Advertisement

Protoplasma

, Volume 254, Issue 2, pp 1031–1043 | Cite as

Changes in rubisco, cysteine-rich proteins and antioxidant system of spinach (Spinacia oleracea L.) due to sulphur deficiency, cadmium stress and their combination

  • Rita Bagheri
  • Javed Ahmad
  • Humayra Bashir
  • Muhammad Iqbal
  • M. Irfan QureshiEmail author
Original Article

Abstract

Sulphur (S) deficiency, cadmium (Cd) toxicity and their combinations are of wide occurrence throughout agricultural lands. We assessed the impact of short-term (2 days) and long-term (4 days) applications of cadmium (40 μg/g soil) on spinach plants grown on sulphur-sufficient (300 μM SO4 2−) and sulphur-deficient (30 μM SO4 2−) soils. Compared with the control (+S and −Cd), oxidative stress was increased by S deficiency (−S and −Cd), cadmium (+S and +Cd) and their combination stress (−S and +Cd) in the order of (S deficiency) < (Cd stress) < (S deficiency and +Cd stress). SDS-PAGE profile of leaf proteins showed a high vulnerability of rubisco large subunit (RbcL) to S deficiency. Rubisco small subunit (RbcS) was particularly sensitive to Cd as well as dual stress (+Cd and −S) but increased with Cd in the presence of S. Cysteine content in low molecular weight proteins/peptide was also affected, showing a significant increase under cadmium treatment. Components of ascorbate-glutathione antioxidant system altered their levels, showing the maximum decline in ascorbate (ASA), dehydroascorbate (DHA), total ascorbate (ASA + DHA, hereafter TA), glutathione (GSH) and total glutathione (GSH + GSSG, hereafter TG) under S deficiency. However, total ascorbate and total glutathione increased, besides a marginal increase in their reduced and oxidized forms, when Cd was applied in the presence of sufficient S. Sulphur supply also helped in increasing the activity of superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione reductase (GR) and catalase (CAT) under Cd stress. However, their activity suffered by S deficiency and by Cd stress during S deficiency. Each stress declined the contents of soluble protein and photosynthetic pigments; the highest decline in contents of protein and pigments occurred under S deficiency and dual stress respectively. The fresh and dry weights, although affected adversely by every stress, declined most under dual stress. It may be concluded that an optimal level of S is required during Cd stress for better response of SOD, APX, GR and CAT activity, as well as synthesis of cysteine. RbcS is as highly sensitive to S deficiency as RbcL is to Cd stress.

Keywords

Spinacia oleracea Sulphur deficiency Cadmium stress SDS-PAGE profile Rubisco Antioxidants 

Notes

Acknowledgments

All authors are grateful to Jamia Millia Islamia (A Central University) for providing lab and other necessary facilities. RB acknowledges the fellowship support to her by ICCR, Govt. of India.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

Supporting information

Supplementary data provided.

Supplementary material

709_2016_1012_MOESM1_ESM.docx (2.2 mb)
ESM 1 (DOCX 2265 kb)

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefPubMedGoogle Scholar
  2. Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–555CrossRefPubMedGoogle Scholar
  3. Anjum NA, Umar S, Ahmad A, Iqbal M (2008) Responses of components of antioxidant system in Mungbean genotypes to cadmium stress. Commun Soil Sci Plant Anal 39:2469–2483CrossRefGoogle Scholar
  4. Anjum NA, Umar S, Iqbal M, Khan NA (2011) Cadmium causes oxidative stress in mung bean by affecting the antioxidant enzyme system and ascorbate-glutathione cycle metabolism. Russ J Plant Physiol 58(1):92–99.CrossRefGoogle Scholar
  5. Anjum NA, Sofo A, Scopam A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I (2015) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22(6):4099–4121CrossRefGoogle Scholar
  6. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefPubMedPubMedCentralGoogle Scholar
  7. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 161:795–802CrossRefPubMedGoogle Scholar
  9. Astolfi S, Zuchi S, Neumann G, Cesco S, di Toppi LS, Pinton R (2012) Response of barley plants to Fe deficiency and Cd contamination as affected by S starvation. J Exp Bot 3:1241–1250CrossRefGoogle Scholar
  10. Azevedo RA, Gratão PL, Monteiro CC, Carvalho RF (2012) What is new in the research on cadmium‐induced stress in plants? Food Eng Security 1:133–140CrossRefGoogle Scholar
  11. Bagheri R, Bashir H, Ahmad J, Baig A, Qureshi MI (2013) Effect of cadmium on leaf proteome of Spinacia oleracea (spinach). Int J Agric Food Sci Technol 4:33–36Google Scholar
  12. Bagheri R, Bashir H, Ahmad J, Baig A, Qureshi MI (2014) Effects of cadmium stress on plants. Environmental sustainability: concepts, principles, evidences and innovations., pp 271–277Google Scholar
  13. Bashir H, Ahmad J, Bagheri R, Nauman M, Qureshi MI (2013a) Limited sulphur resource forces Arabidopsis thaliana to shift towards non- sulphur tolerance under cadmium stress. Environ Exp Bot 94:19–32CrossRefGoogle Scholar
  14. Bashir H, Ahmad J, Bagheri R, Baig A, Qureshi MI (2013b) Thylakoidal pigment-protein complexes: critical requirement of sulphur for proper assemblage and photosynthesis in Arabidopsis thaliana. J Plant Biochem Physiol 1:e110. doi: 10.4172/2329-9029.1000e110 CrossRefGoogle Scholar
  15. Bashir H, Qureshi MI, Ibrahim AM, Iqbal M (2015) Chloroplast and photosystems: impact of cadmium and iron deficiency. Photosynthetica 53(3):321–335CrossRefGoogle Scholar
  16. 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 72:248–254CrossRefPubMedGoogle Scholar
  17. Candiano G, Bruschi M, Musante L, Santucci L et al (2004) Blue silver: a very sensitive colloidal Coomassie G‐250 staining for proteome analysis. Electrophoresis 25:1327–1333CrossRefPubMedGoogle Scholar
  18. Chandler PM, Higgins TJV, Randall PJ, Spencer D (1983) Regulation of legumin levels in developing pea seeds under conditions of sulfur deficiency rates of legumin synthesis and levels of legumin mRNA. Plant Physiol 71:47–54CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chaves MM, Costa JM, Saibo NJM (2011) Recent advances in photosynthesis under drought and salinity. Plant responses to drought and salinity stress. Developments in a post-genomic era 57., p 57Google Scholar
  20. Chmielowska-Bąk J, Lefèvre I, Lutts S, Kulik A, Deckert J (2014) Effect of cobalt chloride on soybean seedlings subjected to cadmium stress. Acta Bot Pol 83:201–207CrossRefGoogle Scholar
  21. Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4):e23681CrossRefPubMedGoogle Scholar
  22. 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 32:93–101CrossRefGoogle Scholar
  23. Forieri I, Wirtz M, Hell R (2013) Toward new perspectives on the interaction of iron and sulfur metabolism in plants. Front Plant Sci 4:357CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627–633CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gallego SM, Pena LB, Barcia RA, Azpilicueta CE et al (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46CrossRefGoogle Scholar
  26. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 12:909–930CrossRefGoogle Scholar
  27. Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants: probing the role of sulfur. Plant Signal Behav 6:215–222CrossRefPubMedGoogle Scholar
  28. Gill SS, Khan NA, Tuteja N (2011) Differential cadmium stress tolerance in five Indian mustard (Brassica juncea L.) cultivars: an evaluation of the role of antioxidant machinery. Plant Signal Behav 6:293–300CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hatata MM, Abdel-Aal EA (2008) Oxidative stress and antioxidant defense mechanisms in response to cadmium treatments. Am-Eurasian J Agric Environ Sci 4:655–669Google Scholar
  30. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  31. Hernandez L, Probst A, Probst JL, Ulrich E (2003) Heavy metal distribution in some French forest soils: evidence for atmospheric contamination. Sci Total Environ 312:195–219CrossRefPubMedGoogle Scholar
  32. Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334CrossRefGoogle Scholar
  33. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:461–465, University of California, Berkeley, CAGoogle Scholar
  34. Kato M, Shimizu S (1985) Chlorophyll metabolism in higher plants VI. Involvement of peroxidase in chlorophyll degradation. Plant Cell Physiol 26:1291–1301CrossRefGoogle Scholar
  35. Khan NA, Samiullah Singh S, Nazar R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193:435–444CrossRefGoogle Scholar
  36. Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium‐exposed poplar plants. Proteomics 12:2514–2530CrossRefGoogle Scholar
  37. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  38. Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903CrossRefPubMedPubMedCentralGoogle Scholar
  39. Marschner H (2012) Marschner’s mineral nutrition of higher plants (3rd Edition). P. Marschner (Ed.) Academic Press, Elsevier Ltd.Google Scholar
  40. Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610CrossRefPubMedGoogle Scholar
  41. Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pilon M, Abdel-Ghany SE, Van Hoewyk D, Ye H, Pilon-Smits EA (2006) Biogenesis of iron-sulfur cluster proteins in plastids. Genet Eng 27:101–117Google Scholar
  43. Pivato M, Fabrega-Prats M, Masi A (2014) Low-molecular-weight thiols in plants: functional and analytical implications. Arch Biochem Biophys 560:83–99CrossRefPubMedGoogle Scholar
  44. Qadir S, Qureshi MI, Javed S, Abdin MZ (2004) Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Sci 167:1171–1181CrossRefGoogle Scholar
  45. Qureshi MI, Qadir S, Zolla L (2007) Proteomics-based dissection of stress-responsive pathways in plants. J Plant Physiol 164:1239–1260CrossRefPubMedGoogle Scholar
  46. Qureshi MI, D’Amici GM, Fagioni M, Rinalducci S, Zolla L (2010) Iron stabilizes thylakoid protein–pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS. J Plant Physiol 167:761–770CrossRefPubMedGoogle Scholar
  47. Radić S, Cvjetko P, Glavas K, Roje V, Pevalek‐Kozlina B, Pavlica M (2009) Oxidative stress and DNA damage in broad bean (Vicia faba L.) seedlings induced by thallium. Environ Toxicol Chem 28:189–196CrossRefPubMedGoogle Scholar
  48. Rodríguez-Celma J, Rellán-Álvarez R, Abadía A, Abadía J, López-Millán A-F (2010) Changes induced by two levels of cadmium toxicity in the 2-DE protein profile of tomato roots. J Prot 73:1694–1706CrossRefGoogle Scholar
  49. Saibo NJ, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623CrossRefPubMedGoogle Scholar
  50. Sen A, Alikamanoglu S (2013) Antioxidant enzyme activities, malondialdehyde, and total phenolic content of PEG-induced hyperhydric leaves in sugar beet tissue culture. In Vitro Cell Dev Bio—Plant 49:396–404CrossRefGoogle Scholar
  51. Sorahan T, Lancashire RJ (1997) Lung cancer mortality in a cohort of workers employed at a cadmium recovery plant in the United States: an analysis with detailed job histories. Occup Environ Med 54:194–201CrossRefPubMedPubMedCentralGoogle Scholar
  52. Touiserkani T, Haddad R (2012) Cadmium-induced stress and antioxidative responses in different Brassica napus cultivars. J Agric Sci Technol 14:929–937Google Scholar
  53. Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55(35):12Google Scholar
  54. Xu J, Duan X, Yang J, Beeching JR, Zhang P (2013) Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiol 3:1517–1528CrossRefGoogle Scholar
  55. Zhu XG, Song Q, Ort DR (2012) Elements of a dynamic systems model of canopy photosynthesis. Curr Opin Plant Biol 15:237–244CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Proteomics and Bioinformatics Lab, Department of BiotechnologyJamia Millia IslamiaNew DelhiIndia
  2. 2.Department of BotanyJamia HamdardNew DelhiIndia

Personalised recommendations