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Genetics of Carotenoid Pigment Biosynthesis from Microbes to Plants GREGORY A

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Genetics of Carotenoid Pigment Biosynthesis from Microbes to Plants GREGORY A JOURNAL OF BACTERIOLOGY, Aug. 1994, p. 4795-4802 Vol. 176, No. 16 0021-9193/94/$04.00+0 Copyright © 1994, American Society for Microbiology MINIREVIEW Eubacteria Show Their True Colors: Genetics of Carotenoid Pigment Biosynthesis from Microbes to Plants GREGORY A. ARMSTRONG* Department of Plant Genetics, Institute for Plant Sciences, Swiss Federal Institute of Technology (ETH), CH-8092 Zurich, Switzerland INTRODUCTION among nonphotosynthetic bacteria and fungi (21, 40). During photosynthesis, carotenoids also absorb light and transfer the Carotenoids compose a widely distributed class of structur- energy to Bchl and Chl, dissipate excess radiant energy, and ally and functionally diverse yellow, orange, and red natural preserve the structural integrity of pigment-protein complexes pigments. Prokaryotes and eukaryotes synthesize an estimated (22, 56). In mammals, the cleavage products of several dietary 108 tons of carotenoids yearly (54), composed of at least 600 carotenoids, particularly ,-carotene, fulfill essential roles in structurally distinct compounds (90). These pigments typically nutrition (vitamin A), vision (retinal), and development (reti- consist of a C40 hydrocarbon backbone in the case of car- noic acid) (21, 35). Metabolism of certain cyclic epoxy-xantho- otenes, often modified by various oxygen-containing functional phylls in higher plants yields abscisic acid, an important groups to produce cyclic or acylic xanthophylls (21, 40). The hormone (81). In addition, carotenoids and their derivatives degree of conjugation and the isomerization state of the provide pigmentation to many birds, fish, and crustaceans (21). backbone polyene chromophore determine the absorption properties of each carotenoid. Compounds with at least seven conjugated double bonds, such as (-carotene, absorb visible light. Some carotenoids occur naturally not only as all trans GENETICS OF CAROTENOID BIOSYNTHESIS isomers but also as cis isomers (17, 40). IN EUBACTERIA Carotenoids are derived from the general isoprenoid biosyn- thetic pathway, along with a variety of other important natural substances (see Fig. 1) (16, 20, 71, 72, 83, 89). The conversion Studies performed with a few species of purple nonsulfur of two molecules of geranylgeranyl pyrophosphate (GGPP) to anoxygenic photosynthetic bacteria (Rhodobacter capsulatus phytoene, a compound common to all C40 carotenogenic and Rhodobacter sphaeroides), nonphotosynthetic bacteria (Er- organisms, constitutes the first reaction unique to the carote- winia herbicola, Erwinia uredovora, and Myxococcus xanthus), noid branch of isoprenoid metabolism (21, 40). Anoxygenic and cyanobacteria (Synechococcus sp. strain PCC7942, Syn- photosynthetic bacteria, nonphotosynthetic bacteria, and fungi echocystis sp. strain PCC6803, Anabaena sp. strain PCC7120) desaturate phytoene either three or four times to yield neuro- have contributed enormously to our molecular-genetic under- sporene or lycopene, respectively (see Fig. 2). In contrast, standing of carotenoid biosynthesis. To illustrate the rapid oxygenic photosynthetic organisms (cyanobacteria, algae, and advances in this field, nucleotide sequences of carotenoid higher plants) convert phytoene to lycopene via (-carotene in biosynthesis genes were first reported in R. capsulatus in 1989 two distinct sets of reactions (15, 17, 48). At the level of (4, 12), E. herbicola and E. uredovora in 1990 (3, 67), Synecho- neurosporene or lycopene, the carotenoid biosynthesis path- coccus sp. strain PCC7942 in 1991 (26), and M. xanthus in 1993 ways of different organisms branch to generate the tremendous (33). The biosynthetic pathways used by these organisms, diversity of carotenoids found in nature. major carotenoid pigments accumulated, and assignments of In photosynthetic organisms and tissues, the lipophilic ca- gene and gene product functions are summarized here (Fig. 1 rotenoid and bacteriochlorophyll (Bchl) or chlorophyll (Chl) and 2 and Table 1) and are discussed in further detail pigment molecules associate noncovalently but specifically elsewhere (2, 43, 46). To complement earlier surveys of with integral membrane proteins (22, 56). In nonphotosyn- biochemical and classical genetic experiments (20, 40), this thetic organisms and tissues, carotenoids, often protein bound, minireview will focus on developments within the last five years occur in cytoplasmic or cell wall membranes, oil droplets, from a molecular-genetic standpoint. crystals, and fibrils (21, 31, 40). Carotenoids provide crucial The crt nomenclature (Table 1) proposed in 1976 for the R. protection against photooxidative damage resulting from the capsulatus genetic loci required for carotenoid biosynthesis combination of visible or near-UV light, singlet oxygen, and (93) has been maintained in subsequent studies with Rho- endogenous lipophilic photosensitizers, such as Bchl, Chl, dobacter species, Erwinia species, and Thermus thermophilus. heme, and protoporphyrin IX (22, 41, 92). This protective Genetic loci involved in carotenoid biosynthesis in M. xanthus function explains the ubiquitous synthesis of carotenoids in have been designated car in a parallel nomenclature from 1987 photosynthetic organisms and their widespread distribution (10). In cyanobacteria, a proposal to replace the current nomenclature that originated in 1991 with the crt nomencla- ture has been made The new * Mailing address: Department of Plant Genetics, Institute for Plant recently (43). proposed gene Sciences, Swiss Federal Institute of Technology (ETH), CH-8092 designations (Table 1) will be employed throughout this mini- Zurich, Switzerland. Phone: (01) 632 3700. Fax: (01) 252 0829. review to reflect the similarities and differences between Electronic mail address: [email protected]. cyanobacteria and other eubacteria. 4795 4796 MINIREVIEW J. BAC-rERIOL. 1). The corresponding enzymes convert farnesyl pyrophos- IPP phate (FPP) to spheroidene in strictly anoxygenic cultures or to spheroidenone in the presence of oxygen (Fig. 1 and 2). Taking advantage of a genetic recombination system in R. capsulatus, mapping of distinct classes of photopigment mu- Cytoldnin-tRNA tants demonstrated the tight genetic linkage of crt and Bchl a 0 - -- Prk ale - Cytokinins (bch) biosynthetic loci (88, 93). Analysis by conjugation- DMAPP mediated marker rescue and transposon and interposon mu- IPP tagenesis of a cloned 46-kb photosynthesis gene supercluster produced an integrated genetic-physical map of the clustered crtA, crtB, crtC, crtD, crtE, crtF, and crtI genes and the s 2015) ----* Monoterpenes physically separated crtJ gene (7, 38, 39, 60, 91, 95). Nucleotide (G 'PP I sequencing of the R capsulatus crt gene cluster (4) (Fig. 3) Baceriochlorophyll c d, e g I3P _-I Dohchof revealed the presence of an additional open reading frame Ubiquinone (ORF) that was designated crtK on the basis of an earlier Monaquinone mutational analysis (39). R sphaeroides was also shown to Hmanond. contain a similarly organized crt gene cluster (29, 36, 74), which A4.1Af AH20o ----* Sterols has been partially characterized molecularly (37, 53). In con- FPP Sesquiterpenes trast to earlier indications, recent mutational analyses demon- Famesylated proteins strate that neither crtJ (18) (now termed ORF 469) nor crtK (53) (now termed ORF 160) participate directly in Baoteriochlorophyll a, b Rhodobacter carotenoid biosynthesis. ORF 469, which may be Chlorophylls Dolichols involved in suppressing Bchl and carotenoid levels (76), en- Plastoquinone codes a product with some sequence features found in known I [HM__. Ubiquinone bacterial transcription factors (1, 2). (UIurr Phylloquinone Inhibitor and mutant studies led to proposals for a Tocopherols Rhodobacter carotenoid biosynthetic pathway from phytoene Gibberellins GGPP crtB Diterpenes to the end products (Fig. 2) (38, 40, 88). Analysis of R Geranylgeranylated proteins capsulatus crtB and crtE mutants blocked in phytoene accumu- lation demonstrated that both mutations permitted the synthe- CHO0 ) _ sis of Bchl in vivo and accumulation of GGPP in vitro, indicating an active isoprenoid biosynthetic pathway through H CH3 the latter compound (Fig. 1) (7). Partly on the basis of these PPPP I data, functions were suggested for CrtB in prephytoene pyro- crtB phosphate synthesis and CrtE in phytoene synthesis. Subse- IF quent proposals that eubacterial CrtB and CrtE might instead be the phytoene and GGPP synthases, respectively (23, 57, 64), were confirmed by in vivo complementation studies with Phytoene Erwinia and Synechococcus crt genes in an Escherichia coli host (25, 64, 85) and with a tomato phytoene synthase cDNA in an FIG. 1. General isoprenoid biosynthetic pathway. Branches in the R capsulatus crtB mutant (14). Interestingly, all Rhodobacter pathway dependent on intermediates common to carotenoid biosyn- thesis are indicated on the right. The bold typeface highlights impor- crtE mutants, including those containing gross gene disrup- tant compounds found in some or all eubacteria, while substances tions, synthesize Bchl-containing pigment-protein complexes produced in eukaryotes appear in normal typeface. Abbreviations not (7, 39, 95). Thus, the effective branchpoint between Bchl a and given in the text are as follows: DMAPP, dimethylallyl pyrophosphate; carotenoid biosynthesis may occur even earlier than previously GPP, geranyl pyrophosphate; IPP, isopentenyl pyrophosphate, PPPP, thought (Fig. 1), and carotenoid- and Bchl a-specific pools of prephytoene pyrophosphate. PPPP is an unstable intermediate
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