Plant Science Travel Advice on the Road to Carotenoids in Plants
Total Page：16
File Type：pdf, Size：1020Kb
Plant Science 179 (2010) 28–48 Contents lists available at ScienceDirect Plant Science journal homepage: www.elsevier.com/locate/plantsci Review Travel advice on the road to carotenoids in plants Gemma Farré a, Georgina Sanahuja a, Shaista Naqvi a, Chao Bai a, Teresa Capell a, Changfu Zhu a, Paul Christou a,b,∗ a Departament de Producció Vegetal i Ciència Forestal, Universitat de Lleida, Av. Alcalde Rovira Roure, 191, Lleida 25198, Spain b Institució Catalana de Recerca i Estudis Avanc¸ ats (ICREA), Barcelona, Spain article info abstract Article history: The carotenoids are a major class of organic pigments produced in plants and microbes. They fulfill many Received 20 January 2010 essential physiological and developmental processes in plants, and also have important roles in animal Received in revised form 8 March 2010 health and nutrition. As such they have been the focus of multidisciplinary research programs aiming Accepted 9 March 2010 to understand how they are synthesized in microbes and plants, and to clone genes encoding the corre- Available online 3 April 2010 sponding enzymes and express them to modulate carotenoid production in recombinant microbial and plant systems. Our deeper understanding of carotenogenic gene regulation, in concert with the develop- Keywords: ment of more effective multi-gene transfer systems for plants, has facilitated more ambitious strategies Secondary metabolites Metabolic engineering for the modulation of plant carotenoid biosynthesis not only in laboratory models but more importantly Plant transformation in staple food crops. Here we review the genetic and molecular tools and resources available for fun- Biosynthetic pathways damental and applied carotenoid research, emphasizing recent achievements in carotenoid engineering Complementation and potential future objectives for carotenoid research in plants. Nutritional improvement © 2010 Elsevier Ireland Ltd. All rights reserved. Contents 1. Introduction .......................................................................................................................................... 29 2. Carotenoid biosynthesis in plants .................................................................................................................... 29 3. Strategies to alter the carotenoid content and composition of plants ............................................................................... 31 4. Resources for applied carotenoid research ........................................................................................................... 35 4.1. Cloned genes and their corresponding enzymes ............................................................................................. 35 4.2. Germplasm (natural diversity and specific mutants) ........................................................................................ 35 4.2.1. Cereal crops ......................................................................................................................... 36 4.2.2. Root vegetables (potato and carrot) ................................................................................................ 36 4.2.3. Tomato and other fruit .............................................................................................................. 36 4.3. Bacterial strains for complementation studies ............................................................................................... 38 4.4. Transgenic plant lines with altered carotenoid profiles ...................................................................................... 39 4.4.1. Laboratory models .................................................................................................................. 39 4.4.2. Golden rice .......................................................................................................................... 39 4.4.3. Amber potatoes and red carrots .................................................................................................... 39 4.4.4. Tomato and other fruits ............................................................................................................. 39 4.4.5. Carotenoid-rich canola .............................................................................................................. 43 4.4.6. Combinatorial transformation in corn .............................................................................................. 43 5. Outlook ............................................................................................................................................... 43 5.1. Outlook for fundamental research ............................................................................................................ 43 5.2. Outlook for applied research.................................................................................................................. 43 Acknowledgements .................................................................................................................................. 44 References ............................................................................................................................................ 44 ∗ Corresponding author. Tel.: +34 973702693; fax: +34 973238264. E-mail addresses: [email protected] (G. Farré), [email protected] (G. Sanahuja), [email protected] (S. Naqvi), [email protected] (C. Bai), [email protected] (T. Capell), [email protected] (C. Zhu), [email protected] (P. Christou). 0168-9452/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.plantsci.2010.03.009 G. Farré et al. / Plant Science 179 (2010) 28–48 29 1. Introduction The bewildering array of available tools and resources makes it difficult to appreciate the best route to follow when embarking Carotenoids are organic pigments that are produced predomi- on carotenoid research. In this review, we provide a guide to the nantly (but not exclusively) by photosynthetic organisms. In plants, resources available to investigators and discuss the most effective their presence is revealed by the rich color of flowers, fruits and strategies for carotenoid research in plants. storage organs in the yellow-to-red part of the spectrum. This reflects the characteristic linear C40 molecular backbone contain- ing up to 11 conjugated double bonds, the number and nature of 2. Carotenoid biosynthesis in plants which determines the excitation and emission maxima and result- ing spectral properties [1]. Animals cannot synthesize carotenoids Carotenoids are tetraterpenoids, i.e. they comprise eight con- but may derive pigmentation from those in their diet, e.g. the yel- densed C5 isoprenoid precursors generating a C40 linear backbone. low of egg yolk, and the pink of lobster shells, salmon flesh and In plants, this condensation reaction involves the isomeric precur- flamingo feathers [2]. sors isopentenyl diphosphate (IPP) and dimethylallyl diphosphate In plants carotenoids fulfill two essential functions during pho- (DMAPP) and occurs de novo within plastids [28,29]. IPP and DMAPP tosynthesis, i.e. light harvesting and protecting the photosynthetic are derived predominantly from the plastidial methylerythritol 4- apparatus from photo-oxidation [3]. They are also the precursors of phosphate (MEP) pathway [30–32] although the same precursors signaling molecules that influence development and biotic/abiotic are formed by the cytosolic mevalonic acid (MVA) pathway, and stress responses, thereby facilitating photomorphogenesis, non- there is some evidence for the shuttling of intermediates [33,34]. photochemical quenching and lipid peroxidation, and attracting The condensation of three IPP molecules with one molecule of pollinators [4–9]. Four carotenoids (-carotene, ␣-carotene, ␥- DMAPP produces the C20 intermediate geranylgeranyl diphosphate carotene and -cryptoxanthin) have vitamin A activity in humans, (GGPP), a reaction catalyzed by GGPP synthase (GGPPS), which is which means they can be converted into the visual pigment retinal encoded by the crtE gene (Fig. 1). and are classed as essential nutrients. The first committed step in plant carotenoid synthesis is the -Carotene (pro-vitamin A) is a precursor of vitamin A in the condensation of two GGPP molecules into 15-cis-phytoene by the human body. It is present in a wide variety of yellow-orange col- enzyme phytoene synthase (PSY), which is encoded by the crtB ored fruits and dark green and yellow vegetables such as broccoli, gene in bacteria [35]. A series of four desaturation reactions carried spinach, turnip greens, carrots, squash, sweet potatoes, and pump- out in plants by phytoene desaturase (PDS) and -carotene desat- kin [10]. Liver, milk, butter, cheese, and whole eggs are direct urase (ZDS) then generates the carotenoid chromophore (Fig. 1). sources of vitamin A. Vitamin A plays an important role in the The product of the first desaturation is 9,15,9-tri-cis--carotene, human body for normal growth and tissue repair. The visual and which is isomerized by light (and perhaps an unknown enzyme immune systems are particularly dependent on this vitamin for [36]) to yield 9,9-di-cis--carotene, the substrate of ZDS [37]. The normal function [11]. end product of the desaturation reactions is converted to all-trans Lycopene is the red pigment in many fruits and vegetables such lycopene by a carotenoid isomerase (CRTISO) in non-green tissue, as tomato, watermelon, pink grapefruit and guava [12] and it does and by light