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Antioxidant enzyme activities in male and female plants of Hippophae salicifolia D. Don in different pheno-phases

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Abstract

Changing seasons or environmental condition of a region and various life phases of the yearly cycle of plants can cause the production of reactive oxygen species in plant tissues. The antioxidative system plays a vital role in acclimations in such stress-full conditions, either enzymes or non-enzymatic molecules. Hippophae salicifolia D. Don. is a dioecious and deciduous tree species growing in temperate to the subalpine region of Indian Himalayas in Lahul Spiti (Himachal Pradesh), Uttarakhand, Sikkim, and Arunachal Pradesh. As a dioecious species, variation in male and female was observed in many aspects in both sexual-morph in a range of studies. A hypothesis was made in this study, that male and female plant of H. salicifolia has a different antioxidant potential for quenching the reactive oxygen species in the various growing season of the year, and the antioxidant enzyme activities of male and female also vary with pheno-phases. For this purpose, 10-year-old male and female plants were selected, and leaves and buds were collected from them according to the growing season. Enzymatic extraction was carried out according to the standardized method and enzyme assays were carried out for superoxide dismutase (SOD) and peroxidase (POD). Results showed the variation in SOD and POD enzyme activities in leaves and buds of male and female plants of H. salicifolia in different pheno-phases. Female leaves showed highest enzymatic antioxidant activities in the fruit maturation period (September) and lowest during leaf senescence period (November), whereas male leaves showed highest SOD activity in September but highest POD activity in July. Buds showed higher SOD activity, but lower POD activity than the leaves and differences in activity was not significant in dormant buds at gender basis, active buds showed lower SOD activity but higher POD activity in both male and female.

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Abbreviations

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

POD:

Peroxidase

EDTA:

Ethylene diamine tetraacetic acid

NBT:

Nitro-blue tetrazolium

References

  • Ahmed D, Arshad MA, Ikram M, Asghar MN (2010) Antioxidant and free radical scavenging potential of Otostegia limbata. Asian J Chem 22(6):4524–4532

    CAS  Google Scholar 

  • Aloni R, Baum SF, Peterson CA (1990) The role of cytokinin in sieve tube regeneration and callose production in wounded coleus internodes. Plant Physiol 93:982–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Banuelos MLG, Moreno LV, Winzerling J, Orozco JA, Gardea AA (2008) Winter metabolism in deciduous trees: mechanisms, genes and associated proteins. Rev Fitotecnia Mex 31(4):295–308

    Google Scholar 

  • Bartolini S, Zanol GC, Viti R (2006) Changes in antioxidant compounds in flower buds of two apricot cultivars during winter season. Acta Hortic 701:69–74

    CAS  Google Scholar 

  • Chance B, Maehly AC (1955) Methods Enzymol 2:773–775

    Google Scholar 

  • Chen Y, Zhang M, Chen T, Zhang Y, An L (2006) The relationship between seasonal changes in anti-oxidative system and freezing tolerance in the leaves of evergreen woody plants of Sabina. South Afr J Bot 72(2):272–279

    Google Scholar 

  • Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxide Redox Signal 21:1305–1326

    CAS  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815

    Google Scholar 

  • Dawson TE, Ward JK, Ehleringer JR (2004) Temporal scaling of physiological responses from gas exchange to tree rings: a gender-specific study of Acer negundo (Boxelder) growing under different conditions. Funct Ecol 18:212–222

    Google Scholar 

  • Derbyshire P, Findlay K, McCann MC, Roberts K (2007) Cell elongation in Arabidopsis Hypocotyls involves dynamic changes in cell wall thickness. J Exp Bot 58:2079–2089

    CAS  PubMed  Google Scholar 

  • Dolkar P, Dolkar D, Angmo S, Kant A, Kumar B, Stobdan T (2017a) Sexual differences and seasonal variations in total phenolics and antioxidant properties in Hippophae rhamnoides leaves. J Berry Res 7:61–69

    CAS  Google Scholar 

  • Dolkar P, Dolkar D, Kant A, Chaurasia OP, Stobdan T (2017b) Gender-specific seasonal pattern and altitudinal variation in freeze tolerance response of Seabuckthorn (Hippophae rhamnoides L.). J Berry Res 7:291–297

    CAS  Google Scholar 

  • Dudley LS (2006) Ecological correlates of secondary dimorphism in Salix glauca (Salicaceae). Am J Bot 93:1775–1783

    PubMed  Google Scholar 

  • Esfandiari E, Shekari F, Shekari F, Esfandiari M (2007) The effect of salt stress on antioxidant enzymes' activity and lipid peroxidation on the wheat seedling. Not Bot Hortic Agrobot Cluj 35:48–56

    CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    CAS  PubMed  Google Scholar 

  • Goud PB, Kachole MS (2012) Antioxidant enzyme changes in neem, pigeonpea and mulberry leaves in two stages of maturity. Plant Signal Behav 7(10):1258–1262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goyal AK, Basistha B, Sen A, Midhha SK (2011) Antioxidant profiling of Hippophae salicifolia growing in sacred forests of Sikkim, India. Funct Plant Biol 38(9):697–701

    CAS  Google Scholar 

  • Gupta SM, Ahmed Z (2010) Sea buckthorn (Hippophae salicifolia L.) plant: as source donor of cold tolerant genes for improving high altitude agriculture during cold stress. Res Environ Life Sci 3(3):105–112

    Google Scholar 

  • Gupta SM, Gupta AK, Ahmed Z, Kumar A (2011) Antibacterial and antifungal activity in leaf, seed extract and seed oil of Seabuckthorn (Hippophae salicifolia D. Don) plant. J Plant Pathol Microbiol 2:1–4

    Google Scholar 

  • Gupta SM, Grover A, Pandey P, Ahmed Z (2012) Female plants of Hippophae salicifolia D. Don are more responsive to cold stress than male plants. Physiol Mol Biol Plants 18(4):377–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gurmet P (2009) Seabuckthorn in SOWA-RIGPA (Tibetan Medicine). In: Dwivedi SK, Parimelazhagan T, Singh SB, Ahmed Z (eds) Seabuckthorn: Hippophae spp., The Golden Bush. Satish Serial Publishing House, Delhi, pp 105–112

    Google Scholar 

  • Hakiman M, Maziah M (2009) Non enzymatic and enzymatic antioxidant activities in aqueous extract of different Ficus deltoidea accessions. J Med Plant Res 3(3):120–131

    Google Scholar 

  • Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1997) Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. J Expt Bot 48:1005–1113

    Google Scholar 

  • Hussain S, Niu Q, Yang F, Hussain N, Teng Y (2015) The possible role of chilling in floral and vegetative bud dormancy release in Pyrus pyrifolia. Biol Plant 59:726–734

    CAS  Google Scholar 

  • Ivakov A, Persson S (2013) Plant cell shape: modulators and measurements. Front Plant Sci 4:439

    PubMed  PubMed Central  Google Scholar 

  • Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214(5):751–758

    CAS  PubMed  Google Scholar 

  • Kang HO, Saltveit ME (2001) Activity of enzymatic antioxidant defense systems in chilled and heat shocked cucumber seedling radicles. Physiol Plant 113:548–552

    CAS  Google Scholar 

  • Keshavkant S, Naithani SC (2001) Chilling-induced oxidative stress in young sal (Shorea robusta) seedlings. Acta Physiol Plant 23:457–466

    CAS  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt and temperature stress induced metabolic rearrangement and regulatory networks. J Exp Bot 63:1593–1608

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar J, Heikurujam M, Agarwal V (2016) Characterization of male and female jojoba plants employing antioxidants, lipid peroxidation and physiological studies. Chem Soc 93(7):911–920

    CAS  Google Scholar 

  • Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159(1):75–85

    CAS  PubMed  Google Scholar 

  • Li Y, Zhao H, Duan B, Korpelainen H, Li C (2011) Adaptability to elevated temperature and nitrogen addition is greater in a high-elevation population than in a low-elevation population of Hippophae rhamnoides. Trees 25(6):1073–1082

    CAS  Google Scholar 

  • Liu N, Lin ZF (2014) Reactive oxygen species and alternative respiration in the developing flowers of two subtropical woody plants. J Plant Growth Regul 32:83–91

    Google Scholar 

  • Lloyd DG, Webb CJ (1977) Secondary sex characters in seed plants. Bot Rev 43:177–216

    Google Scholar 

  • Moudgil AD, Mittra S, Sen D, Agnihotri RK, Sharma D (2015) Biochemical and leucocytic response study of herbal immunomodulators against levamisole in Toxocara canis infected mice. Indian J Anim Res 49(3):336–342

    Google Scholar 

  • Pagter M, Arora R (2013) Winter survival and deacclimation of perennials under warming climate: physiological perspectives. Physiol Plant 147:75–87

    CAS  PubMed  Google Scholar 

  • Pandey VP, Awasthi M, Singh S, Tiwari S, Dwivedi UN (2017) A comprehensive review on function and application of plant peroxidases. Biochem Anal Biochem 6(1):1–16

    Google Scholar 

  • Payton P, Webb R, Kornyeyev D, Allen R, Holaday AS (2001) Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity. J Exp Bot 52:2345–2354

    CAS  PubMed  Google Scholar 

  • Polle A, Rennenberg H (1993) Significance of antioxidant in plant adaptation to environmental stress. In: Mansfield T, Fowden L, Stoddard F (eds) Plant adaptation to environmental stress. Chapman and Hall, London, pp 263–273

    Google Scholar 

  • Prasad VV, Iyengar ERR (1985) Phenology and biochemical changes in male and female shrubs of Jojoba [Simmondsia chinensis (Link) Schneider] during different seasons. Proc Indian Acad Sci Sect A Part 3 Math Sci 95(3):203–211

    CAS  Google Scholar 

  • Procházková D, Wilhelmová N (2007) Leaf senescence and activities of the antioxidant enzymes. Biologia Plant 51(3):401–406

    Google Scholar 

  • Ranjith AK, Sarin Kumar VV, Venugopalan C, Arumughan RC, Sawhney RC, Singh V (2006) Fatty acids, tocols, and carotenoids in pulp oil of three sea buckthorn species (Hippophae rhamnoides, H. salicifolia, and H. tibetana). JAOCS 83:359–364

    CAS  Google Scholar 

  • Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Ame J Bot 82:596–606

    Google Scholar 

  • Retuerto R, Lema BF, Roiloa SR, Obeso JR (2000) Gender, light and water effects in carbon isotope discrimination and growth rates in the dioecious tree Ilex aquifolium. Funct Ecol 14:529–537

    Google Scholar 

  • Robakowski P, Pers-Kamczyc E, Ratajczak E, Thomas PA, Ye ZP, Rabska M, Iszkuło G (2018) Photochemistry and antioxidative capacity of female and male Taxus baccata L. acclimated to different nutritional environments. Front Plant Sci 9:742

    PubMed  PubMed Central  Google Scholar 

  • Rongsen A (1992) Sea buckthorn a multi-purpose plant species for fragile mountains. ICIMOD Occasional Paper No. 20, Khathmandou, pp- 62

  • Rowland LJ, Arora R (1997) Proteins related to endodormancy (rest) in woody perennials. Plant Sci 126:119–144

    CAS  Google Scholar 

  • Saikia M, Handique PJ (2013) Antioxidant and antibacterial activity of leaf and bark extracts of Seabuckthorn (Hippophae salicifolia D Don) of North East India. Int J Lif Sci Biotech Pharm Res 2(1):81–91

    Google Scholar 

  • Sairam RK, Singh DV, Srivastava GC (2003) Changes in activities of antioxidant enzymes in sunflower leas of different ages. Biol Plant 47:61–66

    CAS  Google Scholar 

  • Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570

    PubMed  PubMed Central  Google Scholar 

  • Scebba F, Sebastiani L, Vitagliano C (2001) Activities of antioxidant enzymes during senescence of Prunus armeniaca leaves. Biol Plant 44:41–46

    CAS  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    CAS  PubMed  Google Scholar 

  • Sengupta AS, Webb RP, Holaday AS, Allen RD (1993) Induction of Ascorbate Peroxidase in Superoxide Dismutase-Overexpressing Plants. Plant physiol 103(4):1067–1073

    CAS  Google Scholar 

  • Sharma N, Patl RD, Thakur AK, Gupta VK (2014) The wound healing efficacy of leaf extract of Hippophae salicifolia. Int J Adv Sci Tech Res 4(1):250–261

    Google Scholar 

  • Shi S, Wei X, Chen G, Xu Y (2012) Changes in photosynthetic characteristics and antioxidative protection in male and female ginkgo during natural senescence. JASHS 137(5):349–360

    CAS  Google Scholar 

  • Shu YZ (1998) Recent natural products based drug development: a pharmaceutical industry perspective. J Nat Prod 61:1053–1071

    CAS  PubMed  Google Scholar 

  • Simancas B, Juvany M, Cotado A, Munne- Bosch S (2016) Sex related differences in photoinhibition photo-oxidative stress and photoprotection in stinging nettle (Urtica dioica L.) exposed to drought and nutrient deficiency. J Photochem B Biol 156:22–28

    CAS  Google Scholar 

  • Sreelatha S, Padma PR (2009) Antioxidant activity and total phenolic content of Moringa oleifera leaves in two stages of maturity. Plant Foods Hum Nutr 64(4):303–311

    CAS  PubMed  Google Scholar 

  • Stobdan T, Korekar G, Chaurasia OP, Balaji B, Yadav A, Dwivedi SK (2001) Seabuckthorn production for greening and sustainable income generation in cold desert of India. In: Srivastava RB, Selvamurthy W (eds) Innovation in agro animal technologies. Satish Serial Publishing House, New Delhi, pp 71–86

    Google Scholar 

  • Szalay L, Hegedus A, Stfanovits-Banyai E (2005) Polyphenol oxidase enzymes against freezing stress in peach (Prunus persica L. Batsch). Acta Biol Szeged 49:121–122

    Google Scholar 

  • Uprety Y, Asselin H, Boon E, Yadav S, Shrestha K (2010) Indigenous use and bio-efficacy of medicinal plants in the Rasuwa Distric, central Nepal. J Ethnobiol Ethnomed 6(3):1–10

    Google Scholar 

  • Usha T, Middha SK, Goyal AK, Karthik M, Manoj DA, Faizan S, Goyal P, Prashanth HP, Pande V (2014) Molecular docking studies of anti-cancerous candidates in Hippophae rhamnoides and Hippophae salicifolia. J Biomed Res 28:1–10

    Google Scholar 

  • Weiser CJ (1970) Cold resistance and injury in woody plants. Science 169:1269–1278

    CAS  PubMed  Google Scholar 

  • Wu N, Li Z, Wu F, Tang M (2016) Comparative photochemistry activity and antioxidant responses in male and female Populus cathayana cuttings inoculated with arbuscular mycorrhizal fungi under salt stress. Sci Rep 6(37663):1–15

    Google Scholar 

  • Xu X, Yang F, Xiao X, Zhang S, Korpelainen H, Li C (2008a) Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant Cell Environ 31:850–860

    CAS  PubMed  Google Scholar 

  • Xu G, Duan B, Li C (2008b) Different adaptive responses of leaf physiological and biochemical aspects to drought in two contrasting populations of seabuckthorn. Can J For Res 38(3):584–591

    CAS  Google Scholar 

  • Zahra P, Majid R, Amin B (2009) Seasonal changes of peroxidase, polyphenol oxidase enzyme activity and phenol content during and after rest in pistachio (Pistacia vera L.) flower buds. World App Sci J 6(9):1193–1199

    CAS  Google Scholar 

  • Zhang S, Lu S, Xu X, Korpelainen H, Li C (2010) Changes in antioxidant enzyme activities and isozyme profiles in leaves of male and female Populus cathayana infected with Melampsora larici-populina. Tree Physiol 30:116–128

    PubMed  Google Scholar 

  • Zhao H, Li Y, Duan B, Korpelainen H, Li C (2009) Sex-related adaptive response of Populus cathayana to photoperiod transitions. Plant Cell Environ 32:1401–1411

    CAS  PubMed  Google Scholar 

  • Zhuang WB, Shi T, Gao ZH, Zhang Z, Zhang JY (2013) Differential expression of proteins associated with seasonal bud dormancy at four critical stages in Japanese apricot. Plant Biol 15:233–242

    CAS  PubMed  Google Scholar 

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Acknowledgements

Authors are thankful to Prof. A. R. Nautiyal (Director, HAPPRC) and Prof. P. Prasad (Former Director, HAPPRC) for providing necessary facilities and useful suggestions.

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  1. High Altitude Plant Physiology Research Centre (HAPPRC), HNB Garhwal University (A Central University), Srinagar Garhwal, Uttarakhand, 246174, India

    Vijay Laxmi Trivedi, Mohan Chandra Nautiyal, Jyoti Sati & Dharam Chand Attri

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  1. Vijay Laxmi Trivedi
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  2. Mohan Chandra Nautiyal
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Trivedi, V.L., Nautiyal, M.C., Sati, J. et al. Antioxidant enzyme activities in male and female plants of Hippophae salicifolia D. Don in different pheno-phases. Acta Physiol Plant 42, 64 (2020). https://doi.org/10.1007/s11738-020-03049-5

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