Possible mechanism of medium-supplemented thiourea in improving growth, gas exchange, and photosynthetic pigments in cadmium-stressed maize (Zea mays)

Abstract

Cadmium (Cd) stress is highly damaging to plant growth but its toxicity can be alleviated with exogenous supply of growth promoters. In this greenhouse study, we determined the effectiveness of medium-supplemented thiourea (TU) in improving growth, leaf gas exchange, and photosynthetic pigments contents. Pak-Afgoi (Cd-tolerant) and EV-20 (Cd-sensitive) maize (Zea mays L.) varieties were grown in pots containing sand supplemented with nutrient solution for 30 days. The plants were treated with 1,000 µM or without Cd. On the appearance of Cd-toxicity symptoms (in about 10 days), a pre-optimized level of TU (0.25 mM) was supplemented in the rooting medium, and plants were allowed to grow for further 15 days. Data for various growths, leaf gas exchange characteristics, chlorophyll (Chl), and carotenoids (Car) contents were recorded in spring (February–April) and autumn (August–October) seasons. Results showed that Cd-stress significantly decreased length, fresh and dry weight of shoot and root, number of green leaves and leaf area per plant, net photosynthetic rate (P n), transpiration rate (TR), stomatal conductance (g s), Chl-a, -b, Chl-a-to-b ratio, and Car but increased substomatal CO2 concentration (C i ) in the varieties in both the seasons. Although Cd was toxic to maize, medium-supplemented TU nullified the Cd-toxicity as was evident from improved growth, P n, g s, and Chl-b and Car contents in both varieties. Overall, 0.25 mM TU level was quite effective in reducing the Cd-toxicity on both the maize varieties; especially, sensitive maize more profoundly responded to Cd-toxicity under medium supplementation of TU. Cd-tolerance produced by TU was superior in the autumn- than in spring-grown maize. From the reduced Cd content of leaf and root, the results suggested a possible role of TU in reducing Cd-availability to the root and its transport to shoot. Presence of thiol group in TU appears to be important to Cd-binding/inactivation, and thus its tolerance by maize.

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References

  1. Akladious SA (2014) Influence of thiourea application on some physiological and molecular criteria of sunflower (Helianthus annuus L.) plants under conditions of heat stress. Protoplasma 251:625–638

    Article  CAS  PubMed  Google Scholar 

  2. Amirjani MR (2012) Effects of cadmium on wheat growth and some physiological factors. Int J For Soil Eros 2:50–58

    Google Scholar 

  3. Anjum F, Wahid A, Farooq M, Javed F (2011) Potential of foliar applied thiourea in improving salt and high temperature tolerance of bread wheat (Triticum aestivum L.). Int J Agric Biol 13:251–256

    Google Scholar 

  4. Asthir B, Thapar R, Farooq M, Bains NS (2013) Exogenous application of thiourea improves the performance of late sown wheat by inducing terminal heat resistance. Int J Agric Biol 15:1337–1342

    CAS  Google Scholar 

  5. Bahmani R, Bihamta MR, Habibi D, Forozesh P, Ahmad SI (2012) Effect of cadmium chloride on growth parameters of different bean genotypes (Phaseolus vulgaris L.). ARPN J Agric Biol Sci 7:35–40

    CAS  Google Scholar 

  6. Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64

    Article  CAS  Google Scholar 

  7. Bansal P, Sharma P (2000) Effect of Pb24 and Cd on respiration and mitochondrial electron transport chain in germinating pea seeds (Pisum sativum). Ind J Environ Ecol 3:249–254

    Google Scholar 

  8. Baryla A, Carrier P, Franck F, Coulomb C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium polluted soil, causes and consequences for photosynthesis and growth. Planta 212:696–709

    Article  CAS  PubMed  Google Scholar 

  9. Cao H, Wang J, Zhang X (2007) Ecotoxicity of cadmium to maize and soybean seedlings in black soil. Chin Geogr Sci 17:270–274

    Article  Google Scholar 

  10. Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Bot Stud 52:41–46

    CAS  Google Scholar 

  11. Costa G, Michaut J, Morel J (1994) Influence of cadmium on water relations and gas exchanges in phosphorus deficient Lupinus albus. Plant Physiol Biochem 32:105–114

    CAS  Google Scholar 

  12. Dalla Vecchia F, La Rocca N, Moro I, De Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages suffered by submerged leaves of Elodea canadensis exposed to cadmium. Plant Sci 168:329–338

    Article  CAS  Google Scholar 

  13. Dat J, Vandenabeele S, Iranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  PubMed  Google Scholar 

  14. Davies BH (1976) Carotenoids. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments, vol 2. Academic Press, London, pp 38–165

    Google Scholar 

  15. Day SD, Wiseman PE, Dickinson SB, Harris JR (2010) Tree root ecology in the urban environment and implications for a sustainable rhizosphere. Arboric Urban For 36:193–205

    Google Scholar 

  16. de Pascale S, Maggio A, Fogliano V, Ambrosino P, Ritieni A (2001) Irrigation with saline water improves carotenoids content and antioxidant activity of tomato. J Hortic Sci Biotechnol 76:447–453

    Google Scholar 

  17. El-Beltagi HS, Mohamed AA, Rashed MM (2010) Response of antioxidative enzymes to cadmium stress in leaves and roots of radish (Rahpanus sativus L.). Not Sci Biol 2:76–82

    CAS  Google Scholar 

  18. Faizan S, Kausar S, Perveen R (2011) Varietal differences for cadmium-induced seedling mortality, foliar toxicity symptoms, plant growth, proline and nitrate reductase activity in chickpea (Cicer arietinum L). Biol Med 3:196–206

    CAS  Google Scholar 

  19. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2008) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212

    Article  Google Scholar 

  20. Garg BK, Burman U, Kathju S (2006) Influence of thiourea on photosynthesis, nitrogen metabolism and yield of cluster bean [Cyamopsis tetragonoloba (L.) Taub.] under rainfed conditions of Indian arid zone. Plant Growth Regul 48:237–245

    CAS  Google Scholar 

  21. Gul B, Weber DJ (1998) Effect of dormancy relieving compounds on the seed germination of non-dormant Allenrolfea occidentalis under salinity stress. Ann Bot 82:555–560

    Article  CAS  Google Scholar 

  22. Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151

    Article  Google Scholar 

  23. Hernández-Nistal J, Aldasoro J, Rodriguez D, Matilla A, Nicolás G (1983) Effect of thiourea on the ionic content and dark fixation of CO2 in embryonic axes of Cicer arietinum seeds. Physiol Plant 57:273–278

    Article  Google Scholar 

  24. Hussain I, Ahmad R, Farooq M, Wahid A (2013) Seed Priming improves the performance of poor quality wheat seed. Int J Agric Biol 15:1343–1348

    Google Scholar 

  25. Hussain I, Wahid A, Rasheed R, Akram HM (2014) Seasonal differences in growth, photosynthetic pigments and gas exchange properties in two greenhouse grown maize (Zea mays L.) cultivars. Acta Bot Croat 73:333–345

    Google Scholar 

  26. Jamali MK, Kazi TG, Arain MB, Afridi HI, Jalbani N, Memon AR (2007) Heavy metal contents of vegetables grown in soil, irrigated with mixtures of wastewater and sewage sludge in Pakistan using ultrasonic-assisted pseudo-digestion. J Agron Crop Sci 193:218–228

    Article  CAS  Google Scholar 

  27. Liu Z, Wen W, He X (2011) Cadmium induced changes in growth and antioxidative mechanisms of a medicinal plant (Lonicera japonica Thunb). J Med Plant Res 5:1411–1417

    CAS  Google Scholar 

  28. Pandey M, Srivastava AK, D’Souza SF, Suprasanna P (2013) Thiourea, a ROS scavenger, regulates source-to-sink relationship for enhanced crop yield and oil content in Brassica juncea (L.). PLoS ONE 8:e73921

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Perveen A, Wahid A, Javed F (2011) Varietal differences in spring and autumn sown maize (Zea mays) for tolerance against cadmium toxicity. Int J Agric Biol 13:909–915

    CAS  Google Scholar 

  30. Perveen A, Wahid A, Hussain I, Rasheed R, Mahmood S (2013) Growth bioregulatory role of root-applied thiourea: changes in growth, toxicity symptoms and photosynthetic pigments of maize. Pak J Agric Sci 50:455–462

    Google Scholar 

  31. Riaz S, Iqbal M, Hussain I, Rasheed R, Ashraf MA, Mahmood S, Younas M, Iqbal MZ (2014) Chronic cadmium induced oxidative stress not the DNA fragmentation modulates growth in spring wheat (Triticum aestivum). Int J Agric Biol 16:789–794

    CAS  Google Scholar 

  32. Sivritepes HO, Sivritepes N, Eris A, Turhan E (2005) The effects of NaCl pre-treatment on salt tolerance of melons grown under long term salinity. Sci Hort 106:568–581

    Article  Google Scholar 

  33. Srivastava AK, Srivastava S, Suprasanna P, D’Souza SF (2011) Thiourea orchestrates regulation of redox state and antioxidant responses to reduce the NaCl-induced oxidative damage in Indian mustard (Brassica juncea (L.) Czern.). Plant Physiol Biochem 49:676–686

    Article  CAS  PubMed  Google Scholar 

  34. Srivastava AK, Srivastava S, Mishra S, Suprasanna P, D’Souza SF (2014) Identification of redox-regulated components of arsenate (AsV) tolerance through thiourea supplementation in rice. Metallomics 6:1718–1730

    Article  CAS  PubMed  Google Scholar 

  35. Steel RGD, Torrie JH, Dickey DA (1996) Principles and procedures of statistics: a biometrical approach, 3rd edn. McGraw Hill Co., New York

    Google Scholar 

  36. Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates Inc. Publishers, Sunderland

    Google Scholar 

  37. Wahid A, Ghani A (2008) Varietal differences in mungbean (Vigna radiata) for growth, yield, toxicity symptoms and cadmium accumulation. Ann Appl Biol 152:59–69

    Article  CAS  Google Scholar 

  38. Wahid A, Ghani A, Javed F (2008a) Effect of cadmium on photosynthesis, nutrition and growth of mungbean. Agron Sustain Dev 28:273–280

    Article  CAS  Google Scholar 

  39. Wahid A, Noreen A, Basra SMA, Gelani S, Farooq M (2008b) Priming-induced metabolic changes in sunflower (Helianthus annuus) achenes improve germination and seedling growth. Bot Stud 49:343–350

    CAS  Google Scholar 

  40. Wahid A, Arshad M, Farooq M (2009) Cadmium phytotoxicity: responses, mechanisms and mitigation strategies. In: Lichtfouse E (ed) Advances in sustainable—book series, vol 1. Springer, NY, pp 371–403

    Google Scholar 

  41. Winter T, Lena B, Jurgen Z, Michael R (2012) Heavy metal stress can prime for herbivore-induced plant volatile emission. Plant Cell Environ 10:1365–3040

    Google Scholar 

  42. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  43. Yoshida S, Forno DA, Cock J, Gomez KA (1976) Laboratory manual for physiological studies of rice. IRRI, Los Banos

    Google Scholar 

  44. 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 

  45. Zhang L, Zhang H, Guo W, Tian Y, Chen Z, Wei X (2012) Photosynthetic responses of energy plant maize under cadmium contamination stress. Adv Mat Res 356–360:283–286

    Google Scholar 

Download references

Acknowledgments

This work is a part of Ph.D. dissertation of first author (AP), who acknowledges the help of field and laboratory staff during greenhouse handling of plants and analytical work.

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Correspondence to Abdul Wahid.

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Perveen, A., Wahid, A., Mahmood, S. et al. Possible mechanism of medium-supplemented thiourea in improving growth, gas exchange, and photosynthetic pigments in cadmium-stressed maize (Zea mays). Braz. J. Bot 38, 71–79 (2015). https://doi.org/10.1007/s40415-014-0124-8

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Keywords

  • Cadmium
  • Carotenoids
  • Chlorophyll-b
  • Maize
  • Organic ligand
  • P n
  • Thiol group