Skip to main content
SpringerLink
Log in

NMR metabolomics of berry quality in sea buckthorn (Hippophae L.)

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Sea buckthorn (Hippophae L.) is a woody perennial shrub or small tree whose berries are rich in bioactive compounds with powerful nutritional and medicinal properties. Untargeted 1H nuclear magnetic resonance (NMR) spectroscopy and principal component analysis (PCA) were used to characterize the metabolic profile of berry quality. There was strong separation in the NMR signal intensity of bioactive compounds between pulp and seeds, such as amino acids [gamma-aminobutyric acid (GABA), aspartate, glutamate, theanine, and proline], organic acids (citrate, succinate, malate, acetate, quinate, and heriguard), and carbohydrates (sucrose, fructose, glucose, and melibiose). Sea buckthorn cultivars could be clearly separated into two groups using principal component analysis (PCA) based on NMR spectroscopy of bioactive compounds in the pulp and seeds. Several metabolic compounds such as sugar, organic acids, and amino acids could serve as biomarkers for prediction of berry quality and for classification of germplasm collections. This dataset provides potential information concerning the mechanisms of berry quality formation and contributes to increasing the breeding efficiency of sea buckthorn quality improvement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersson SC, Olsson ME, Johansson E, Rumpunen K (2009) Carotenoids in sea buckthorn (Hippophae rhamnoides L.) berries during ripening and use of pheophytin a as maturity marker. J Agric Food Chem 57:250–258

    Article  PubMed  CAS  Google Scholar 

  • Arif S, Ahmed SD, Shah AH, Hassan L, Awan SI, Hamid A, Batool F (2010) Determination of optimum harvesting time for vitamin C, oil and mineral elements in berries sea buckthorn (Hippophae rhamnoides). Pak J Bot 42:3561–3568

    CAS  Google Scholar 

  • Bal LM, Meda V, Naik SN, Satya S (2011) Sea buckthorn berries: a potential source of valuable nutrients for nutraceuticals and cosmoceuticals. Food Res Int 44:1718–1727

    Article  CAS  Google Scholar 

  • Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  PubMed  CAS  Google Scholar 

  • Breitkreuz KE, Shelp BJ, Fischer WN, Schwacke R, Rentsch D (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett 450:280–284

    Article  PubMed  CAS  Google Scholar 

  • Caspi R, Altman T, Dale JM, Dreher K, Fulcher CA, Gilham F, Kaipa P, Karthikeyan AS, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Paley S, Popescu L, Pujar A, Shearer AG, Zhang P, Karp PD (2010) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 38:D473–D479

    Article  PubMed  CAS  Google Scholar 

  • Chaman S, Syed N, Danish Z, Khan F (2011) Phytochemical analysis, antioxidant and antibacterial effects of sea buckthorn berries. Pak J Pharm Sci 24:345–351

    PubMed  CAS  Google Scholar 

  • Choi YH, Sertic S, Kim HK, Wilson EG, Michopoulos F, Lefeber AWN, Erkelens C, Kricun SDP, Verpoorte R (2005) Classification of IIex species based on metabolomics fingerprinting using nuclear magnetic resonance and multivariate data analysis. J Agric Food Chem 53:1237–1245

    Article  PubMed  CAS  Google Scholar 

  • Deborde C, Maucourt M, Baldet P, Bernillon S, Biais B, Talon G, Ferrand C, Jacob D, Helene FD, Daruvar A, Rolin D, Moing A (2009) Proton NMR quantitative profiling for quality assessment of greenhouse-grown tomato fruit. Metabolomics 5:183–198

    Article  CAS  Google Scholar 

  • Deleanu M, Kiss C, Nicolescu A, Socaciu C, Deleanu C (2009) Characterization of sea buckthorn oil by GC and 1H-NMR. Bull UASVM Agric 66:559

    Google Scholar 

  • Duddeck H, Dietrich W, Toth G (1998) Structure elucidation by modern NMR: a workbook. Springer-Steinkopff, Darmstadt

    Google Scholar 

  • Eriksson L, Johansson E, Kettaneh-Wold N, Wold S (2001) Multi- and megavariate data analysis: principles and applications. Umetrics AB, Umeå, pp 43–111

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hall RD (2011) Plant metabolomics in a nutshell: potential and future challenges. Ann Plant Rev 43:1–24

    Article  CAS  Google Scholar 

  • Han YZ, Feng XJ, You J, Chen X, Ning P, Zhang Y (2008) Survival performance of introduced 5 large berry cultivars of sea buckthorn in Shanxi province (in Chinese with English abstract). J Shanxi Agric Univ (Nat Sci Edit) 28:241–245

    Google Scholar 

  • Heinaaho M, Hegerman AE, Julkunen-Tiitto R (2009) Effect of different organic farming methods on the phenolic composition of sea buckthorn berries. J Agric Food Chem 57:1940–1947

    Article  PubMed  CAS  Google Scholar 

  • Holmes E, Loo RL, Stamler J, Bictash M, Yap IKS, Chan Q, Ebbels T, De Iorio M, Brown IJ, Veselkov KA, Daviglus ML, Kesteloot H, Ueshima H, Zhao L, Nicholson JK, Elliott P (2008) Human metabolic phenotype diversity and its association with diet and blood pressure. Nature 453:396–400

    Article  PubMed  CAS  Google Scholar 

  • Huang Q, Zhao Y (2004) Selection and breeding of Wucifeng and Shengqiuhong sea buckthorn (in Chinese with English abstract). Hippophae 17:7–9

    Google Scholar 

  • Kallio H, Lassila M, Jarvenpaa E, Haraldsson GG, Jonsdottir S, Yang BR (2009) Inositols and methylinositols in sea buckthorn (Hippophae rhamnoides) berries. J Chromatogr B 877:1426–1432

    Article  CAS  Google Scholar 

  • Lee EJ, Shaykhutdinov R, Weljie AM, Vogel HJ, Facchini PJ (2009) Quality assessment of ginseng by 1H NMR metabolite fingerprinting and profiling analysis. J Agric Food Chem 57:7513–7522

    Article  PubMed  CAS  Google Scholar 

  • Li DQ, Liang YM, Hou XL, Huang J, Jiang J, Ruan CJ, Hao DY, Qi JY (2004) A study on the functions and benefits of sea buckthorn for improving eco-environment of the loess plateau (in Chinese with English Abstract). Global Sea Buckthorn Res Develop 2:6–11

    Google Scholar 

  • Li Q, Li H, Ruan CJ, Wang XY (2009) Assessment of genetic stability of propagated plantlets of four Hippophae varieties and the establishment of genetic relationships between them by ISSR markers. Int J Fruit Sci 9:232–246

    Article  Google Scholar 

  • Liang YQ, Liu P, Chen XJ (2009) Research progress on the soil conservation functions of sea buckthorn and resources utilization (in Chinese with English Abstract). Subtropic Soil Water Conserv 21:35–38

    Google Scholar 

  • Lindo JC, Nicholson JK, Everett JR (1999) NMR spectroscopy of biofluids. Annu Rep NMR Spectrosc 38:1–88

    Article  Google Scholar 

  • Maloney V (2004) Plant metabolomics. Bio Teach J 2:92–99

    Google Scholar 

  • Mao XA (2000) Modern NMR technique and application (in Chinese). Shanghai Press of Science and Technology, Shanghai

    Google Scholar 

  • Michel T, Destandau E, Elfakir C (2011) On-line hyphenation of centrifugal partition chromatography and high pressure liquid chromatography for the fractionation of flavonoids from Hippophae rhamnoides L. berries. J Chromatogr A 1218:6173–6178

    Article  PubMed  CAS  Google Scholar 

  • Moco S, Schneider B, Vervoort J (2009) Plant micrometabolomics: the analysis of endogenous metabolites present in a plant cell or tissue. J Prot Res 8:1694–1703

    Article  CAS  Google Scholar 

  • Pereira GE, Gaudillere JP, Van Leeuwen C, Hilbert G, Lavialle O, Maucourt M, Deborde C, Moing A, Rolin D (2005) 1H NMR and chemometrics to characterize mature grape berries in four wine-growing areas in Bordeaux, France. J Agric Food Chem 53:6382–6389

    Article  PubMed  CAS  Google Scholar 

  • Pereira GE, Gaudillere JP, Van Leeuwen C, Hilbert G, Maucourt M, Deborde C, Moing A, Rolin D (2006) 1H NMR metabolite fingerprints of grape berry: comparison of vintage and soil effects in Bordeaux grapevine growing areas. Anal Chim Acta 563:346–352

    Article  CAS  Google Scholar 

  • Rosch D, Krumbein A, Mugge C, Kroh LW (2004) Structural investigations of flavonol glycosides from sea buckthorn (Hippophae rhamnoides) pomace by NMR spectroscopy and HPLC-ESI-MS. J Agric Food Chem 52:4039–4046

    Article  PubMed  Google Scholar 

  • Ruan CJ, Teixeira da Silva JA (2011) Metabolomics: creating new potentials for unraveling the mechanisms in response to salt and drought stress and for the biotechnological improvement of xero-halophytes. Crit Rev Biotechnol 31:153–169

    Article  PubMed  CAS  Google Scholar 

  • Ruan CJ, Teixeira da Silva JA, Li Q, Li H, Zhang J (2010) Pathogenicity of dried-shrink disease and evaluation of resistance in a germplasm collection of sea buckthorn (Hippophae L.) from China and other countries. Sci Hortic 127:70–78

    Article  Google Scholar 

  • Schripsema J (2009) Application of NMR in plant metabolomics: techniques, problems and prospects. Phytochem Anal 21:14–21

    Article  Google Scholar 

  • Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. Plant Cell 11:377–391

    PubMed  CAS  Google Scholar 

  • Socaciu C (2011) Metabolomics studies applied on different sea buckthorn (Hippophae rhamnoides L.) varieties. Abstract of PhD thesis. University of Agricultural Sciences and Veterinary Medicine, Romania

  • Tang X, Kalviainen N, Tuorila H (2001) Sensory and hedonic characteristics of juice of sea buckthorn (Hippophae rhamnoides L.) origins and hybrids. Lebensm Wiss Technol 34:102–110

    Article  CAS  Google Scholar 

  • Tarachiwin L, Masako O, Fukusaki E (2008) Quality evaluation and prediction of Citrullus lanatus by 1H NMR based metabolomics and multivariate analysis. J Agric Food Chem 56:5827–5835

    Article  PubMed  CAS  Google Scholar 

  • Tarpley L, Duran AL, Kebrom TH, Sumner LW (2005) Biomarker metabolites capturing the metabolite variance present in a rice plant developmental period. BMC Plant Biol 5:8

    Article  PubMed  Google Scholar 

  • Tiitinen KM, Yang BR, Haraldsson GG, Jonsdottir S, Kallio HP (2006a) Fast analysis of sugars, fruit acids, and vitamin C in sea buckthorn (Hippophae rhamnoides L.) varieties. J Agric Food Chem 54:2508–2513

    Article  PubMed  CAS  Google Scholar 

  • Tiitinen K, Vahvaselka M, Hakala M, Laakso S, Kallio H (2006b) Malolactic fermentation in sea buckthorn (Hippophae rhamnoides) juice processing. Eur Food Res Technol 222:686–691

    Article  CAS  Google Scholar 

  • Wang L (2007) The study based on 1H-NMR-MSA on the plants of Hippophae Linn. M.Sc. Thesis. Sichuan University, China

  • Wannes WA, Mhamdi B, Sriti J, Marzouk B (2010) Glycerolipid and fatty acid distribution in pericarp, seed and whole fruit oils of Myrtus communis var. italica. Ind Crop Prod 31:77–83

    Article  CAS  Google Scholar 

  • Ward JL, Harris C, Lewis J, Beale MH (2003) Assessment of 1H NMR spectroscopy and multivariate analysis as a technique for metabolite fingerprinting of Arabidopsis thaliana. Phytochemistry 62:949–957

    Article  PubMed  CAS  Google Scholar 

  • Yang BR, Zheng J, Kallio H (2011) Influence of origin, harvesting time and weather conditions on content of inositols and methylinositols in sea buckthorn (Hippophae rhamnoides) berries. Food Chem 125:388–396

    Article  CAS  Google Scholar 

  • Zheng J, Kallio H, Linderborg K, Yang BR (2011) Sugars, sugar alcohols, fruit acids, and ascorbic acid in wild Chinese sea buckthorn (Hippophae rhamnoides ssp. sinensis) with special reference to influence of latitude and altitude. Food Res Int 44:2018–2026

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was jointly supported by a Marie Curie International Incoming Fellowship (main and return phase) within the 7th European Community Framework Programme (PIIF-GA-2010-272048-HIPPOHEALTH, PIIFR-GA-2010-910048-HIPPOHEALTH), the Agriculture Science and Technology Research Item of the Liaoning Scientific and Technological Committee of China (nos. 2007207005, 2008207001), and the Fundamental Research Funds for the Central Universities (no. DC12010220).

Author information

Authors and Affiliations

  1. College of Life Science, Liaoning Normal University, Dalian, 116029, China

    Wei Li & Chun-E Zhao

  2. Institute of Bio-Resources, Dalian Nationalities University, Dalian City, 116600, Liaoning, China

    Cheng-Jiang Ruan

  3. Department of Plant Breeding and Biotechnology Balsgård, Swedish University of Agricultural Sciences, 29194, Kristianstad, Sweden

    Cheng-Jiang Ruan

  4. Faculty of Agriculture and Graduate School of Agriculture, Kagawa University, Miki-cho, Kagawa, 761-0795, Japan

    Jaime A. Teixeira da Silva

  5. Plant Materials Center for Soil and Water Conservation, Ministry of Water Resources, Beijing, 100038, China

    Hai Guo

  6. Conseco Sea buckthorn Co., Ltd., Beijing, 100038, China

    Hai Guo

Authors
  1. Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng-Jiang Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaime A. Teixeira da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hai Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chun-E Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cheng-Jiang Ruan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, W., Ruan, CJ., Teixeira da Silva, J.A. et al. NMR metabolomics of berry quality in sea buckthorn (Hippophae L.). Mol Breeding 31, 57–67 (2013). https://doi.org/10.1007/s11032-012-9768-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-012-9768-x

Keywords

Search

Navigation