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Provitamin A carotenoids from an engineered high-carotenoid maize are bioavailable and zeaxanthin does not compromise β-carotene absorption in poultry

Transgenic Research volume 26, pages 591–601 (2017)Cite this article

Abstract

High-carotenoid (HC) maize, a biofortified staple crop which accumulates β-carotene, β-cryptoxanthin, lutein and zeaxanthin, was used as a feed component in a chicken feeding trial to assess the bioavailability of provitamin A (PVA) carotenoids in the kernel matrix compared to the synthetic and natural color additives routinely used in the poultry industry. We found that the PVA carotenoids in HC maize were not metabolized in the same manner: β-carotene was preferentially converted into retinol in the intestine whereas β-cryptoxanthin accumulated in the liver. We also considered the effect of zeaxanthin on the absorption of PVA carotenoids because zeaxanthin is the major carotenoid component of HC maize. We found that chickens fed on diets with low levels of zeaxanthin accumulated higher levels of retinol in the liver, suggesting that zeaxanthin might interfere with the absorption of β-carotene, although this observation was not statistically significant. Our results show that HC maize provides bioavailable carotenoids, including PVA carotenoids, and is suitable for use as a feed component.

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References

  • Bai C, Twyman RM, Farré G, Sanahuja G, Christou P, Capell T, Zhu C (2011) A golden era—pro-vitamin A enhancement in diverse crops. In Vitro Cell Dev Biol Plant 47:205–221

    Article  CAS  Google Scholar 

  • Bohn T (2008) Bioavailability of non-provitamin A carotenoids. Curr Nutr Food Sci 4:240–258

    Article  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

    CAS  PubMed  Google Scholar 

  • Bramley P (2003) The genetic enhancement of phytochemicals: the case of carotenoids. In: Johnson I, Williamson G (eds) Phytochemical functional foods. Woodhead Publishing Limited, Cambridge, pp 253–279

    Chapter  Google Scholar 

  • Breithaupt DE (2007) Modern application of xanthophylls in animal feeding—a review. Trends Food Sci Technol 18:501–506

    Article  CAS  Google Scholar 

  • Carbonell-Capella JM, Buniowska M, Barba FJ, Esteve MJ, Frígola A (2014) Analytical methods for determining bioavailability and bioaccessibility of bioactive compounds from fruits and vegetables: a review. Compr Rev Food Sci Food Saf 13:155–171

    Article  CAS  Google Scholar 

  • Castañeda MP, Hirschler EM, Sams AR (2005) Skin pigmentation evaluation in broilers fed natural and synthetic pigments. Poult Sci 84:143–147

    Article  PubMed  Google Scholar 

  • Commission Internationale de l’Éclairage—International Commission on Illumination (CIE) (2004) CIE 15: Technical Report: Colorimetry, 3rd edn. CIE, vol 552, p 24

  • Davis CR, Howe JA, Rocheford TR, Tanumihardjo SA (2008) The xanthophyll composition of biofortified maize (Zea mays sp.) does not influence the bioefficacy of provitamin A carotenoids in mongolian gerbils (Meriones unguiculatus). J Agric Food Chem 56:6745–6750

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Gómez J, Moreno JA, Angulo E, Sandmann G, Zhu C, Ramos AJ, Capell T, Christou P, Nogareda C (2017a) High-carotenoid biofortified maize is an alternative to color additives in poultry feed. Anim Feed Sci Technol. doi:10.1016/j.anifeedsci.2017.06.007

    Google Scholar 

  • Díaz-Gómez J, Twyman RM, Zhu C, Farré G, Serrano JCE, Portero-Otin M, Muñoz P, Sandmann G, Capell T, Christou P (2017b) Biofortification of crops with nutrients: factors affecting utilization and storage. Curr Opin Biotechnol 44:1–9

    Article  Google Scholar 

  • Escaron AL, Tanumihardjo SA (2006) Absorption and transit of lutein and beta-carotene supplements in the Mongolian gerbil (Meriones unguiculatus). Int J Vitam Nutr Res 76:315–323

    Article  CAS  PubMed  Google Scholar 

  • European Commission (2002) Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed. Off J Eur Commun L 269:1–15

    Google Scholar 

  • European Commission (2003) Commission Directive 2003/100/EC of 31 October 2003 amending Annex I to Directive 2002/32/EC of the European Parliament and of the Council on undesirable substances in animal feed. Off J Eur Union L 285:33–37

    Google Scholar 

  • European Commission (2006) Commission Recommendation of 17 August 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding (2006/576/EC). Off J Eur Union L 229:7–9

    Google Scholar 

  • European Commission (2007) Commission Recommendation of 18 June 2007 on guidelines for the accomodation and care of animals used for experimental and other scientific purposes (2007/526/EC). Off J Eur Union L 197:1–89

    Google Scholar 

  • European Commission (2009) Commission Regulation (EC) No. 152, 2009 of 27 January 2009 laying down the methods of sampling and analysis for the official control of feed. Off J Eur Union L 54(1):1–130

    Google Scholar 

  • European Commission (2013) Commission Recommendation of 27 March 2013 on the presence of T-2 and HT-2 toxin in cereals and cereal products (2013/165/EU). Off J Eur Union L 91:12–15

    Google Scholar 

  • European Parliament (2010) Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals for scientific purposes. Off J Eur Union L 276:33–79

    Google Scholar 

  • Farré G, Sanahuja G, Naqvi S, Bai C, Capell T, Zhu C, Christou P (2010) Travel advice on the road to carotenoids in plants. Plant Sci 179:28–48

    Article  Google Scholar 

  • Furr HC, Clark RM (1997) Intestinal absorption and tissue distribution of carotenoids. J Nutr Biochem 8:364–377

    Article  CAS  Google Scholar 

  • Gao Y-Y, Ji J, Jin L, Sun B-L, Xu L-H, Wang C-K, Bi Y-Z (2016) Xanthophyll supplementation regulates carotenoid and retinoid metabolism in hens and chicks. Poult Sci 95:541–549

    Article  PubMed  Google Scholar 

  • Gómez-Galera S, Rojas E, Sudhakar D, Zhu C, Pelacho AM, Capell T, Christou P (2010) Critical evaluation of strategies for mineral fortification of staple food crops. Transgenic Res 19:165–180

    Article  PubMed  Google Scholar 

  • Grolier P, Duszka C, Borel P, Alexandre-Gouabau MC, Azais-Braesco V (1997) In vitro and in vivo inhibition of beta-carotene dioxygenase activity by canthaxanthin in rat intestine. Arch Biochem Biophys 348:233–238

    Article  CAS  PubMed  Google Scholar 

  • Gurak PD, Mercadante AZ, González-Miret ML, Heredia FJ, Meléndez-Martínez AJ (2014) Changes in antioxidant capacity and colour associated with the formation of β-carotene epoxides and oxidative cleavage derivatives. Food Chem 147:160–169

    Article  CAS  PubMed  Google Scholar 

  • Institute of Medicine (US) (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

    Google Scholar 

  • International Life Sciences Institute (ILSI) International Food Biotechnology Committee (2007) Best practices for the conduct of animal studies to evaluate crops genetically modified for output traits. ILSI, Washington

    Google Scholar 

  • Jintasataporn O, Yuangsoi B (2012) Stability of carotenoid diets during feed processing and under different storage conditions. Molecules 17:5651–5660

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Oh D-K (2009) Substrate specificity of a recombinant chicken β-carotene 15,15′-monooxygenase that converts β-carotene into retinal. Biotechnol Lett 31:403–408

    Article  PubMed  Google Scholar 

  • Kim YS, Oh D-K (2010) Biotransformation of carotenoids to retinal by carotenoid 15,15′-oxygenase. Appl Microbiol Biotechnol 88:807–816

    Article  CAS  PubMed  Google Scholar 

  • Lee CM, Boileau AC, Boileau TW, Williams AW, Swanson KS, Heintz KA, Erdman JW (1999) Review of animal models in carotenoid research. J Nutr 129:2271–2277

    CAS  PubMed  Google Scholar 

  • Lietz G, Lange J, Rimbach G (2010) Molecular and dietary regulation of β, β-carotene 15,15′-monooxygenase 1 (BCMO1). Arch Biochem Biophys 502:8–16

    Article  CAS  PubMed  Google Scholar 

  • Liu G-D, Hou G-Y, Wang D-J, Lv S-J, Zhang X-Y, Sun W-P, Yang Y (2008) Skin pigmentation evaluation in broilers fed different levels of natural okra and synthetic pigments. J Appl Poult Res 17:498–504

    Article  CAS  Google Scholar 

  • Mamatha BS, Baskaran V (2011) Effect of micellar lipids, dietary fiber and β-carotene on lutein bioavailability in aged rats with lutein deficiency. Nutrition 27:960–966

    Article  CAS  PubMed  Google Scholar 

  • Molldrem KL, Tanumihardjo SA (2004) Lutein supplements are not bioavailable in the Mongolian gerbil while consuming a diet with or without cranberries. Int J Vitam Nutr Res 74:153–160

    Article  CAS  PubMed  Google Scholar 

  • Moreno JA, Díaz-Gómez J, Nogareda C, Angulo E, Sandmann G, Portero-Otin M, Serrano JCE, Twyman RM, Capell T, Zhu C, Christou P (2016) The distribution of carotenoids in hens fed on biofortified maize is influenced by feed composition, absorption, resource allocation and storage. Sci Rep 6:35346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Na JC, Song JY, Lee BD, Lee SJ, Lee CY, An GH (2004) Effect of polarity on absorption and accumulation of carotenoids by laying hens. Anim Feed Sci Technol 117:305–315

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Naqvi S, Zhu C, Farré G, Ramessar K, Bassie L, Breitenbach J, Perez Conesa D, Ros G, Sandmann G, Capell T, Christou P (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106:7762–7767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • National Research Council (NRC) (1994) Nutrient requeriments of poultry, 9th edn. National Academy Press, Washington DC

    Google Scholar 

  • National Research Council (NRC) (2011) Guide for the care and use of laboratory animals, 8th edn. National Academy Press, Washington

    Google Scholar 

  • Nogareda C, Moreno JA, Angulo E, Sandmann G, Portero M, Capell T, Zhu C, Christou P (2016) Carotenoid-enriched transgenic corn delivers bioavailable carotenoids to poultry and protects them against coccidiosis. Plant Biotechnol J 14:160–168

    Article  CAS  PubMed  Google Scholar 

  • Palczewski G, Amengual J, Hoppel CL, von Lintig J (2014) Evidence for compartmentalization of mammalian carotenoid metabolism. FASEB J 28:4457–4469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Vendrell AM, Hernández JM, Llauradó L, Schierle J, Brufau J (2001) Influence of source and ratio of xanthophyll pigments on broiler chicken pigmentation and performance. Poult Sci 80:320–326

    Article  PubMed  Google Scholar 

  • Pretorius B, Schönfeldt HC (2013) Effect of different maize meal diets on growth and vitamin A: case-study on chickens. Food Chem 140:520–525

    Article  CAS  PubMed  Google Scholar 

  • Reboul E (2013) Absorption of vitamin A and carotenoids by the enterocyte: focus on transport proteins. Nutrients 5:3563–3581

    Article  PubMed  PubMed Central  Google Scholar 

  • Saltzman A, Birol E, Bouis HE, Boy E, De Moura FF, Islam Y, Pfeiffer WH (2013) Biofortification: progress toward a more nourishing future. Glob Food Sec 2:9–17

    Article  Google Scholar 

  • Sanahuja G, Farré G, Berman J, Zorrilla-López U, Twyman RM, Capell T, Christou P, Zhu C (2013) A question of balance: achieving appropriate nutrient levels in biofortified staple crops. Nutr Res Rev 26:235–245

    Article  PubMed  Google Scholar 

  • Sandmann G (2002) Combinatorial biosynthesis of carotenoids in a heterologous host: a powerful approach for the biosynthesis of novel structures. ChemBioChem 3:629–635

    Article  CAS  PubMed  Google Scholar 

  • Sharifzadeh S, Clemmensen LH, Borggaard C, Stoier S, Ersboll BK (2014) Supervised feature selection for linear and non-linear regression of L*a*b* color from multispectral images of meat. Eng Appl Artif Intell 27:211–227

    Article  Google Scholar 

  • Tanumihardjo SA (2002) Factors influencing the conversion of carotenoids to retinol: bioavailability to bioconversion to bioefficacy. Int J Vitam Nutr Res 72:40–45

    Article  CAS  PubMed  Google Scholar 

  • Thakkar SK, Failla ML (2008) Bioaccessibility of pro-vitamin A carotenoids is minimally affected by non pro-vitamin A xanthophylls in maize (Zea mays sp.). J Agric Food Chem 56:11441–11446

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Roger Illingworth D, Connor SL, Barton Duell P, Connor WE (2010) Competitive inhibition of carotenoid transport and tissue concentrations by high dose supplements of lutein, zeaxanthin and beta-carotene. Eur J Nutr 49:327–336

    Article  CAS  PubMed  Google Scholar 

  • Yeum K-J, Russell RM (2002) Carotenoid bioavailability and bioconversion. Annu Rev Nutr 22:483–504

    Article  CAS  PubMed  Google Scholar 

  • Yuan J, Roshdy AR, Guo Y, Wang Y, Guo S (2014) Effect of dietary vitamin A on reproductive performance and immune response of broiler breeders. PLoS ONE 9:1–9

    Google Scholar 

  • Zhu C, Naqvi S, Breitenbach J, Sandmann G, Christou P, Capell T (2008) Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize. Proc Natl Acad Sci USA 105:18232–18237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Sanahuja G, Yuan D, Farré G, Arjó G, Berman J, Zorrilla-López U, Banakar R, Bai C, Pérez-Massot E, Bassie L, Capell T, Christou P (2013) Biofortification of plants with altered antioxidant content and composition: genetic engineering strategies. Plant Biotechnol J 11:129–141

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the University of Lleida for a Ph.D. fellowship awarded to J. Díaz-Gómez, IRTA-Mas de Bover (Reus, Spain) for diet formulation and manufacture, ITPSA (Barcelona, Spain) for providing the color additives, Ferran Roura for his involvement in the trial, and Antonio Michelena and Jaume Lloveras for the production of HC and M37W maize used in the preparation of the diets in experimental field trials.

Funding

This work was supported by La Caixa (Recercaixa project PC084082 VitaMaize: High quality and safe food through antioxidant fortified maize), the Spanish Ministry of Economy and Competitiveness (BIO2014-54426-P; BIO2014-54441-P, FEDER funds), the Catalan Government (2014 SGR 1296 Agricultural Biotechnology Research Group) and the Agrotecnio Center.

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Authors and Affiliations

  1. Food Technology Department, University of Lleida-Agrotecnio Center, Av. Rovira Roure 191, 25198, Lleida, Spain

    Joana Díaz-Gómez

  2. Animal Science Department, University of Lleida-Agrotecnio Center, Av. Rovira Roure 191, 25198, Lleida, Spain

    Joana Díaz-Gómez, Jose A. Moreno, Eduardo Angulo & Carmina Nogareda

  3. Biosynthesis Group, Department of Molecular Biosciences, J. W. Goethe University, Max von Laue Str. 9, 60438, Frankfurt, Germany

    Gerhard Sandmann

  4. Plant Production and Forestry Science Department, University of Lleida-Agrotecnio Center, Av. Rovira Roure 191, 25198, Lleida, Spain

    Changfu Zhu & Teresa Capell

Authors
  1. Joana Díaz-Gómez
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  2. Jose A. Moreno
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  3. Eduardo Angulo
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  4. Gerhard Sandmann
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Correspondence to Carmina Nogareda.

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Díaz-Gómez, J., Moreno, J.A., Angulo, E. et al. Provitamin A carotenoids from an engineered high-carotenoid maize are bioavailable and zeaxanthin does not compromise β-carotene absorption in poultry. Transgenic Res 26, 591–601 (2017). https://doi.org/10.1007/s11248-017-0029-y

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  • DOI: https://doi.org/10.1007/s11248-017-0029-y

Keywords

  • Chicken
  • Bioavailability
  • Metabolic engineering
  • Pigments
  • β-carotene