Advertisement

Alterations in photosynthetic pigments, protein, and carbohydrate metabolism in a wild plant Coronopus didymus L. (Brassicaceae) under lead stress

  • Gagan Preet Singh Sidhu
  • Harminder Pal Singh
  • Daizy R. Batish
  • Ravinder Kumar Kohli
Original Article

Abstract

Coronopus didymus has been emerged as a promising wild, unpalatable plant species to alleviate lead (Pb) from the contaminated soils. This work investigated the hypothesis regarding various metabolic adaptations of C. didymus under lead (Pb) stress. In pot experiments, we assessed the effect of Pb at varied concentrations (500–2900 mg kg−1) on growth, photosynthetic pigments, alteration of macromolecular (protein and carbohydrate) content, and activities of enzymes like protease, α-and β-amylase, peroxidase (POX), and polyphenol oxidase (PPO) in C. didymus for 6 weeks. Results revealed that Pb exposure enhanced the growth, protein, and carbohydrate level, but decreased the leaf pigment concentration and activities of hydrolytic enzymes. The activities of POX and PPO in roots increased progressively by ~337 and 675%, respectively, over the control, at 2900 mg kg−1 Pb treatment. Likewise, contemporaneous findings were noticed in shoots of C. didymus, strongly indicating its inherent potential to cope Pb-induced stress. Furthermore, the altered plant biochemical status and upregulated metabolic activities of POX and PPO indulged in polyphenol peroxidation elucidate their role in allocating protection and conferring resistance against Pb instigated stress. The current work suggests that stress induced by Pb in C. didymus stimulated the POX and PPO activities which impart a decisive role in detoxification of peaked Pb levels, perhaps, by forming physical barrier or lignifications.

Keywords

Biochemical status Coronopus didymus Detoxification Pb stress Peroxidase Polyphenol oxidase 

Abbreviations

CAT

Catalase

DMSO

Dimethyl sulphoxide

DNSA

Dinitrosalicylic acid

H2O2

Hydrogen peroxide

HSP

Heat shock proteins

POX

Peroxidase

PPO

Polyphenol oxidase

ROS

Reactive oxygen species

Notes

Acknowledgements

Gagan Preet Singh Sidhu is thankful to University Grants Commission (UGC), New Delhi, India, for Maulana Azad National Fellowship for Minority Students (MANF-SIK-PUN-4078) for undertaking this research.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Agency for Toxic Substances and Disease Registry (ATSDR) (2015) CERCLA priority list of hazardous substances. http://www.atsdr.cdc.gov/spl/index.html
  2. Ahmed CB, Rouina BB, Sensoy S, Boukhriss M, Abdullah FB (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58:4216–4222CrossRefPubMedGoogle Scholar
  3. Ali B, Song WJ, Hu WZ, Luo XN, Gill RA, Wang J, Zhou WJ (2014a) Hydrogen sulfide alleviates lead-induced photosynthetic and ultrastructural changes in oilseed rape. Ecotox Environ Safe 102:25–33CrossRefGoogle Scholar
  4. Ali B, Mwamba TM, Gill RA, Yang C, Ali S, Daud MK, Wu Y, Zhou W (2014b) Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 74:261–273CrossRefGoogle Scholar
  5. Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M, Zhou W (2014c) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crops Prod 52:617–626CrossRefGoogle Scholar
  6. Al-Whaibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ Sci 23:139–150CrossRefGoogle Scholar
  7. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefPubMedPubMedCentralGoogle Scholar
  8. Batish DR, Singh HP, Setia N, Kaur S, Kohli RK (2006) Effect of 2-benzoxazolinone (BOA) on seedling growth and associated biochemical changes in mung bean (Phaseolus aureus). Z Naturforsch 61c:709–714Google Scholar
  9. Burzyński M, Kłobus G (2004) Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. Photosynthetica 42:505–510CrossRefGoogle Scholar
  10. Domash VI, Sharpio TP, Zabreiko SA, Sosnovskaya TF (2008) Proteolytic enzymes and trypsin inhibitors of higher plants under stress conditions. Russ J Bioorg Chem 34:318–322CrossRefGoogle Scholar
  11. Gao Y, Miao CY, Mao L, Zhou P, Jin ZG, Shi WJ (2010) Improvement of phytoextraction and antioxidative defense of Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid synergy. J Hazard Mater 181:771–777CrossRefPubMedGoogle Scholar
  12. Hiscox JD, Israelstam GF (1979) A method for extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334CrossRefGoogle Scholar
  13. Hong FS (2003) Study of the effect of Pb2+ on alpha-amylase activity by spectroscopy. Guang Pu Xue Yu Guang Pu Fen Xi 23:583–586PubMedGoogle Scholar
  14. Hu R, Sunc K, Suc X, Pana Y, Zhanga Y, Wanga X (2012) Physiological responses and tolerance mechanisms to Pb in two xerophils: Salsola passerina Bunge and Chenopodium album L. J Hazard Mater 205–206:131–138CrossRefPubMedGoogle Scholar
  15. Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154:914–926CrossRefPubMedGoogle Scholar
  16. Kováčik J, Klejdus B, Hedbavny J, Štork F, Bačkor M (2009) Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant Soil 320:231–242CrossRefGoogle Scholar
  17. Kuriakose SV, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54:143–156CrossRefGoogle Scholar
  18. Lamhamdi M, Bakrim A, Aarab A, Lafont R, Sayah F (2011) Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. C R Biol 334:118–126CrossRefPubMedGoogle Scholar
  19. Lavid N, Schwartz A, Lewinsohn E, Tel-Or E (2001) Phenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nymphaeaceae). Planta 214:189–196CrossRefPubMedGoogle Scholar
  20. Lichtenthaler HK, Wellburn WR (1983) Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592CrossRefGoogle Scholar
  21. Liu D, Li TQ, Jin XF, Yang XE, Islam E, Mahmood Q (2008) Lead induced changes in the growth and antioxidant metabolism of the lead accumulating and non-accumulating ecotypes of Sedum alfredii. J Integr Plant Biol 50:129–140CrossRefPubMedGoogle Scholar
  22. Loewus FA (1952) Improvement in the anthrone method for determination of carbohydrates. Ann Chem 24:219CrossRefGoogle Scholar
  23. Lowry OH, Rosebrough NJ, Farr AL, Rendall RJ (1951) Protein estimation with folin–phenol reagent. J Biol Chem 193:265–278PubMedGoogle Scholar
  24. Lummerzheim M, Roby D, Timmerman B (1995) Comparative microscopic and enzymatic characterization of the leaf necrosis induced in Arabidopsis thaliana by lead nitrate and by Xanthomonas campestris pv. campestris after foliar spray. Plant Cell Environ 18:499–509CrossRefGoogle Scholar
  25. Mahajan P, Singh HP, Batish DR, Kohli RK (2013) Cr (VI) imposed toxicity in maize seedlings assessed in terms of disruption in carbohydrate metabolism. Biol Trace Elem Res 156:316–322CrossRefPubMedGoogle Scholar
  26. Majdi H, Andersson P (2005) Fine root production and turnover in a Norway spruce stand in northern Sweden: effects of nitrogen and water manipulation. Ecosystems 8:191–199CrossRefGoogle Scholar
  27. Malar S, Manikandan R, Favas PJ, Sahi SV, Venkatachalam P (2014a) Effect of lead on phytotoxicity, growth, biochemical alterations and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation. Ecotox Environ Safe 108:249–257CrossRefGoogle Scholar
  28. Malar S, Vikram SS, Favas PJ, Perumal V (2014b) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 55:1–11CrossRefGoogle Scholar
  29. Meeinkuirt W, Kruatrachue M, Tanhan P, Chaiyarat R, Pokethitiyook P (2013) Phytostabilization potential of Pb mine tailings by two grass species, Thysanolaena maxima and Vetiveria zizanioides. Water Air Soil Pollut 224:1–12CrossRefGoogle Scholar
  30. Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039CrossRefPubMedGoogle Scholar
  31. Mohan BS, Hosetti BB (1997) Potential phytotoxicity of lead and cadmium to Lemna minor grown in sewage stabilization ponds. Environ Pollut 98:233–238CrossRefGoogle Scholar
  32. Nagajyoti PC, Dinakar N, Suresh S, Udaykiran Y, Suresh C, Prasad TNVKV, Damodharam T (2009) Biomass industrial effluent effect on carbohydrates, amino acids, nitrite and nitrite enzyme activities of Arachis hypogaea L. Agric Sci China 8:203–215CrossRefGoogle Scholar
  33. Negi A, Singh HP, Batish DR, Kohli RK (2014) Ni+2-inhibited radicle growth in germinating wheat seeds involves alterations in sugar metabolism. Acta Physiol Plant 36:923–929CrossRefGoogle Scholar
  34. Prassad TK (1996) Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. Plant J 10:1017–1026CrossRefGoogle Scholar
  35. Rani D, Kohli RK (1991) Fresh matter is not an appropriate relation unit for chlorophyll content: experience from experiments on effects of herbicides and allelopathic substances. Photosynthetica 25:655–658Google Scholar
  36. Ruley AT, Sharma NC, Sahi SV (2004) Antioxidant defense in a lead accumulating plant, Sesbania drummondii. Plant Physiol Biochem 42:899–906CrossRefPubMedGoogle Scholar
  37. Saffar A, Bagherieh Najjar MB, Mianabadi M (2009) Activity of antioxidant enzymes in response to cadmium in Arabidopsis thaliana. J Biol Sci 9:44–50CrossRefGoogle Scholar
  38. Samarakoon AB, Rauser WE (1979) Carbohydrate levels and photo assimilate export from leaves of Phaseolus vulgaris exposed to excess cobalt, nickel, and zinc. Plant Physiol 63:1165–1169CrossRefPubMedPubMedCentralGoogle Scholar
  39. Shakoor MB, Ali S, Hameed A, Farid M, Hussain S, Yasmeen T, Najeeb U, Bharwana SA, Abbasi GH (2014) Citric acid improves lead (Pb) phytoextraction in Brassica napus L. by mitigating Pb-induced morphological and biochemical damages. Ecotox Environ Safe 109:38–47CrossRefGoogle Scholar
  40. Sharma P, Dubey RS (2005) Pb toxicity in plants. Braz J Plant Physiol 17:35–52CrossRefGoogle Scholar
  41. Shu X, Yin L, Zhang Q, Wang W (2012) Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res 19:893–902CrossRefGoogle Scholar
  42. Sidhu GPS (2016) Heavy metal toxicity in soils: Sources, remediation technologies and challenges. Adv Plants Agric Res 5:00166Google Scholar
  43. Sidhu GPS, Singh HP, Batish DR, Kohli RK (2016) Effect of lead on oxidative status, antioxidative response and metal accumulation in Coronopus didymus. Plant Physiol Biochem 105:290–296CrossRefPubMedGoogle Scholar
  44. Sidhu GPS, Singh HP, Batish DR, Kohli RK (2017a) Tolerance and hyperaccumulation of cadmium by a wild, unpalatable herb Coronopus didymus (L.) Sm. (Brassicaceae). Ecotox Environ Safe 135:209–215CrossRefGoogle Scholar
  45. Sidhu GPS, Singh HP, Batish DR, Kohli RK (2017b) Appraising the role of environment friendly chelants in alleviating lead by Coronopus didymus from Pb-contaminated soils. Chemosphere 182:129–136CrossRefPubMedGoogle Scholar
  46. Singh HP, Kaur G, Batish DR, Kohli RK (2011) Lead (Pb)-inhibited radicle emergence in Brassica campestris involves alterations in starch-metabolizing enzymes. Biol Trace Elem Res 144:1295–1301CrossRefPubMedGoogle Scholar
  47. Srivastava S, Mishra S, Dwivedi S, Baghel VS, Verma S, Tandon PK, Rai UN, Tripathi RD (2005) Nickel phytoremediation potential of broad bean Vicia faba L. and its biochemical responses. Bull Environ Cotamin Toxicol 74:715–724CrossRefGoogle Scholar
  48. Wang C, Lu J, Zhang S, Wang P, Hou J, Qian J (2011) Effects of Pb stress on nutrient uptake and secondary metabolism in submerged macrophyte Vallisneria natans. Ecotox Environ Safe 74:1297–1303CrossRefGoogle Scholar
  49. Xiong ZT, Zhao F, Li MJ (2006) Lead toxicity in Brassica pekinensis Rupr.: effect on nitrate assimilation and growth. Environ Toxicol 21:147–153CrossRefPubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  • Gagan Preet Singh Sidhu
    • 1
  • Harminder Pal Singh
    • 1
  • Daizy R. Batish
    • 2
  • Ravinder Kumar Kohli
    • 2
    • 3
  1. 1.Department of Environment StudiesPanjab UniversityChandigarhIndia
  2. 2.Department of BotanyPanjab UniversityChandigarhIndia
  3. 3.Central University of PunjabBathindaIndia

Personalised recommendations