Acta Physiologiae Plantarum

, Volume 35, Issue 8, pp 2501–2511 | Cite as

Glutathione regulates enzymatic antioxidant defence with differential thiol content in perennial pepperweed and helps adapting to extreme environment

  • Tarandeep Kaur
  • Hilal A. Bhat
  • Anuj Raina
  • Sushma Koul
  • Dhiraj Vyas
Original Paper
First Online:
Received:
Revised:
Accepted:

Abstract

Perennial pepperweed (Lepidium latifolium Linn.) is a preferred ‘phytofood’ that is available for the longest period of a year in Ladakh. Present study was undertaken to identify the mechanism of redox homeostasis and understand factors responsible for its biochemical superiority during low temperatures. Results reveal that despite the stressful environment at higher altitude, the cellular conditions are more reducing for this plant. The reducing environment is maintained by significant induction of GSH rather than changes in its oxidation state, which changes the redox potential by 12 mV. Lower ratio of NADP+/NADPH and induction of new antioxidative isozymes at Leh (3,505 m) suggest crucial role of redox regulation in adaptation. These new proteins have higher thiol content and could provide an efficient redox sensing mechanism in Lepidium latifolium that respond through GSH/NADPH redox buffers. In vitro feeding experiment suggested that GSH plays an important role in induction of antioxidant enzymes, which may not be the direct consequence of H2O2 accumulation. It needs to be further investigated whether its responsive redox metabolism has some role in its invasive growth in riparian plains of America.

Keywords

Antioxidant system Glutathione Lepidium latifolium Phytofood Redox potential 

Abbreviations

ASC/DHA

Reduced and oxidized form of ascorbate

DCPIP

2,6-dichlorophenol-indophenol

DPPH

1,1-diphenyl-2-picrylhydrazyl

GSH/GSSG

Reduced and oxidized form of glutathione

MDA

Malondialdehyde

NAD+/NADH

Reduced and oxidized form of nicotinamide adenine dinucleotide

NADP+/NADPH

Reduced and oxidized form of nicotinamide adenine dinucleotide phosphate

ROS

Reactive oxygen species

TBA

2-thiobarbituric acid

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Notes

Acknowledgments

Authors would like to thank anonymous reviewers for suggesting necessary changes in improving the quality of manuscript. Authors thank the Director, IIIM, Jammu for providing necessary facilities to carry out the work. Authors are grateful to the Council of Scientific and Industrial Research (CSIR), Government of India, for financial support under CSIR- networking project (BSC-0109) on ‘Plant Diversity: Studying adaptation biology and understanding/exploiting medicinally important plants for useful bioactives (SIMPLE)’.

References

  1. Abrol E, Vyas D, Koul S (2012) Metabolic shift from secondary metabolite production to induction of anti-oxidative enzymes during NaCl stress in Swertia chirata Buch-Ham. Acta Physiol Plant 34:541–546CrossRefGoogle Scholar
  2. Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257PubMedGoogle Scholar
  3. Aravind P, Prasad MN (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116PubMedCrossRefGoogle Scholar
  4. Aslam M, Sinha VB, Singh RK, Anandhan S, Ahmed Z, Pande V (2010) Isolation of cold stress-responsive genes from Lepidium latifolium by suppressive subtraction hybridization. Acta Physiol Plant 32:205–210CrossRefGoogle Scholar
  5. Bartoli CG, Tambussi EA, Diego F, Foyer CH (2009) Control of ascorbic acid synthesis and accumulation and glutathione by the incident light red/far red ratio in Phaseolus vulgaris leaves. FEBS Lett 583:118–122PubMedCrossRefGoogle Scholar
  6. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Ann Rev Plant Bio 56:187–220CrossRefGoogle Scholar
  7. Chen H, Qualls RG, Miller GC (2002) Adaptive responses of Lepidium latifolium to soil flooding: biomass allocation, adventitious rooting, aerenchyma formation and ethylene production. Environ Exp Bot 48:119–128CrossRefGoogle Scholar
  8. Chronopoulou E, Madesis P, Asimakopoulou B, Dimitrios P, Tsaftaris A, Labrou NE (2012) Catalytic and structural diversity of the fluazifop-inducible glutathione transferases from Phaseolus vulgaris. Planta 235(6):1253–1269PubMedCrossRefGoogle Scholar
  9. Colville L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 59:3857–3868PubMedCrossRefGoogle Scholar
  10. Eskling M, Arvidsson PO, Akerlund H-K (1997) The xanthophyll cycle, its regulation and components. Physiol Plant 100:806–816CrossRefGoogle Scholar
  11. Fendt SM, Buescher JM, Rudroff F, Picotti P, Zamboni N, Sauer U (2010) Trade off between enzyme and metabolite efficiency maintains metabolic homeostasis upon perturbations in enzyme capacity. Mol Sys Biol 6:356Google Scholar
  12. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905PubMedCrossRefGoogle Scholar
  13. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18PubMedCrossRefGoogle Scholar
  14. Golding AJ, Finazzi G, Johnson GN (2004) Reduction of the thylakoid electron transport chain by stromal reductants: evidence for activation of cyclic electron transport upon dark adaptation or under drought. Planta 220:356–363PubMedCrossRefGoogle Scholar
  15. Gomez LD, Noctor G, Knight M, Foyer CH (2004) Regulation of calcium signaling and gene expression by glutathione. J Exp Bot 55:1851–1859PubMedCrossRefGoogle Scholar
  16. Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640PubMedGoogle Scholar
  17. Guleria S, Tiku AK, Singh G, Vyas D, Bhardwaj A (2011) Antioxidant activity and protective effect against plasmid DNA strand scission of leaf, bark, and Heartwood Extracts from Acacia catechu. J Food Sci 76:959–964CrossRefGoogle Scholar
  18. Hancock JT, Desikan R, Neill SJ, Cross AR (2004) New equations for redox and nano-signal transduction. J Theor Biol 226(1):65–68PubMedCrossRefGoogle Scholar
  19. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 12:189–198CrossRefGoogle Scholar
  20. Hultén E, Fries M (eds) (1986) Atlas of North European vascular plants, part I-III, maps and commentaries. Koeltz Scientific books, GermanyGoogle Scholar
  21. Jubany-Mari T, Alegre-Batlle L, Jiang K, Feldman LJ (2010) Use of a redox-sensitive GFP (c-roGFP1) for real-time monitoring of cytosol redox status in Arabidopsis thaliana water-stressed plants. FEBS Lett 584:889–897PubMedCrossRefGoogle Scholar
  22. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulate the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640PubMedGoogle Scholar
  23. Kornas A, Kuźniak E, Slesak I, Miszalski Z (2010) The key role of the redox status in regulation of metabolism in photosynthesizing organisms. Acta Biochem Pol 57:143–151Google Scholar
  24. Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78PubMedCrossRefGoogle Scholar
  25. Kranner I, Birtić S, Anderson KM, Pritchard HW (2006) Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Rad Biol Med 40:2155–2165PubMedCrossRefGoogle Scholar
  26. Levitt J (1962) A sulphydryl-disulfide hypothesis of frost injury and resistance in plants. J Theor Biol 3:355–391CrossRefGoogle Scholar
  27. Lowry OH, Rosebrough NJ, Farr AL, Randall RL (1951) Protein measurement with the folin-phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  28. Mehler AH (1951) Studies on reactions of illuminated chloroplasts I mechanisms of the reduction of oxygen and other hill reagents. Arch Biochem Biophys 33:65–77PubMedCrossRefGoogle Scholar
  29. Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, Saindrenan P, Gouia H, Isaakidis-Bourguet E, Renou J-P, Noctor G (2010) Arabidopsis glutathione reductase I plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic and jasmonic acid signalling pathways. Plant Physiol 153(1144):1160Google Scholar
  30. Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566PubMedCrossRefGoogle Scholar
  31. Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582PubMedCrossRefGoogle Scholar
  32. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  33. Navarro E, Alonso J, Rodriguez R, Trujillo J, Boada J (1994) Diuretic action of an aqueous extract of Lepidium latifolium L. J Ethnopharmacol 41:65–69PubMedCrossRefGoogle Scholar
  34. Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425PubMedCrossRefGoogle Scholar
  35. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  36. Noctor G, Mhamdi A, Chaouchi S, Han Y, Neukermans J, Marquez–Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484PubMedCrossRefGoogle Scholar
  37. Pal Murugan M, Raj J, Kumar PG, Gupta S, Singh SB (2010) Phytofoods of Nubra valley, Ladakh-The cold desert. Indian J Trad Knowl 9(2):303–308Google Scholar
  38. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of non indigenous species in the United States. BioScience 50:53–65CrossRefGoogle Scholar
  39. Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal Biochem 363:58–69PubMedCrossRefGoogle Scholar
  40. Rajagopal S, Bukhov NG, Tajmir-Riahi H, Carpentier R (2003) Control of energy dissipation and photochemical activity in photosystem I by NADP-dependent reversible conformational changes. Biochemistry 42:11839–11845PubMedCrossRefGoogle Scholar
  41. Rao MV, Hale BA, Ormrod DP (1995) Amelioration of Ozone-lnduced oxidative damage in wheat plants grown under high carbon dioxide role of antioxidant enzymes. Plant Physiol 109:421–432PubMedGoogle Scholar
  42. Rollins RC (1993) The Cruciferae of Continental North America. Stanford University Press, StanfordGoogle Scholar
  43. Sawhney SK, Singh R (eds) (2009) Introductory practical biochemistry, 2nd edn. Narosa Publishing House, New DelhiGoogle Scholar
  44. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Rad Biol Med 30(11):1191–1212PubMedCrossRefGoogle Scholar
  45. Scheibe R, Backhausen JE, Emmerlich V, Simone H (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489PubMedCrossRefGoogle Scholar
  46. Schultze-Motel W (ed) ((1986)) Lepidium latifolium. Illustrierte Flora von Mittel-europa, 3rd edn. Verlag Paul Parey, BerlinGoogle Scholar
  47. Smirnoff N (2000) Ascorbate biosynthesis and function in photoprotection. Royal Soc 355:1455–1464Google Scholar
  48. Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 50-dithiobis(2nitrobenzoic acid). Anal Biochem 175:408–413PubMedCrossRefGoogle Scholar
  49. Snedecor GW, Cochran WG (1989) Statistical methods, 8th edn. Iowa State University Press, AmesGoogle Scholar
  50. Sonnentag O, Detto M, Runkle BRK, Teh YA, Silver WL, Kelly M, Baldocchi DD (2011) Carbon dioxide exchange of a pepperweed (Lepidium latifolium L.) infestation: How do flowering and mowing affect canopy photosynthesis and autotrophic respiration? J Geophys Res 116:G01021. doi: 10.1029/2010JG001522
  51. Tabassum N, Ahmad F (2011) Role of natural herbs in the treatment of hypertension. Pharmacogn 9:30–34Google Scholar
  52. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522PubMedCrossRefGoogle Scholar
  53. Vyas D, Kumar S (2005a) Purification and partial characterization of a low temperature responsive Mn-SOD from tea (Camellia sinensis(L.) O. Kuntze.). Biochem Biophys Res Comm 329:831–838PubMedCrossRefGoogle Scholar
  54. Vyas D, Kumar S (2005b) Tea (Camellia sinensis (L.) O. Kuntze) clone with lower period of winter dormancy exhibits lesser cellular damage in response to low temperature. Plant Physio Biochem 43:383–388CrossRefGoogle Scholar
  55. Woodbury W, Spencer AK, Stahman MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305PubMedCrossRefGoogle Scholar
  56. Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2007) Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J Exp Bot 58:2661–2671PubMedCrossRefGoogle Scholar
  57. Young JA, Turner CE, James LF (1995) Perennial pepperweed. Rangelands 17:121–123Google Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2013

Authors and Affiliations

  • Tarandeep Kaur
    • 1
    • 2
  • Hilal A. Bhat
    • 2
  • Anuj Raina
    • 2
  • Sushma Koul
    • 2
  • Dhiraj Vyas
    • 1
    • 2
  1. 1.Academy of Scientific and Innovative ResearchIndian Institute of Integrative Medicine (CSIR)JammuIndia
  2. 2.Biodiversity and Applied Botany DivisionIndian Institute of Integrative Medicine (CSIR)JammuIndia

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