Review
The biosynthesis and nutritional uses of carotenoids

https://doi.org/10.1016/j.plipres.2003.10.002Get rights and content

Abstract

Carotenoids are isoprenoid molecules that are widespread in nature and are typically seen as pigments in fruits, flowers, birds and crustacea. Animals are unable to synthesise carotenoids de novo, and rely upon the diet as a source of these compounds. Over recent years there has been considerable interest in dietary carotenoids with respect to their potential in alleviating age-related diseases in humans. This attention has been mirrored by significant advances in cloning most of the carotenoid genes and in the genetic manipulation of crop plants with the intention of increasing levels in the diet. The aim of this article is to review our current understanding of carotenoid formation, to explain the perceived benefits of carotenoids in the diet and review the efforts that have been made to increase carotenoids in certain crop plants.

Introduction

The carotenoids are the most widespread group of pigments in nature, with over 600 characterised structurally and an estimated yield of 100 million tonnes per annum. They are present in all photosynthetic organisms and responsible for most of the yellow to red colours of fruits and flowers. The characteristic colours of many birds, insects and marine invertebrates are also due to the presence of carotenoids, which have originated in the diet. Commercially, carotenoids are used as food colourants and in nutritional supplements [1], with an estimated global market of some $935 million by 2005. Since animals are unable to synthesise carotenoids de novo, they rely upon the diet as the source of these compounds. There is considerable interest in dietary carotenoids with respect to their antioxidant properties and ability to alleviate chronic diseases. The large amount of research in this topic has been paralleled by the significant advances in cloning most of the genes involved in carotenogenesis and our increased understanding of factors that regulate carotenoid formation and deposition in plants. Taken together, it is these advances in knowledge that now open the way to enhancing carotenoid levels in crop plants and foods.

Carotenoids are isoprenoids and generally consist of eight isoprene units joined together so that the linking of units is reversed at the centre of the molecule to give methyl groups 20 and 20′ with a 1,6 positional relationship, whereas the remaining methyl groups are 1,5. The most obvious feature of the carotenoid molecule is the long polyene chain, which may extend from 3 to 15 conjugated double bonds. The length of the chromophore determines the absorption spectrum of the molecule and hence its colour to the eye. All are based upon seven different end groups of which only four (β,ε,κ,ψ) are found in higher plant carotenoids [2].

Cyclisation of the carbon skeleton occurs at one or both ends of the molecule, whilst xanthophylls are formed from the hydrocarbon carotenes by the introduction of oxygen functions. In addition, modifications involving chain elongation or degradation can occur. Many of the commonly used trivial names of carotenoids relate to the original source from which they were isolated, e.g. β-carotene from carrots. There is a systematic nomenclature [2]. In this article, however, the trivial names will be used.

Carotenoids found in the human diet are primarily derived from crop plants, where the carotenoids are located in roots, leaves, shoots, seeds, fruit and flowers. Around 60 different carotenoids have been identified in fruits and vegetables consumed by humans [3], [4], [5]. To a lesser extent, carotenoids can also be ingested in eggs, poultry and fish, where typically plant or algal products have been included in the feed of poultry or fish itself, e.g. zeaxanthin from maize in poultry feed. Typical amounts of carotenoids in crop plants are shown in Table 1.

More recently, a carotenoid database for European fruits and vegetables has been published [6], whilst those in vegetable oils are listed by Ong and Tee [7]. In contrast to most dietary carotenoids, sources of lycopene are limited, with at least 85% of our dietary lycopene coming from tomato fruit and tomato-based products, with the remainder being obtained from watermelon, pink grapefruit, guava and papaya (Table 2). Of the tomato products, juice, ketchup, soup and pizza and spaghetti sauces are the major contributors in the diet. A survey of carotenoid intake across Europe revealed considerable variation in the major dietary sources of carotenoids between countries [6].

Bioavailability is defined as the fraction of an ingested nutrient that becomes available to the body for utilisation in physiological functions or for storage [8]. There are at least 9 factors that influence the bioavailability of carotenoids: species of carotenoid, molecular linkage, amount consumed in a meal, matrix in which the carotenoid is incorporated, effectors of absorption and bioconversion, nutrient status of the host, genetic factors, host-related factors and interactions. These are often summarised in the mnemonic SLAMENGHI [9], [10], [11]. Since carotenoids are lipid-soluble they are taken up from the intestine far better from a fatty diet, although the amount of fat required is low, at about 3–5 g per meal [12]. The mechanism of fat-stimulated absorption may involve enhanced incorporation into mixed micelles. With respect to the food matrix, it has been shown that lutein is more bioavailable from spinach following disruption of the plant cell wall [13]. The uptake of β-carotene from vegetables is low (14% for mixed vegetables) compared with purified β-carotene added to a simple matrix [12]. Cis isomers of carotenoids appear to be more bioavailable than the all-trans forms [14], perhaps because they are more soluble in bile acid micelles and so preferentially incorporated into chylomicrons. It has been suggested that individual carotenoids antagonise absorption of each other, e.g. canthaxanthin inhibits lycopene uptake [15] and It is likely that uptake by intestinal cells is a facilitated process [16]. The use of isotopic tracer techniques to study bioavailability will improve the accuracy of such measurements [17], [18].

Once ingested, carotenoids appear in plasma, initially in the VLDL and chylomicron fractions and later in LDL and HDL. The highest levels are found in LDL. Serum concentrations, however, vary enormously, e.g., lycopene levels are from 50 to 900 nM, with large interperson variations. Studies of β-carotene uptake and plasma clearance, using human ileostomy volunteers showed that absorbed β-carotene is rapidly cleared from the plasma to an unobservable pool at a rate similar to that of chylomicron triacylglycerols [19].

Lycopene is found in most human tissues, but is not deposited uniformly (Table 3). These differences suggest that there are specific mechanisms for the preferential deposition of lycopene, particularly in the adrenals and testes.

Section snippets

Roles of carotenoids in animals

Carotenoids have a broad range of functions, especially in relation to human health and their role as biological antioxidants.

The biosynthesis of carotenoids

The biosynthetic pathways involved in carotenoid formation were elucidated in the 1950s and 1960s using classical biochemical approaches, using specific inhibitors and mutants blocked at certain steps in the pathway. In the early 1970s in vitro systems were developed [76] enabling the study of biosynthetic enzymes. Unfortunately, the practical difficulties associated with these enzymes prevented purification in most cases. The advent of modern molecular genetic techniques has facilitated gene

Regulation of carotenoid biosynthesis in higher plants

The regulation of carotenoid biosynthesis at the gene and enzyme level is poorly understood. No regulatory genes involved in carotenoid formation have been isolated, although the Or gene identified in cauliflower [162] and the apricot (Ap) tomato mutant look promising in this respect. The central role of carotenoids in plant development and adaptation suggest that their synthesis is coordinated with other developmental processes such as plastid formation, flowering and fruit development.

The

Strategies for enhancing carotenoid levels in crop plants

Before embarking on an experimental programme to enhance nutritionally important carotenoids in crop plants several pre-requisites should be considered. Confronting these issues at an early conceptual stage will enable achievable aims and objectives to be devised as well as placing proof of concept approaches on sound foundations for subsequent exploitation.

One of the first questions to be considered is what are the disease states to be addressed by dietary intake? Secondly, is there sound

Future prospects

The application of molecular genetics to the biotechnological exploitation of carotenoid formation has facilitated rapid advancements in our understanding of carotenoid biosynthesis and its manipulation in higher plants. The fundamental reaction sequences involved in the biosynthesis of carotenoids are now known and all encoding genes, with the exception of the α-hydroxylase, have now been isolated and identified. Quantitative and qualitative manipulations of the pathway have been reported.

Acknowledgements

The authors would like to thank past and present members of the laboratory for their valuable contributions to our studies quoted in this review. We also acknowledge with gratitude funding from the BBSRC, European Union, Royal Society, MAFF and Syngenta.

References (209)

  • P.M Bramley
  • A.J.H Ong et al.

    Methods Enzymol.

    (1992)
  • K.H Van het Hof et al.

    J. Nutr.

    (2000)
  • J.J.M Castenmiller et al.

    J. Nutr.

    (1999)
  • A.C Boileau et al.

    J. Nutr

    (1999)
  • A During et al.

    J Lip Res.

    (2002)
  • M Van Lieshout et al.

    Am. J. Clin. Nutr.

    (2003)
  • H.H Schmitz et al.

    Nutr

    (1991)
  • W Stahl et al.

    Archiv Biochem Biophys

    (1992)
  • T.M Redmond et al.

    J Biol. Chem.

    (2001)
  • A Lindqvist et al.

    J. Biol. Chem.

    (2002)
  • S.H Schwartz et al.

    Biochim Biophys Acta

    (2003)
  • C.E West et al.

    J. Nutr.

    (2002)
  • G.J Handelman

    Nutrition

    (2001)
  • P.M Bramley

    Phytochem

    (2000)
  • P Palozza et al.

    Free Rad Biol Med.

    (1995)
  • A.R Collins

    Mutat. Res.

    (2001)
  • L Brown et al.

    Am. J. Clin. Nutr.

    (1999)
  • R.A Bone et al.

    Exp. Eye Res.

    (1997)
  • D.M Snodderly

    Am. J. Clin. Nutr.

    (1995)
  • L Kohlmeier et al.

    Am. J. Clin. Nutr.

    (1995)
  • C.W Hadley et al.

    J. Nutr.

    (2003)
  • P Astorg

    Trends Fd Sci Technol

    (1997)
  • P Terry et al.

    Am. J. Clin. Nutr.

    (2002)
  • E.C Miller et al.

    Urol Clin N Am

    (2002)
  • M.L Slattery et al.

    Am. J. Clin. Nutr.

    (2000)
  • W Stahl et al.

    Am. J. Clin. Nutr.

    (2000)
  • W Eisenreich et al.

    Trends Plant Sci.

    (2001)
  • H Kasahara et al.

    J. Biol. Chem.

    (2002)
  • B.M Lange et al.

    Arch. Biochem. Biophys.

    (1999)
  • J Schwender et al.

    FEBS Lett.

    (1999)
  • J Querol et al.

    FEBS Lett.

    (2002)
  • B Maudinas et al.

    Biochem. Biophys. Res. Commun.

    (1975)
  • O Dogbo et al.

    Biochem Biophys Acta

    (1987)
  • M Lützow et al.

    Biochem Biophys Acta

    (1988)
  • B.C.L Weedon et al.
  • J.C Bauernfeind

    J Agric Fd Chem.

    (1972)
  • F Khachik et al.

    J Agric Food Chem.

    (1992)
  • K.J Scott et al.

    The carotenoid composition of vegetables and fruit commonly consumed in the UK

    (1994)
  • M.E O'Neill et al.

    Br. J. Nutr.

    (2001)
  • M.J Jackson

    Eur J Clin Nutr

    (1997)
  • J.J.M Castenmiller et al.

    Annu. Rev. Nutr.

    (1998)
  • S de Pee et al.

    Eur J Clin Nutr

    (1996)
  • K.-J Yeum et al.

    Annu. Rev. Nutr.

    (2002)
  • H Van den Berg

    Nutr Rev.

    (1999)
  • R.S Parker et al.

    Proc Nutr Soc.

    (1999)
  • R.M Faulks et al.

    Clin Sci.

    (1997)
  • S.K Clinton et al.

    Cancer Epidemiol Biomarkers Prev

    (1996)
  • J.A Olson et al.

    Proc Natl Acad Sci.

    (1965)
  • C Kiefer et al.

    J Biol Chem.

    (2002)
  • Cited by (0)

    View full text