Skip to main content
SpringerLink
Log in

Lipid-dissolved γ-carotene, β-carotene, and lycopene in globular chromoplasts of peach palm (Bactris gasipaes Kunth) fruits

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

High levels of β-carotene, lycopene, and the rare γ-carotene occur predominantly lipid-dissolved in the chromoplasts of peach palm fruits. First proof of their absorption from these fruits is reported.

The structural diversity, the physical deposition state in planta, and the human bioavailability of carotenoids from the edible fruits of diverse orange and yellow-colored peach palm (Bactris gasipaes Kunth) varieties were investigated. HPLC–PDA–MSn revealed a broad range of carotenes, reaching total carotenoid levels from 0.7 to 13.9 mg/100 g FW. Besides the predominant (all-E)-β-carotene (0.4–5.4 mg/100 g FW), two (Z)-isomers of γ-carotene (0.1–3.9 mg/100 g FW), and one (Z)-lycopene isomer (0.04–0.83 mg/100 g FW) prevailed. Approximately 89–94 % of total carotenoid content pertained to provitamin A carotenoids with retinol activity equivalents ranging from 37 to 609 µg/100 g FW. The physical deposition state of these carotenoids in planta was investigated using light, transmission electron, and scanning electron microscopy. The plastids found in both orange and yellow-colored fruit mesocarps were amylo-chromoplasts of the globular type, containing carotenoids predominantly in a lipid-dissolved form. The hypothesis of lipid-dissolved carotenoids was supported by simple solubility estimations based on carotenoid and lipid contents of the fruit mesocarp. In our study, we report first results on the human bioavailability of γ-carotene, β-carotene, and lycopene from peach palm fruit, particularly proving the post-prandial absorption of the rarely occurring γ-carotene. Since the physical state of carotenoid deposition has been shown to be decisive for carotenoid bioavailability, lipid-dissolved carotenoids in peach palm fruits are expected to be highly bioavailable, however, further studies are required.

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

Abbreviations

FW:

Fresh weight

RAE:

Retinol activity equivalents

TEM:

Transmission electron microscopy

TRL:

Triglyceride-rich lipoprotein

References

  • Bauernfeind JC (1972) Carotenoid vitamin A precursors and analogs in foods and feeds. J Agric Food Chem 20:456–473

    Article  PubMed  CAS  Google Scholar 

  • Ben-Amotz A, Lers A, Avron M (1988) Stereoisomers of β-carotene and phytoene in the alga Dunaliella bardawil. Plant Physiol 86:1286–1291

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Boehm V, Puspitasari-Nienaber NL, Ferruzzi MG, Schwartz SJ (2002) Trolox equivalent antioxidant capacity of different geometrical isomers of α-carotene, β-carotene, lycopene, and zeaxanthin. J Agric Food Chem 50:221–226

    Article  CAS  Google Scholar 

  • Borel P (2012) Genetic variations involved in interindividual variability in carotenoid status. Mol Nutr Food Res 56:228–240

    Article  PubMed  CAS  Google Scholar 

  • Borel P, Grolier P, Armand M, Partier A, Lafont H, Lairon D, Azais-Braesco V (1996) Carotenoids in biological emulsions: solubility, surface-to-core distribution, and release from lipid droplets. J Lipid Res 37:250–261

    PubMed  CAS  Google Scholar 

  • Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1b., spectroscopy. Birkhäuser Verlag, Basel, Boston, Berlin, pp 13–62

    Google Scholar 

  • Britton G (1998) Overview of carotenoid biosynthesis. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 3., Biosynthesis and metabolism. Birkhäuser Verlag, Basel, Boston, Berlin, pp 13–147

    Google Scholar 

  • Brown MJ, Ferruzzi MG, Nguyen ML, Cooper DA, Eldridge AL, Schwartz SJ, White WS (2004) Carotenoid bioavailability is higher from salads ingested with full-fat than with fat-reduced salad dressings as measured with electrochemical detection. Am J Clin Nutr 80:396–403

    PubMed  CAS  Google Scholar 

  • Burns J, Fraser PD, Bramley PM (2003) Identification and quantification of carotenoids, tocopherols and chlorophylls in commonly consumed fruits and vegetables. Phytochemistry 62:939–947

    Article  PubMed  CAS  Google Scholar 

  • Castenmiller JJM, West CE (1998) Bioavailability and bioconversion of carotenoids. Annu Rev Nutr 18:19–38

    Article  PubMed  CAS  Google Scholar 

  • De Rosso VV, Mercadante AZ (2007) Identification and quantification of carotenoids, by HPLC-PDA-MS/MS, from Amazonian fruits. J Agric Food Chem 55:5062–5072

    Article  PubMed  Google Scholar 

  • Deruere J, Romer S, d’Harlingue A, Backhaus RA, Kuntz M, Camara B (1994) Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6:119–133

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Devitt LC, Fanning K, Dietzgen RG, Holton TA (2010) Isolation and functional characterization of a lycopene β-cyclase gene that controls fruit colour of papaya (Carica papaya L.). J Exp Bot 61:33–39

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dias MG, Camões MFGFC, Oliveira L (2009) Carotenoids in traditional Portuguese fruits and vegetables. Food Chem 113:808–815

    Article  CAS  Google Scholar 

  • FAO/WHO (2001) Vitamin A. Human vitamin and mineral requirements. FAO, Rome, pp 87–101

    Google Scholar 

  • Ferruzzi MG, Nguyen ML, Sander LC, Rock CL, Schwartz SJ (2001) Analysis of lycopene geometrical isomers in biological microsamples by liquid chromatography with coulometric array detection. J Chromatogr B Biomed Sci Appl 760:289–299

    Article  PubMed  CAS  Google Scholar 

  • Gamlieli-Bonshtein I, Korin E, Cohen S (2002) Selective separation of cis-trans geometrical isomers of β-carotene via CO2 supercritical fluid extraction. Biotechnol Bioeng 80:169–174

    Article  PubMed  CAS  Google Scholar 

  • Garti N, Shevachman M, Shani A (2004) Solubilization of lycopene in jojoba oil microemulsion. JAOCS J Am Oil Chem Soc 81:873–877

    Article  CAS  Google Scholar 

  • Hansmann P, Sitte P (1982) Composition and molecular structure of chromoplast globules of Viola tricolor. Plant Cell Rep 1:111–114

    Article  PubMed  CAS  Google Scholar 

  • Institute of Medicine (2001) Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium and zinc. National Academy Press, Washington, DC

    Google Scholar 

  • Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell 14:333–342

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jatunov S, Quesada S, Díaz C, Murillo E (2010) Carotenoid composition and antioxidant activity of the raw and boiled fruit mesocarp of six varieties of Bactris gasipaes. Arch Latinoam Nutr 60:99–104

    PubMed  CAS  Google Scholar 

  • Kishimoto S, Ohmiya A (2012) Carotenoid isomerase is key determinant of petal color of Calendula officinalis. J Biol Chem 287:276–285

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kopec RE, Riedl KM, Harrison EH, Curley RW Jr, Hruszkewycz DP, Clinton SK, Schwartz SJ (2010) Identification and quantification of apo-lycopenals in fruits, vegetables, and human plasma. J Agric Food Chem 58:3290–3296

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kopec RE, Schweiggert RM, Riedl KM, Carle R, Schwartz SJ (2013) Comparison of high-performance liquid chromatography/tandem mass spectrometry and high-performance liquid chromatography/photo-diode array detection for the quantitation of carotenoids, retinyl esters, α-tocopherol and phylloquinone in chylomicron-rich fractions of human plasma. Rapid Commun Mass Spectrom 27:1393–1402

    Article  PubMed  CAS  Google Scholar 

  • Leterme P, García M-F, Londoño A-M, Rojas M-G, Buldgen A, Souffrant W-B (2005) Chemical composition and nutritive value of peach palm (Bactris gasipaes Kunth) in rats. J Sci Food Agric 85:1505–1512

    Article  CAS  Google Scholar 

  • Marx M, Schieber A, Carle R (2000) Quantitative determination of carotene stereoisomers in carrot juices and vitamin supplemented (ATBC) drinks. Food Chem 70:403–408

    Article  CAS  Google Scholar 

  • McLellan MR, Lind LR, Kime RW (1995) Hue angle determinations and statistical analysis for multiquadrant Hunter L, a, b data. J Food Qual 18:235–240

    Article  Google Scholar 

  • Monge-Rojas R, Campos H (2011) Tocopherol and carotenoid content of foods commonly consumed in Costa Rica. J Food Compos Anal 24:202–216

    Article  CAS  Google Scholar 

  • Mortensen A (2005) Analysis of a complex mixture of carotenes from oil palm (Elaeis guineensis) fruit extract. Food Res Int 38:847–853

    Article  CAS  Google Scholar 

  • Namitha KK, Negi PS (2010) Chemistry and biotechnology of carotenoids. Crit Rev Food Sci Nutr 50:728–760

    Article  PubMed  CAS  Google Scholar 

  • Nguyen M, Francis D, Schwartz S (2001) Thermal isomerisation susceptibility of carotenoids in different tomato varieties. J Sci Food Agric 81:910–917

    Article  CAS  Google Scholar 

  • Nielsen JP (1943) Rapid determination of starch. An index to maturity in starchy vegetables. Ind Eng Chem Anal Ed 15:176–179

    Article  CAS  Google Scholar 

  • Provesi JG, Dias CO, Amante ER (2011) Changes in carotenoids during processing and storage of pumpkin puree. Food Chem 128:195–202

    Article  PubMed  CAS  Google Scholar 

  • Quesada S, Azofeifa G, Jatunov S, Jiménez G, Navarro L, Gómez G (2011) Carotenoids composition, antioxidant activity and glycemic index of two varieties of Bactris gasipaes. Emir J Food Agric 23:482–489

    Google Scholar 

  • Rojas-Garbanzo C, Pérez AM, Bustos-Carmona J, Vaillant F (2011) Identification and quantification of carotenoids by HPLC-DAD during the process of peach palm (Bactris gasipaes H.B.K.) flour. Food Res Int 44:2377–2384

    Article  CAS  Google Scholar 

  • Schweiggert RM, Steingass CB, Mora E, Esquivel P, Carle R (2011a) Carotenogenesis and physico-chemical characteristics during maturation of red fleshed papaya fruit (Carica papaya L.). Food Res Int 44:1373–1380

    Article  CAS  Google Scholar 

  • Schweiggert RM, Steingass CB, Heller A, Esquivel P, Carle R (2011b) Characterization of chromoplasts and carotenoids of red- and yellow-fleshed papaya (Carica papaya L.). Planta 234:1031–1044

    Article  PubMed  CAS  Google Scholar 

  • Schweiggert RM, Mezger D, Schimpf F, Steingass CB, Carle R (2012a) Influence of chromoplast morphology on carotenoid bioaccessibility of carrot, mango, papaya, and tomato. Food Chem 135:2736–2742

    Article  PubMed  CAS  Google Scholar 

  • Schweiggert RM, Steingass CB, Esquivel P, Carle R (2012b) Chemical and morphological characterization of Costa Rican papaya (Carica papaya L.) hybrids and lines with particular focus on their genuine carotenoid profiles. J Agric Food Chem 60:2577–2585

    Article  PubMed  CAS  Google Scholar 

  • Schweiggert RM, Kopec RE, Villalobos-Gutierrez MG, Högel J, Quesada S, Esquivel P, Schwartz SJ, Carle R (2013) Carotenoids are more bioavailable from papaya than from tomato and carrot in humans: a randomised cross-over study. Br J Nutr 111:490–498

    Article  PubMed  PubMed Central  Google Scholar 

  • Sitte P, Falk H, Liedvogel B (1980) Chromoplasts. In: Czygan FC (ed) Pigments in plants. Gustav Fischer Verlag, Stuttgart, New York, pp 117–148

    Google Scholar 

  • Straus W (1953) Chromoplast—development of crystalline forms, structure, state of the pigments. Bot Rev 19:147–186

    Article  CAS  Google Scholar 

  • Surles RL, Weng N, Simon PW, Tanumihardjo SA (2004) Carotenoid profiles and consumer sensory evaluation of specialty carrots (Daucus carota, L.) of various colors. J Agric Food Chem 52:3417–3421

    Article  PubMed  CAS  Google Scholar 

  • USDA (2012) USDA national nutrient database for standard reference, Release 25. Nutrient Data Laboratory Home Page. http://www.ars.usda.gov/ba/bhnrc/ndl. Accessed Aug 2013

  • Vásquez-Caicedo AL, Sruamsiri P, Carle R, Neidhart S (2005) Accumulation of all-trans-β-carotene and its 9-cis and 13-cis stereoisomers during postharvest ripening of nine thai mango cultivars. J Agric Food Chem 53:4827–4835

    Article  PubMed  Google Scholar 

  • Vásquez-Caicedo AL, Heller A, Neidhart S, Carle R (2006) Chromoplast morphology and β-carotene accumulation during postharvest ripening of mango Cv. ‘Tommy Atkins’. J Agric Food Chem 54:5769–5776

    Article  PubMed  Google Scholar 

  • Vishnevetsky M, Ovadis M, Vainstein A (1999) Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4:232–235

    Article  PubMed  Google Scholar 

  • Zechmeister L (1949) Stereoisomeric provitamins A. Vitam Horm 7:57–81

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Erika Rücker (Institute of Botany, Universität Hohenheim) for supporting transmission electron microscopy. J.H. is grateful for a travel grant by the fiat panis Foundation (Ulm, Germany). We also thank the Alexander von Humboldt Foundation (Bonn, Germany) for partially funding this study in the frame of the Research Group Linkage Program.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Institute of Food Science and Biotechnology, Hohenheim University, 70599, Stuttgart, Germany

    Judith Hempel, Reinhold Carle & Ralf M. Schweiggert

  2. Institute of Botany, Hohenheim University, 70599, Stuttgart, Germany

    Evelyn Amrehn & Annerose Heller

  3. Department of Biochemistry, School of Medicine, University of Costa Rica, 2060, San Pedro, Costa Rica

    Silvia Quesada

  4. School of Food Technology, University of Costa Rica, 2060, San Pedro, Costa Rica

    Patricia Esquivel

  5. CIGRAS, University of Costa Rica, 2060, San Pedro, Costa Rica

    Víctor M. Jiménez

  6. Biological Science Department, King Abdulaziz University, P. O. Box 80257, Jeddah, 21589, Saudi Arabia

    Reinhold Carle

Authors
  1. Judith Hempel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Evelyn Amrehn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Silvia Quesada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia Esquivel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Víctor M. Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Annerose Heller
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Reinhold Carle
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ralf M. Schweiggert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ralf M. Schweiggert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hempel, J., Amrehn, E., Quesada, S. et al. Lipid-dissolved γ-carotene, β-carotene, and lycopene in globular chromoplasts of peach palm (Bactris gasipaes Kunth) fruits. Planta 240, 1037–1050 (2014). https://doi.org/10.1007/s00425-014-2121-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2121-3

Keywords

Search

Navigation