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Cloning and nucleotide sequence of a cDNA encoding a major fucoxanthin-, chlorophylla/c-containing protein from the chrysophyteIsochrysis galbana: implications for evolution of thecab gene family

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Abstract

We investigated the primary structure of a cDNA encoding a light-harvesting protein from the marine chrysophyteIsochrysis galbana. Antibodies raised against the major fucoxanthin, chlorophylla/c-binding light-harvesting protein (FCP) ofI. galbana were used to select a cDNA clone encoding one of the FCP apoproteins. The nucleic acid and deduced amino acid sequences reveal conserved regions within the first and third transmembrane spans with Chla/b-binding proteins and with FCPs of another chromophyte. However, the amino acid identity betweenI. galbana FCP and othercab genes of FCPs is only ca. 30%. Phylogenetic analyses demonstrated that the FCP genes of both diatoms and chrysophytes sequenced to date are more closely related tocab genes encoding LHC I, CP 29, and CP 24 of higher plants than tocab genes encoding LHC II of chlorophytes. We propose that LHC I, CP 24 and CP 29 and FCP might have originated from a common ancestral chl binding protein and that the major LHC II of Chla/b-containing organisms arose after the divergence between the chromophytes and the chlorophytes.

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References

  1. Auchincloss AH, Alexander A, Kohorn BD: Requirement for three membrane-spanning alpha helices in the post translational insertion of a thylakoid membrane protein. J Biol Chem 267: 10439–10446 (1992).

    Google Scholar 

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

    Google Scholar 

  3. Bhaya D, Grossman AR. Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatomPhaeodactylum tricornutum. Nucl Acids Res 2: 4458–4466 (1993).

    Google Scholar 

  4. Boczar BA, Prezelin BB: Light- and MgCl2-dependent characteristics of four chlorophyll-protein complexes iso lated from the marine dinoflagellate,Glenodinium sp. Biochim Biophys Acta 850: 300–309 (1986).

    Google Scholar 

  5. Chou P, Fasman GD: Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol 47: 45–147 (1978).

    Google Scholar 

  6. Demmin DS, Stockinger EJ, Chang YC, Walling LL: Phylogenetic relationship between the Chlorophylla/b binding protein (CAB) multigene family: an intra- and interspecies study. J Mol Evol 29: 266–279 (1989).

    Google Scholar 

  7. Di Paolo ML, Dal Balin Peruffo A, Bassi R. Immunological studies on chlorophyll-a/b proteins and their distribution in thylakoid membrane domains. Planta 181: 275–286 (1990).

    Google Scholar 

  8. Falkowski PG, Owens TG: Light shade adaptations; two strategies in marine phytoplankton. Plant Physiol 66: 592–595 (1980).

    Google Scholar 

  9. Fawley MW, Grossman AR: Polypeptides of a light-harvesting complex of the diatomPhaeodactylum tricornutum are synthesized in the cytoplasm of the cell as precursors. Plant Physiol 81: 149–155 (1986).

    Google Scholar 

  10. Felsenstein J: Confidence limits on phytogenies: an approach using the bootstrap. Evolution 39: 783–791 (1985).

    Google Scholar 

  11. Friedman AL, Alberte RS. A diatom light-harvesting pigment protein complex. Purification and characterization. Plant Physiol 76: 483–489 (1984).

    Google Scholar 

  12. Gibbs SP. The route of entry of cytoplasmically synthesized proteins into chloroplasts of algae possessing chloroplast ER. J Cell Sci 35: 253–266 (1979).

    Google Scholar 

  13. Granick S. Speculations on the origins of evolution of photosynthesis. Ann NY Acad Sci 69: 292–308 (1957).

    Google Scholar 

  14. Grant DM, Gillham NW, Boynton JE. Inheritance of chloroplast DNA inChlamydomonas reinhardtii. Proc Natl Acad Sci USA 77: 6067–6071 (1980).

    Google Scholar 

  15. Gribskov M, McLachlan AD, Eisenberg D: Profile analysis: detection of distantly related proteins. Proc Natl Acad Sci USA 84: 4355–4358 (1987).

    Google Scholar 

  16. Grimm B, Kruse E, Kloppstech K: Transiently expressed early light-inducible thylakoid proteins share transmembrane domains with light-harvesting chlorophyll binding proteins. Plant Mol Biol 13: 583–593 (1989).

    Google Scholar 

  17. Grossman A, Manodori A, Snyder D: Light-harvesting proteins of diatoms: their relationship to the chlorophyll a/b binding proteins of higher plants and their mode of transport into plastids. Mol Gen Genet 224: 91–100 (1990).

    Google Scholar 

  18. Henry D: Characterization of the light-harvesting complex and isolation of a cDNA clone of the marine chrysophyteIsochrysis galbana. MSc. Thesis, Marine Sciences Research Center, State University of New York at Stony Brook (1990).

  19. Higgins DG, Sharp PM: Fast and sensitive multiple alignments on a microcomputer CABIOS 5: 151–153 (1989).

    Google Scholar 

  20. Hiller RG, Anderson JM, Larkum AWD: The chlorophyll-protein complexes of algae. In: Scheer H (ed) Chlorophylls, pp. 530–543. CRC Press, Boca Raton, FL (1991).

    Google Scholar 

  21. Hiller RG, Bardin A-M, Nabedryk E: The secondary structure content of pigment-protein complexes from the thylakoids of two chromophyte algae. Biochim Biophys Acta 894: 365–369 (1987).

    Google Scholar 

  22. Hoffman NE, Pichersky E, Malik VS, Castresana C, Ko K, Darr SC, Cashmore AR: A cDNA clone encoding a photosystem I protein with homology to photosystem II chlorophylla/b-binding polypeptides. Proc Natl Acad Sci USA 84: 8844–8848 (1987).

    Google Scholar 

  23. Hsu B-D, Lee J-Y: Orientation of pigments and pigment-protein complexes in the diatomCylindrotheca fusiformis. A linear-dichroism study. Biochim Biophys Acta 893: 572–577 (1987).

    Google Scholar 

  24. Imbault P, Wittemer C, Johanningmeier U, Jacobs JD, Howell SH: Structure of theChlamydomonas reinhardtii cabII-I gene encoding a chlorophyll-a/b-binding protein. Gene 73: 397–407 (1988).

    Google Scholar 

  25. Kishore R, Muchhal US, Schwartzbach SD: The presequence ofEuglena LHCP II, a cytoplasmically synthesized chloroplast protein, contains a functional endoplasmic reticulum-targeting domain. Proc Natl Acad Sci USA 90: 11845–11849 (1993).

    Google Scholar 

  26. Klessig DF, Berry JO: Improved filter hybridization method for detection of single copy sequences in large eucaryotic genomes. Plant Mol Biol Rep 1: 12–18 (1983).

    Google Scholar 

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

    Google Scholar 

  28. Larkum AWD: 1991. The evolution of chlorophylls. In: Scheer H (ed) Chlorophylls, pp. 368–380. CRC Press, Boca Raton, FL (1991).

    Google Scholar 

  29. LaRoche J, Bennett J, Falkowski PG: Characterization of a cDNA encoding for the 28.5-kDa LHCII apoprotein from the unicellular marine chlorophyte,Dunaliella tertiolecta. Gene 95: 165–171 (1990).

    Google Scholar 

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

    Google Scholar 

  31. Larouche L, Tremblay C, Simard C, Bellemare G: Characterization of a cDNA encoding a PSII-associated chlorophylla/b-binding protein (CAB) fromChlamydomonas mowuesii fitting into neither type I or type II. Curr Genet 19: 285–288 (1991).

    Google Scholar 

  32. Lers A, Levy H, Zamir A: Co-regulation of a gene homologous to early light-induced genes in higher plants and β-carotene biosynthesis in the algaDunaliella bardawil. J Biol Chem 266: 13698–13705 (1991).

    Google Scholar 

  33. Livne A, Nelson EY, Sukenik A: Immunological cross reactivity among photosynthetic proteins from various marine unicellular algal species. Bot Marina 35: 181–187 (1992).

    Google Scholar 

  34. Lockhart PJ, Beanland TJ, Howe CJ, Larkum WD: Sequence ofProchloron didemni atpE and the inference of chloroplast origins. Proc Natl Acad Sci USA 89: 2742–2746 (1992).

    Google Scholar 

  35. Long Z, Wang S-Y, Nelson N: Cloning and nucleotide sequence analysis of genes coding for the major chlorophyll-binding protein of the mossPhyscomitrella patens and the halotolerant algaDunaliella salina. Gene 76: 299–312 (1989).

    Google Scholar 

  36. Luan S, Bogorad L: Nucleotide sequences of two genes encoding the light harvesting chlorophyll a/b binding protein of rice. Nucl Acids Res 17: 2357 (1989).

    Google Scholar 

  37. Maitsudaira P: Limited N-terminal sequence analysis. Methods in Enzymology 182: 602–613 (1990).

    Google Scholar 

  38. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  39. Morden CW, Golden SS: psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–284 (1989).

    Google Scholar 

  40. Morishige DT, Thornber JP: Identification and analysis of a barley cDNA clone encoding the 31 kilodalton LHC IIa (CP29) apoprotein of the light harvesting antenna complex of photosystem II. Plant Physiol 98: 238–245 (1992).

    Google Scholar 

  41. Muchhal US, Schwartzbach SD: Characterization of aEuglena gene encoding a polyprotein precursor to the light-harvesting chlorophylla/b-binding protein of photosystem II. Plant Mol Biol 18: 287–299 (1992).

    Google Scholar 

  42. Nelson JR, Wakeham SG: A phytol-substituted chlorophyllc fromEmiliania huxleyi (Prymnesiophyceae). J Phycol 25: 761–766 (1989).

    Google Scholar 

  43. Olson JM, Pierson BK: Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol 108: 209–248 (1987).

    Google Scholar 

  44. Owens TG: Light-harvesting function in the diatomPhaeodactylum tricornutum. Plant Physiol 80: 739–746 (1986).

    Google Scholar 

  45. Owens TG, Wold ER: Light harvesting function in the diatomPhaeodactylum tricornutum. Plant Physiol 80: 732–738 (1986).

    Google Scholar 

  46. Palenik B, Hazelkorn R: Multiple evolutionary origins of prochlorophytes, the chlorophyllb-containing prokaryotes. Nature 355: 265–267 (1992).

    Google Scholar 

  47. Pichersky E, Subramaniam R, White MJ, Reid J, Aebersold R, Green BR. Chlorophylla/b binding (CAB) polypeptides of CP29, the internal chlorophylla/b 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 (1991).

    Google Scholar 

  48. Pichersky E, Bernartzky R, Tanskley SD, Breidenbach RB, Kausch AP, Cashmore A. Molecular characterization and genetic mapping of two clusters of genes encoding chlorophylla/b-binding proteins inLycopersicon esculentum tomato). Gene 40: 247–258 (1985).

    Google Scholar 

  49. Saitou N, Nei M: The neighbour joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425 (1987).

    Google Scholar 

  50. Sanger F, Nicklens S, Coulson AR: DNA sequencing with chain-termination inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    Google Scholar 

  51. Schwartz E, Pichersky E: Sequence of two tomato nuclear genes encoding chlorophyll a/b-binding proteins of CP24, a PSII antenna component. Plant Mol Biol 15: 157–160 (1990).

    Google Scholar 

  52. Schwartz E, Shen D, Aeboersold R, McGrath JM, Pichersky E, Green BR: 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 (1991).

    Google Scholar 

  53. Sidler W, Frank G, Wehrmeyer W, Zuber H: Structural studies on chlorophylla/c light harvesting complex from the cryptomonadCryptomonas maculata: partial amino acid sequences. Experientia 44: A60 (1988).

    Google Scholar 

  54. Sukenik A, Bennett J, Falkowski PG: Changes in the abundance of individual apoproteins of light harvesting chlorophylla/b protein complexes of PSII with growth irradiance in the marine chlorophyteD. tertiolecta. Biochim Biophys Acta 932: 206–215 (1988).

    Google Scholar 

  55. Sukenik A, Wyman K, Bennett J, Falkowski P: A novel mechanism for regulating the excitation of photosystem II in a green algae. Nature 327: 704–707 (1987).

    Google Scholar 

  56. Thompson WF, Everett M, Polans NO, Jorgensen RA: Phytochrome control of RNA levels in developing pea and mung-bean leaves. Planta 158: 487–500 (1983).

    Google Scholar 

  57. Thornber JP, Morishige DT, Anandan S, Peters GF: Chlorophyll-carotenoid proteins of higher plant thylakoids. In: Scheer H (ed) Chlorophylls, pp. 549–586. CRC Press, boca Raton, FL (1991).

    Google Scholar 

  58. Urbach E, Robertson DL, Chisholm SW: Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355: 267–270 (1992).

    Google Scholar 

  59. Wilhelm C: Purification and identification of chlorophyllc 1 from the green algaMantoniella squamata. Biochim Biophys Acta 892: 23–29 (1987).

    Google Scholar 

  60. Young RA, Davis RW: Efficient isolation of genes using antibody probes. Proc Natl Acad Sci USA 80 1194–1198 (1983).

    Google Scholar 

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LaRoche, J., Henry, D., Wyman, K. et al. Cloning and nucleotide sequence of a cDNA encoding a major fucoxanthin-, chlorophylla/c-containing protein from the chrysophyteIsochrysis galbana: implications for evolution of thecab gene family. Plant Mol Biol 25, 355–368 (1994). https://doi.org/10.1007/BF00043865

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