat exposed to enhanced ultraviolet-B. Ecotoxicol Environ Saf 92:320–326

    CAS  Article  Google Scholar 

  • Zayed AM, Terry N (1992) Selenium volatilization in broccoli as influenced by sulfate supply. J Plant Physiol 140:646–652

    CAS  Article  Google Scholar 

  • Zembala M, Filek M, Walas S, Mrowiec H, Kornas A, Miszalski Z, Hartikainen H (2010) Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil 329:457–468

    CAS  Article  Google Scholar 

  • Zhu G, Xiao H, Guo Q, Zhang Z, Zhao J, Yang D (2018) Effects of cadmium stress on growth and amino acid metabolism in two compositae plants. Ecotoxicol Environ Saf 158:300–308

    CAS  Article  Google Scholar 

  • Zouari M, Ahmed CB, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Abdallah FB, Rouina BB (2016) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defence system of Oleaeuropaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Saf 128:195–205

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors thank to Prof. Dr José Carlos Barbosa (Universidade Estadual Paulista—UNESP—Faculdade de Ciências Agrárias e Veterinárias. Departamento de Ciências Exatas, Brazil) for the collaboration in statistical analyses.

Funding

This work was funded by Fundação de Amparo à Pesquisa do Estadode São Paulo (FAPESP - Grant n°2017/04787-6); PLG also thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research fellowship (Grant nº 314380/2018-3) – Brazil; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (L.R.A.) for the scholarship granted (Finance Code 001).

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Correspondence to Priscila Lupino Gratão.

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Alves, L.R., Prado, E.R., de Oliveira, R. et al. Mechanisms of cadmium-stress avoidance by selenium in tomato plants. Ecotoxicology 29, 594–606 (2020). https://doi.org/10.1007/s10646-020-02208-1

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Keywords

  • Abiotic stress
  • Antioxidant metabolism
  • Selenium
  • Solanum lycopersicum