Phenological variations of primary biochemicals in male and female plants of Hippophae salicifolia D. Don

  • Vijay Laxmi TrivediEmail author
  • Dharam Chand Attri
  • Jyoti Sati
  • Mohan Chandra Nautiyal
Original Article


Dioecious nature of a plant shows variations in male and female individuals of that species, due to their differential role in sexual reproduction. So it is evident for them to have different metabolite stock in various stages of their life. Hippophae salicifolia D. Don. is a deciduous and dioecious plant species with its immense livelihood, health, and ecological potential. Focussing on the dioecious nature of this plant species male and female individuals of the H. salicifolia were screened for primary metabolite contents viz. Total soluble protein content (TSPC), total free amino acid content (TFAAC) and Carbohydrates (total soluble sugars content-TSSC and total soluble starch content-TSStC) content in different growing seasons of the year. For this leaves and buds of male and female plants were selected during active and dormant seasons respectively. Variations were observed in primary metabolites in all studied months in leaves and buds of the male and female plant. TSSC in female leaves was lower in May and July whereas it was higher in September and November than male leaves. TSPC were found higher in male leaves than female leaves in all observed month except November. TFAAC in male was most elevated in September whereas it was highest in November in female leaves. Carbohydrate, protein and free amino acid contents were found higher in winter buds which help the plants to cope up with the harsh and chilled winter conditions. During dormancy releasing period, buds showed higher TSSC, lower TSStC, higher TSPC, and lower TFAAC.


Hippophae salicifolia Dioecious Total soluble protein content Total free amino acid content Carbohydrates content Seasonal changes 



High Altitude Plant Physiology Research Centre


Bovine serum albumin


Total soluble protein content


Total free amino acid content


Total soluble sugar content


Total soluble starch content



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

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Allan P (2001) Seasonal variations in carbohydrate content of Carica papaya plants. S Afr J Plant Soil 18(2):47–49. Google Scholar
  2. Angelovici R, Fait A, Fernie AR, Galili G (2011) A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytol 189:148–159. Google Scholar
  3. Araujo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, Leaver CJ, Fernie AR (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternativeelectron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22:1549–1563. Google Scholar
  4. Bajpai V, Pandey R, Negi MPS, Bindu KH, Kumar N, Kumar B, Madhusudanan KP (2012) Characteristic differences in metabolite profile in male and female plants of dioecious Piper betle L. J Biosci 37(6):1061–1066. Google Scholar
  5. Banuelos MLG, Moreno LV, Winzerling J, Orozco JA, Gardea AA (2008) Winter metabolism in deciduous trees: mechanisms, genes and associated proteins. Rev Fitotec Mex 31(4):295–308Google Scholar
  6. Barrett SCH, Hough J (2013) Sexual dimorphism in flowering plants. J Exp Bot 64(1):67–82. Google Scholar
  7. Biancucci M, Mattioli R, Forlani G, Funck D, Costantino P, Trovato M (2015) Role of proline and GABA in sexual reproduction of angiosperms. Front Plant Sci 6(680):1–11. Google Scholar
  8. Boldingh H, Smith GS, Klages K (2000) Seasonal concentrations of non-structural carbohydrates of five Actinidia species in fruit, leaf and fine root tissue. Ann Bot 85:469–476. Google Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Ann Biochem 72:248–254. Google Scholar
  10. Case AL, Ashman TL (2005) Sex-specific physiology and its implications for the cost of reproduction. In: Reekie E, Bazzaz F (eds) Reproductive allocation in plants. Elsevier, London, pp 129–157Google Scholar
  11. Cepeda-Cornejo V, Dirzo R (2010) Sex-related differences in reproductive allocation, growth, defense and herbivory in three dioecious neotropical palms. PLoS ONE 235(3):e9824. Google Scholar
  12. Chen L, Wang L, Chen F, Korpelainen H, Li C (2013) The effects of exogenous putrescine on sex-specific responses of Populus cathayana to copper stress. Ecotoxicol Environ Saf 97:94–102. Google Scholar
  13. Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanism. Plant Cell Environ 35:1707–1728. Google Scholar
  14. Correia O, Diaz-Barradas MC (2000) Ecophysiological differences between male and female plants of Pistacia lentiscus L. Plant Ecol 149:131–142. Google Scholar
  15. Dawei S, Wei X, Chen G, Xu Y (2012) Changes in photosynthetic characteristics and antioxidative protection in male and female Ginkgo during natural senescence. J Am Soc Hortic Sci 137(5):349–360. Google Scholar
  16. 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 condition. Fun Ecol 18:212–222. Google Scholar
  17. De Soto L, Olano JM, Rozas V (2016) Secondary growth and carbohydrate storage patterns differ between sexes in Juniperus thurifera. Front Plant Sci 7:723. Google Scholar
  18. Dhyani D, Maikhuri RK, Dhyani S, Rao KS (2010) Endorsing the declining indigenous ethnobotanical knowledge system of Seabuckthorn in Central Himalaya, India. Ethnopharma 127:329–334. Google Scholar
  19. Eichelmann H, Oja V, Rasulov B, Padu E, Bichele I, Pettai H, Niinemets U, Laisk A (2004) Development of leaf photosynthetic parameters in Betula pendula Roth leaves: correlations with photosystem I density. Plant Biol 6:307–318. Google Scholar
  20. El Kayal W, Allen CC, Ju CJ, Adams E, King-Jones S, Zaharia LI et al (2011) Molecular events of apical bud formation in white spruce Picea glauca. Plant Cell Environ 34:480–500. Google Scholar
  21. Ensminger I, Busch F, Hüner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44. Google Scholar
  22. Espirito-Santo MM, Madeira BG, Neves FS, Faria ML, Fagundes M, Fernandes GW (2003) Sexual differences in reproductive phenology and their consequences for the demography of Baccharis dracunculifolia (Asteraceae), a dioecious tropical shrub. Ann Bot 91:13–19. Google Scholar
  23. Gao L, Yang J, Liu RX (2010) Leaf morphological structure and physiological and biochemical characteristics of female and male Hippophae rhamnoides subsp. sinensis under different soil moisture condition. Yingyong Shengtai Xuebao 21(9):2201–2208Google Scholar
  24. Götz KP, Chmielewski FM, Homann T, Huschek G, Matzneller P, Rawel HM (2014) Seasonal changes of physiological parameters in sweet cherry (Prunus avium L.) buds. Sci Hortic 172:183–190. Google Scholar
  25. 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. Google Scholar
  26. Guangxiu L, Wei Z, Tuo C, Xuelin C, Yongshan L, Lizhe A (2009) Gender-specific carbon discrimination and stomatal density in the dioecious tree of Hippophate rhamnoides. S Afr J Bot 75:268–275. Google Scholar
  27. 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
  28. 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. Google Scholar
  29. Gurmeet 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 105–112Google Scholar
  30. Harris MS, Pannell JR (2010) Canopy seed storage is associated with sexual dimorphism in the woody dioecious genus Leucadendron. J Ecol 98:509–515. Google Scholar
  31. Hesse E, Pannell JR (2011) Sexual dimorphism in a dioecious population of the wind-pollinated herb Mercurialis annua: the interactive effects of resource availability and competition. Ann Bot 107:1039–1045. Google Scholar
  32. Hsiao TC (1973) Plant responses to water stress. Annu Rev Physiol 24:519–570. Google Scholar
  33. Juvany M, Munné-Bosch S (2015) Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. J Exp Bot 66:6083–6092. Google Scholar
  34. Kaufmann H, Blanke M (2017) Changes in carbohydrate levels and relative water content (RWC) to distinguish dormancy phases in sweet cherry. J Plant Physiol 218:1–5. Google Scholar
  35. Kirma M, Araujo WL, Fernie AR, Galili G (2012) The multifaceted role of aspartate-family amino acids in plant metabolism. J Exp Bot 63:4995–5001. Google Scholar
  36. Königer M, Harrisa GC, Kibler E (2000) Seasonal changes in the physiology of shade leaves of Acer saccharum. J Plant Physiol 157:627–636. Google Scholar
  37. Li C, Xu G, Zang R, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406. Google Scholar
  38. Li L, Zhang Y, Luo J, Korpelainen H, Li C (2013) Sex-specific responses of Populus yunnanensis exposed to elevated CO2 and salinity. Physiol Planta 147:477–488. Google Scholar
  39. Makhlouf-Gafsi I, Mokni-Ghribi A, Bchir B, AttiaH Blecker C, Besbes S (2015) Physico-chemical properties and amino acid profiles of sap from Tunisian date palm. Sci Agric 73(1):85–90. Google Scholar
  40. Marafon AC, Herter FG, Hawerroth FJ, Bierhals AN (2016) Free amino acids in the xylem sap of pear trees during dormancy. Cienc Rural 46(7):1136–1141. Google Scholar
  41. McCready RM, Guggolz J, SilvieraV, Owen HS (1950) Determination of starch and amylase in vegetables. Analy Chem 22:1156–1158. Google Scholar
  42. Melke A (2015) The physiology of chilling temperature requirements for dormancy release and bud-break in temperate fruit trees grown at mild winter. Trop Clim J Plant Stud 4(2):110–156. Google Scholar
  43. Michailidis M, Karagiannis E, Tanou G, Sarrou E, Adamakis ID, Karamanoli K, Martens S, Molassiotis A (2018) Metabolic mechanisms underpinning vegetative bud dormancy release and shoot development in sweet cherry. Environ Exp Bot 155:1–11. Google Scholar
  44. Midgley JJ (2010) Causes of secondary sexual differences in plants—evidence from extreme leaf dimorphism in Leucadendron (Proteaceae). S Afr J Bot 76:588–592. Google Scholar
  45. Ming R, Wang J, Moore PH, Paterson AH (2007) Sex chromosomes in flowering plants. Am J Bot 94:2141–2150. Google Scholar
  46. Moore S, Stein WH (1954) A modified ninhydrin method for use in the chromatography of amino acids. J Biol Chem 176:367–388Google Scholar
  47. Morgan JM (1984) Osmoregulation and water stress in higher plants. Ann Rev Plant Physiol 35:299–319. Google Scholar
  48. 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
  49. Park JY, Canam T, Kang KY, Unda F, Mansfield SD (2009) Sucrose phosphate synthase expression influences poplar phenology. Tree Physiol 29:937–946. Google Scholar
  50. Pomeroy MK, Siminovitch D (2011) Seasonal cytological changes in secondary phloem parenchyma cells in Robinia pseudoacacia in relation to cold hardiness. Can J Bot 49(5):787–795. Google Scholar
  51. Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753. Google Scholar
  52. Ranjith A, Sarin Kumar K, Venugopalan VV, Arumughan C, 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 83:359–364Google Scholar
  53. 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. Fun Ecol 14:529–537. Google Scholar
  54. Rongsen A (1992) Seabuckthorn a multi-purpose plant species for fragile mountains. ICIMOD occasional paper no. 20, Khathmandou, p 62Google Scholar
  55. 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):81–91Google Scholar
  56. 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):250–261Google Scholar
  57. Signorelli S, Agudelo-Romero P, Meitha K, Foyer CH, Considine MJ (2018) Roles for light, energy, and oxygen in the fate of quiescent axillary buds. Plant Physiol 176:1171–1181. Google Scholar
  58. Singh V, Gupta R (2015) Fatty acid composition of fruit pulp and seed oils of Himalayan Seabuckthorn (Hippophae L). Int J Food Nutri Sci 4(1):91–100Google Scholar
  59. Singh V, Sawhney RC (2005) Progress report (2004–2005) of the project—biochemical characterization and micropropagation of Seabuckthorn (Hippophae L.)- A multipurpose plant of dry temperate Himalayas. CSK Himanchal Pradesh Agricultural University, Hill Agriculture Research and Extension Centre, Bajaura – 175125 (Kullu) H.P. and Defense Institute of Physiology and Allied Sciences, (DRDO), Delhi-110054. Funded by Department of Biotechnology, Ministry of Science and Technology, New DelhiGoogle Scholar
  60. Singh B, Bhatt TK, Singh V (2001) Nutritional evaluation of seabuckthorn leaves as cattle feed—a resource for health and environment in 21 century. In: Proceedings of international workshop on Sea buckthorn, 18–21 Feb, New Delhi, pp 175–181Google Scholar
  61. Thakur SR, Chilikuri P, Pulugurtha B, Yaidikar L (2014) Flavonoid rich fraction of willow leaved Seabuckthorn berries attenuated ischemia reperfusion induced neurobehavioral deficits, excitotoxicity and neuronal damage. J Pharm Sci Innov 3(5):478–481Google Scholar
  62. 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 28:1–10Google Scholar
  63. Wang J, Zhang C, Zhao X, Gadow KV (2013) Limitations to reproductive success in the dioecious tree Rhamnus davurica. PLoS One 8(12): e81140. Google Scholar
  64. Whitworth JL, Young E (1992) Chilling unit accumulation and forcing effects on carbohydrates of young apple rootstocks. J Hortic Sci 67:225–230. Google Scholar
  65. Wong BL, Baggett KL, Rye AH (2003) Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Can J Bot 81(8):780–788. Google Scholar
  66. Yasumura Y, Hikosaka K, Hirose T (2006) Seasonal changes in photosynthesis, nitrogen content and nitrogen partitioning in Lindera umbellata leaves grown in high or low irradiance. Tree Physiol 26:1315–1323. Google Scholar
  67. 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. Google Scholar

Copyright information

© Society for Plant Biochemistry and Biotechnology 2019

Authors and Affiliations

  • Vijay Laxmi Trivedi
    • 1
    Email author
  • Dharam Chand Attri
    • 1
  • Jyoti Sati
    • 1
  • Mohan Chandra Nautiyal
    • 1
  1. 1.High Altitude Plant Physiology Research Centre (HAPPRC)HNB Garhwal University (A Central University)Srinagar, GarhwalIndia

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