Abstract
ALaminaria saccharina genomic library in the phage EMBL 4 was used to isolate and sequence a full-length gene encoding a fucoxanthin-chlorophyll a/c-binding protein. Contrary to diatom homologues, the coding sequence is interrupted by an intron of about 900 bp which is located in the middle of the transit peptide. The deduced amino acid sequence of the mature protein is very similar to those of related proteins fromMacrocystis pyrifera (Laminariales) and, to a lesser extent, to those from diatoms and Chrysophyceae. Seven of the eight putative chlorophyll-binding amino acids determined in green plants are also present.
Alignments of different sequences related to the light-harvesting proteins (LHC) demonstrate a structural similarity among the three transmembrane helices and suggest a unique ancestral helix preceded by two β-turns. The β-turns are conserved in front of the second helices of the chlorophyll a/c proteins more so than in chlorophyll a/b proteins.
Phylogenetic trees generated from sequence data indicate that fucoxanthin-chlorophyll-binding proteins diverged prior to the separation of photosystem I and photosystem II LHC genes of green plants. Among the fucoxanthin-containing algae, LHC I or II families could not be distinguished at this time.
Similar content being viewed by others
References
Adamska I (1995) Light stress proteins (ELIPs); the intriguing relatives of CAB gene family. Xth international photosynthesis congress. Photosynthesis: From light to biosphere. In: Mathis P, ed. Kluwer Ac. Pr., Dordrecht, III, pp. 887–892
Anderson JM (1980) P-700 content and polypeptide profile of chlorophyll-protein complexes of spinach and barley thylakoids. Biochim Biophys Acta 591:113–126
Apt KE, Bhaya D, Grossman AR (1994) Characterization of genes encoding the light-harvesting proteins in diatoms: biogenesis of the fucoxanthin chlorophyll a/c protein complex. J Appl Phycol 6:225–230
Apt KE, Clendennen SK, Powers DE, Grossman AR (1995) The gene family encoding the fucoxanthin chlorophyll proteins from the brown algalMacrocystis pyrifera. Mol Gen Genet 246:455–464
Bassi R, Pineau B, Dainese P, Marquardt J (1993) Carotenoid-binding proteins of photosystem II. Eur J Biochem 212:297–303
Benet H, Bruss U, Duval J-C, Kloareg B (1994) Photosynthesis and photoinhibition in protoplast of the marine brown algaLaminaria saccharina. J Exp Bot 45:211–220
Berkaloff C, Caron L, Rousseau B (1990) Subunit organization of PSI particles from brown algae and diatoms: polypeptide and pigment analysis. Photosynth Res 23:181–193
Bhaya D, Grossman AR (1991) Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol Gen Genet 229:400–404
Bhaya D, Grossman AR (1993) Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatomPhaeodactylum tricomutum. Nucleic Acids Res 21:4458–4446
Caron L, Dubacq JP, Berkaloff C, Jupin H (1985) Subchloroplast fractopms from the brown algaFucus serratus: phosphatidylglycerol contents. Plant Cell Physiol 26:131–139
Dolganov NAM, Bhaya D, Grossman AR (1995) Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc Natl Acad Sci USA 92:636–640
Donath M, Mendel R, Cerff R, Martin W (1995) Intron-dependent transient expression of a maize GapAl gene. Plant Mol Biol 28: 667–676
Douady D, Rousseau B, Berkaloff C (1993) Isolation and characterization of PSII core complexes from a brown alga,Laminaria saccharina. FEBS Lett 324:22–26
Douady D, Rousseau B, Caron L (1994) Fucoxanthin chlorophyll a/c light-harvesting complexes ofLaminaria saccharina: partial amino acid sequences and arrangement in thylakoid membranes. Biochemistry 33:3165–3170
Durnford DG (1995) An analysis of the fucoxanthin-chlorophyll protein and the genes encoding them in the unicellular marine raphidophyte,Heterosigma carterae: characterization and evolution. Thesis, University of British Columbia, Vancouver, Canada
Durnford DG, Green BR (1994) Characterization of the light harvesting proteins of the chromophytic alga,Olisthodiscus luteus (Heterosigma carterae). Biochim Biophys Acta 1184:118–123
Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783–791
Flachmann R, Kühlbrandt W (1995) Accumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobacco. Plant Cell 7:149–16
Friedman AA, Alberte RS (1986) Biogenesis and light regulation of the major light harvesting chlorophyll-protein of diatoms. Plant Physiol 80:43–51
Funk C, Schroder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B (1995) The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry 34:11133–11141
Gajadhar A, Marquardt W, Hall R, Gunderson J, Aritzia-Carmona E, Sogin M (1991) Ribosomal RNA sequences ofSarcocystis muris, Theileria annulata andCrypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates and ciliates. Mol Biol Parasitol 45:147–154
Gibbs SJ (1979) The route of entry of cytoplasmically synthetized proteins into chloroplasts of algae possessing chloroplast ER. Cell Sci 35:253–266
Green BR, Kühlbrandt W (1995) Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Phorosynth Res 44:139–148
Grossman A, Manodori A, Snyder D (1990) Light-harvesting proteins of diatoms: their relationship to the chlorophyll a/b binding proteins of higher plants and their mode of transport into plasmids. Mol Gen Genet 224:91–100
Henze K, Badr A, Wettern M, Cerff R, Martin W (1995) A nuclear gene of eubacterial origin in Euglena gracilis reflects crytic endosymbioses during protist evolution. Proc Natl Acad Sci USA 92: 9122–9127
Hiller RG, Wrench PM, Sharples FPS (1995) The light-harvesting chlorophyll a-c-binding protein of dinoflagellates: a putative polyprotein. FEBS Lett 363:175–178
Hobe S, Föster R, Klingler J, Paulsen H (1995) N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34:10224–10228
Hoffman NE, Pichersky E, Malik VP, Castresana C, Ko K, Darr SC, Cashmere AR (1987) A cDNA clone encoding a photosystem I protein with homology to photosystem II chlorophyll a/b-binding polypeptides. Proc Natl Acad Sci USA 84:844–848
Janssen S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184:1–19
Katoh T, Mimuro M, Takaichi S (1989) Light-harvesting particles isolated from a brown alga,Dictyota dichotoma. A supramolecular assembly of fucoxanthin-chlorophyll-protein complexes. Biochim Biophys Acta 976:233–240
Kim S, Sandussky P, Bowlby NR, Aebersold R, Green BR, Vlahakis S, Yocum CF, Pichersky E (1992) Characterization of a spinach pbsS cDNA encoding the 22 kDa protein of photosystem II. FEBS Lett 314:67–71
Kolanus W, Scharnhorst C, Huhne U, Herzfeld F (1987) The structure and light-dependent transient expression of a nuclear-encoded a chloroplast protein gene from pea (Pisum sativum L.). Mol Gen Genet 204:234–239
Kroth-Pancic PG (1995) Nucleotide sequence of two cDNA encoding fucoxanthin chlorophyll a/c proteins in the diatomOdontella sinensis. Plant Mol Biol 27:825–828
Kühlbrandt W, DN Wang, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621
LaRoche J, Henry D, Wyman K, Sukenik A, Falkowski P (1994) Cloning and nucleotide sequence of a cDNA encoding a major fucoxanthin-chlorophyll a/c-containing protein from the chrysophyteIsochrysis galbana: implication for evolution of thecab gene family. Plant Mol Biol 25:355–368
Lemoine Y, Harker M, Rmiki NE, Rousseau B, Berkaloff C, Duval JC, Young AJ, Britton G (1995) Xanthophyll cycle operation and photo-protection in brown algae: effects of high light and dissication. Proceedings of the Xth International Congress on Photosynthesis. In: Mathis P, ed. Photosynthesis: from light to biosphere. Kluwer Ac. Pr. Dorolrecht, IV, 119–122
Liaud M-F, Valentin C, Brandt U, Bouget F-Y, Kloareg B, Cerff R (1993) The GAPDH gene system of the algaChondrus crispus: structures, intron organization, genomic complexity and differential expression of genes. Plant Mol Biol 23:981–994
Martin W, Somerville CC, Loiseaux-de Goër S (1992) Molecular phylogenies of plastid origins and algal evolution. J Mol Evol 35:385–404
Mimuro M, Katoh T (1991) Carotenoids in photosynthesis: absorption transfer and dissipation of light energy. Pure Appl Chem 63:123–130
Muchhal US, Schwartzbach SD (1992) Characterization of aEuglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll a/b-binding of photosystem II. Plant Mol Biol 18:287–299
Nußberger S, Dörr, DN Wang, Kühlbrandt W (1993) Lipid-protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234:347–356
Owens TG, Wold ER (1986) Light-harvesting function in the diatomPhaeodactylum tricornutum. I. Isolation and characterization of pigment-protein complexes. Plant Physiol 80:732–738
Passaquet C, Lichtlé C (1995) Molecular study of a light-harvesting apoprotein ofGiraudyopsis stellifer (Chrysophyceae). Plant Mol Biol 29:135–148
Passaquet C, Thomas JC, Caron L, Hauswirth N, Puel F, Berkaloff C (1991) Light-harvesting complexes of brown algae. Biochemical characterization and immunological relationships. FEBS Lett 280: 21–26
Peter GF, Thornber JP (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem 266:16745–16754
Pichersky E, Bernartzky R, Tanskley SD, Breidenbach RB, Kausch AP, Cashmore A (1985) Molecular characterization and genetic mapping of two clusters of genes encoding chlorophyll a/b-binding proteins inLycopersicon esculentum (tomato). Gene 40:247–258
Pichersky E, Hoffman NE, Bernatzky R, Piechulla B, Tanksley SD, Cashmore AR (1987) Molecular characterization and genetic mapping of DNA sequences encoding the type I chlorophyll a/b-binding polypeptide of photosystem I inLycopersicon esculentum (tomato). Plant Mol Biol 9:205–216
Pichersky E, Tanksley SD, Piechulla B, Stayton MM, Dunsmuir P (1988) Nucleotide sequence and chromosomal location ofCab-7, the tomato gene encoding the type II chlorophyll a/b-binding polypeptide of photosystem I. Plant Mol Biol 11:69–71
Pichersky E, Brock TG, Nguyen D, Hoffman NE, Piechulla B, Tanksley SD, Green BR (1989) A new member of the CAB gene family: structure, expression and chromosomal location ofCab-8, the tomato gene encoding the type III chlorophyll a/b-binding polypeptide of photosystem I. Plant Mol Biol 12:257–270
Pichersky E, Subramaniam R, White MJ, Reid J, Aebersold R, Green BR (1991) Chlorophyll a/b binding (CAB) polypeptides of CP29, the internal chlorophyll alb complex of PSII: characterization of the tomato gene encoding the 26 kDa (type 1) polypeptides, and evidence for a second CP29 polypeptide. Mol Gen Genet 227:277–284
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, NY
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schmitt A, Frank G, James P, Staudenmann W, Zuber H, Wilhelm C (1994) Polypeptide sequence of the chlorophyll a/b/c-binding protein of the prasinophycean algaMantoniella squamata. Photosynth Res 40:269–277
Schwartz E, Pichersky E (1990) Sequence of two tomato nuclear genes encoding chlorophyll a/b-binding proteins CP24, a PSII antenna component. Plant Mol Biol 15:157–160
Schwartz E, Shen D, Aebersold R, Mc Grath SM, Pichersky E, Green R (1991a) Nucleotide sequence and chromosomal location ofCab11 andCab12, the genes for the fourth polypeptide of the photosystem I light-harvesting antenna (LHCI). FEBS Lett 280: 229–234
Schwartz E, Stasyp R, Aebersold R, Mc Grath S, Green R, Pichersky E (1991b) Sequence of a tomato gene encoding a third type of LHCII chlorophyll a/b-binding polypeptide. Plant Mol Biol 17:923–925
Shapiro MB, Senapathy P (1987) RNA Splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 15:7155–7174
Thompson WF, White MJ (1991) Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42:423–466
Tremolières A, Dainese P, Bassi R (1994) Heterogenous lipid distribution among chlorophyll-binding proteins of photosystem II in maize mesophyll chloroplasts. J Biochem 227:721–730
Wedel N, Klein R, Ljungberg U, Andersson B, Herrmann RG (1992) The single-copy gene psbS codes for a phylogenetically intriguing 22 kDa polypeptide of photosystem II. FEBS Lett 314:61–66
Author information
Authors and Affiliations
Additional information
Correspondence to: L. Caron
Rights and permissions
About this article
Cite this article
Caron, L., Douady, D., Quinet-Szely, M. et al. Gene structure of a chlorophyll a/c-binding protein from a brown alga: Presence of an intron and phylogenetic implications. J Mol Evol 43, 270–280 (1996). https://doi.org/10.1007/BF02338835
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02338835