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The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera

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Abstract

Six members of a multigene family encoding polypeptide constituents of the fucoxanthin, chlorophyll a/c protein complex from female gametophytes of the brown alga Macrocystis pyrifera have been cloned and characterized. The deduced amino acid sequences are very similar to those of fucoxanthin chlorophyll binding proteins (Fcp) from the diatom Phaeodactylum tricornutum and exhibit limited homology to chlorophyll a/b binding (Cab) polypeptides from higher plants. The primary translation products from the M. pyrifera fcp genes are synthesized as higher molecular weight precursors that are processed prior to their assembly into the Fcp complex. The presumed N-terminal 40-amino acid presequence of the Fcp precursor polypeptide has features resembling that of a signal sequence. This presequence may be required for the protein to transverse the endoplasmic reticulum that surrounds the plastid in brown algae. A subsequent targeting step would be required for the protein to cross the double membrane of the plastid envelope. M. pyrifera fcp transcripts are of two sizes, 1.2 and 1.6 kb. The size difference is accounted for by the length of the 3′ untranslated region, which can be up to 1000 bases. Transcript abundance's of members of the fcp gene family are dependent on light quantity, light quality, or both. Transcript levels of one gene increased approximately five- to tenfold in thalli grown in low intensity relative to high intensity white or blue light. Transcripts from this gene also significantly increase in red light relative to blue light at equivalent light intensities.

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References

  • Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166

    Google Scholar 

  • Anderson DJ, Blobel G (1983) Immunoprecipitation of proteins from cell-free translations. Methods Enzymol 96:111–120

    Google Scholar 

  • Apt KE, Hoffman NE, Grossman AR (1993) The γ subunit of R-phycoerythrin and its possible mode of transport into the plastid of red algae. J Biol Chem 268:16208–16215

    Google Scholar 

  • Apt KE, Bhaya D, Grossman AR (1994) Characterization of the genes encoding the light-harvesting proteins in diatoms: the biogenesis of the fucoxanthin chlorophyll a/c protein complex. J Appl Phycol 6:225–230

    Google Scholar 

  • Berkaloff C, Duval JC, Jupin H, Chrissovergis F, Caron L (1981) Spectroscopic studies of isolated pigment-protein complexes of some brown algae thylakoids. In: Akoyonoglou G (ed) Photosynthesis III. Balaban International Service, Philadelphia, pp 485–494

    Google Scholar 

  • Berkaloff C, Caron L, Rousseau B (1990) Subunit organization of PSI particles from brown algae and diatoms: polypeptide and pigment analysis. Photosyn Res 23:181–193

    Google Scholar 

  • Bhattacharya D, Medlin L, Wainright PO, Ariztia EV, Bibeau C, Stickel SK, Sogin ML (1992) Algae containing chlorophylls a+c are paraphyletic: Molecular evolutionary analysis of the Chromophyta. Evolution 46:1801–1817

    Google Scholar 

  • Bhaya D, Grossman AR (1991) Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol Gen Genet 229:400–404

    Google Scholar 

  • Bhaya D, Grossman AR (1993) Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatom Phaeodactylum tricornutum. Nucleic Acids Res 21:4458–4466

    Google Scholar 

  • Caron L, Remy R, Berkaloff C (1988) Polypeptide composition of light-harvesting complexes from some brown algae and diatoms. FEBS Lett 229:11–15

    Google Scholar 

  • Chitnis PR, Thornber JP (1988) The major light-harvesting complex of photosystem II: aspects of its molecular and cell biology. Photosyn Res 16:41–63

    Google Scholar 

  • De Boer AD, Weisbeek PJ (1991) Chloroplast protein topogenesis, import, sorting and assembly. Biochim Biophys Acta 1071:221–254

    Google Scholar 

  • Douady D, Rousseau B, Caron L (1994) Fucoxanthin-chlorophyll a/c light-harvesting complexes of Laminaria saccharina: Partial amino acid sequences and arrangement in thylakoid membranes. Biochemistry 33:1165–1170

    Google Scholar 

  • Dring MJ (1987) Marine plants and blue light. In: Senger H (ed) Blue light responses; phenomena and occurrence in plants and microorganisms, vol II. CRC Press, Boca Raton, pp 122–140

    Google Scholar 

  • Duval J, Jupin H, Berkaloff C (1983) Photosynthetic properties of plastids isolated from macrophytic brown seaweeds. Physiol Veg 21:1145–1157

    Google Scholar 

  • Fawley MW, Grossman AR (1986) Polypeptides of light-harvesting complexes of the diatom Phaeodactylum tricornutum are synthesized in the cytoplasm of the cell as precursors. Plant Physiol 81:149–155

    Google Scholar 

  • Fawley MW, Morton JS, Stewart KD, Mattox KR (1987) Evidence for a common evolutionary origin of light-harvesting fucoxanthin chlorophyll a/c protein complexes of Pavlova gyrans (Prymnesiophyceae) and Phaeodactylum tricornutum (Bacillariophyceae).J Phycol 23:377–381

    Google Scholar 

  • Friedman AL, Alberte RS (1987) Phylogenetic distribution of the major diatom light-harvesting pigment-protein determined by immunological methods. J Phycol 23:427–433

    Google Scholar 

  • Gibbs SP (1981) The chloroplast endoplasmic reticulum: structure, function and evolutionary significance. Int Rev Cytol 72:49–99

    Google Scholar 

  • Green BR, Pichersky E (1994) Hypothesis for the evolution of three-helix chl a/b and a/c light-harvesting antenna proteins from two-helix and four-helix ancestors. Photosyn Res 39:149–162

    Google Scholar 

  • Green BR, Pichersky E, Kloppstech K (1991) Chlorophyll a/b-binding proteins: an extended family. Trends Biochem Sci 16:181–186

    Google Scholar 

  • Grevby C, Sundquist C (1992) Characterization of light-harvesting complex in Ochromonas danica (Chrysophyceae). J Plant Physiol 140:414–420

    Google Scholar 

  • Grossman AR, 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. Mol Gen Genet 224:91–100

    Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–746

    Google Scholar 

  • Hiller G, Larkum AWD, Wrench P (1988) Chlorophyll proteins of the prymnesiophyte Pavlova lutherii (Droop) comb. nov.; identification of the major light-harvesting complex. Biochim Biophys Acta 932:223–231

    Google Scholar 

  • Hiller RG, Wrench PM, Gooley AP, Shoebridge G, Breton J (1993) The major intrinsic light-harvesting protein of Amphidinium: characterization and relation to other light-harvesting proteins. Photochem Photobiol 57:125–131

    Google Scholar 

  • Hoffman NE, Pichersky E, Malik VS, Castresana C, Ko K, Darr SC, Cashmore 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 84:8844–8848

    Google Scholar 

  • Jackson RJ, Standart N (1990) Do the poly(A) tail and 3′ untranslated region control mRNA translation? Cell 62:15–24

    Google Scholar 

  • Jenkins GI, Jackson JA, Shaw MJ, Urwin AR (1993) A genetic approach to understanding responses to uv-A/blue light. In: Holmes MG, Johnson CB (eds) Plant photoreceptors and photoperception. Cambridge University Press, Cambridge

    Google Scholar 

  • Katoh T, Ehara T (1990) Supramolecular assembly of fucoxanthin-chlorophyll-protein complexes isolated from the brown alga, Petalonia fascia: Electron microscopic studies. Plant Cell Physiol 31:439–448

    Google Scholar 

  • 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

    Google Scholar 

  • Kaufman LS (1993) Transduction of blue-light signals. Plant Physiol 102:333–337

    Google Scholar 

  • Keegstra K (1989) Transport and routing of proteins into chloroplasts. Cell 56:247–254

    Google Scholar 

  • Kindle KL (1987) Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii: effect of light and acetate. Plant Mol Biol 9:547–583

    Google Scholar 

  • Kühlbrandt WK, Wang DN (1991) Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature 350:130–134

    Google Scholar 

  • Kühlbrandt WK, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light harvesting complex by electron crystallography. Nature 367:614–621

    Google Scholar 

  • Laemmh UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • LaRoche J, Mortain-Bertrand A, Falkowski PG (1991) Light intensity-induced changes in cab mRNA and light harvesting complex II apoprotein levels in the unicellular chlorophyte Dunaliella tertiolecta. Plant Physiol 97:147–153

    Google Scholar 

  • Lüning K, Neushul M (1978) Light and temperature demands for growth and reproduction of laminarian gametophytes in Southern and Central California. Marine Biol 45:297–309

    Google Scholar 

  • Mackay RM (1991) Beta-tubulins are encoded by at least four genes in the brown alga Ectocarpus variabilis. Plant Mol Biol 17:487–492

    Google Scholar 

  • Magruder WH (1984) Specialized appendages from the red alga Aglaothamnion neglectum (Ceramiales, Ceramiaceae) specifically bind with trichogynes. J Phycol 20:436–440

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Manodori A, Grossman AR (1990) Light harvesting genes of Phaeodactylum tricornutum. In: Baltscheftsky M (ed) Current research in photosynthesis, vol III. Kluwer Academic Publishers, Boston, pp 541–544

    Google Scholar 

  • Marrs KA, Kaufman LS (1989) Blue-light regulation for nuclear genes in pea. Proc Natl Acad Sci USA 86:4492–4495

    Google Scholar 

  • Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499

    Google Scholar 

  • Melis A, Manodori A, Glick RE, Ghirardi ML, McCauley SW, Neale PJ (1985) The mechanisms of photosynthetic membrane adaptation to environmental stress conditions: a hypothesis on the role of electron-transport capacity and of the ATP/NADPH pool in the regulation of thylakoid membrane organization and function. Physiol Veg 23:757–765

    Google Scholar 

  • Mimuro M, Katoh T, Kawai H (1990) Spatial arrangement of pigments and their interaction in the fucoxanthin-chlorophyll a/c protein assembly (FCPA) isolated from Dictyota dichotoma: Analysis by means of polarized spectroscopy. Biochim Biophys Acta 1015:450–456

    Google Scholar 

  • Neushul M (1971) The species of Macrocystis with particular reference to those of North and South America. Nova Hedwigia 32:223–228

    Google Scholar 

  • 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

    Google Scholar 

  • Peyriere M, Caron L, Jupin J (1984) Pigment complexes and energy transfer in brown algae. Photosynthetica 18:184–191

    Google Scholar 

  • 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 in Lycopersicon esculentum (tomato) Gene 40:247–258

    Google Scholar 

  • Plumley FG, Martinson TA, Herrin DL, Ikeuchi M, Schmidt GW (1993) Structural relationships of the photosystem I and photosystem II chlorophyll a/b and a/c light-harvesting apoproteins of plants and algae. Photochem Photobiol 57:143–151

    Google Scholar 

  • Rosen KM, Lamporti ED, Villa-Komaroff L (1990) Optimizing the northern blot procedure. Biotechniques 8:398–403

    Google Scholar 

  • Schmidt GW, Mishkind (1986) The transport of proteins into chloroplasts. Annu Rev Biochem 55:879–912

    Google Scholar 

  • Senger H (1984) Blue light effects in biological systems. Springer-Verlag, Berlin

    Google Scholar 

  • Sukenik A et al (1992) Purification, characterization of a light-harvesting chlorophyll-protein complex from the marine eustigmatophyte Nannochloropsis sp. Plant Cell Physiol 33:1041–1048

    Google Scholar 

  • van de Peer Y, de Baere R, Cauwen Berghs J, de Wachter R (1990) Evolution of green plants and their relationship with other photosynthetic eukaryotes as deduced from 5S ribosomal RNA sequences. Plant Syst Evol 170:85–96

    Google Scholar 

  • Wolfe GR, Cunningham FX, Durnford D, Green BR, Gantt E (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367:566–568

    Google Scholar 

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Authors and Affiliations

  1. Department of Plant Biology, Carnegie Institution of Washington, 290 Panama St., 94305, Stanford, CA, USA

    Kirk E. Apt & Arthur R. Grossman

  2. Hopkins Marine Station, Stanford University, 93950, Pacific Grove, CA, USA

    Stephanie K. Clendennen & Dennis A. Powers

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  1. Kirk E. Apt
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  2. Stephanie K. Clendennen
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  3. Dennis A. Powers
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  4. Arthur R. Grossman
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Communicated by R. Herrmann

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Apt, K.E., Clendennen, S.K., Powers, D.A. et al. The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera . Molec. Gen. Genet. 246, 455–464 (1995). https://doi.org/10.1007/BF00290449

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