Advertisement

Current Genetics

, Volume 26, Issue 2, pp 159–165 | Cite as

Chloroplastic genomes of Ginkgo biloba and Chlamydomonas moewusii contain a chlB gene encoding one subunit of a light-independent protochlorophyllide reductase

  • Martine Richard
  • Colette Tremblay
  • Guy Bellemare
Original Articles

Abstract

We have cloned and sequenced a Chlamydomonas moewusii chloroplastic DNA fragment that includes a 563 amino-acid open reading frame (ORF563, chlB) presenting 89% amino-acid homology with ORF513 from Marchantia polymorpha. It is also homologous to ORF510 from Pinus thumbergii but includes two insertions absent in both M. polymorpha and P. thunbergii. The derived polypeptide is 54% similar to the product of bchB from Rhodobacter capsulatus, identified as one subunit of a light-independent NADH-protochlorophyllide reductase. We also isolated and sequenced an homologous chloroplastic gene from the gymnosperm Ginkgo biloba. Northern hybridizations performed on RNA isolated from synchronized Chlamydomonas eugametos cells showed higher expression between the tenth hour of light and the eighth hour of darkness, peaking during the first 2 h of darkness.

Key words

Chlamydomonas chlB Ginkgo biloba Protochlorophyllide reductase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baldauf SL, Palmer JD (1990) Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature 344:262–265Google Scholar
  2. Beal SI, Weinstein JD (1991) Biochemistry and regulation of photosynthetic pigment formation in plants and algae. In: Jordan PM (ed) New comprehensive biochemistry, vol 19. Biosynthesis of tetrapyrroles. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 155–235Google Scholar
  3. Bellemare G (1987) Use of a phage vector for rapid synthesis and cloning of single-stranded cDNA. Gene 52:11–19Google Scholar
  4. Bold HC, Alexopoulos CJ, Delevoryas T (1987) Morphology of plants and fungi, 5th edn. Harper and Row, New YorkGoogle Scholar
  5. Bonen I, Doolittle WF (1976) Partial sequence of 16s rRNA and the phylogeny of blue-green algae and chloroplasts. Science 199: 395–403Google Scholar
  6. Burke DH, Alberti M, Hearst JE (1993) bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants. J Bacteriol 175:2414–2422Google Scholar
  7. Castelfranco PA, Beale SI (1983) Chlorophyll biosynthesis: recent advances and areas of current interest. Annu Rev Plant Physiol 34:241–278Google Scholar
  8. Choquet X, Rahire M, Girard-Bascou J, Erickson J, Rochaix JD (1992) A chloroplast gene is required for the light-independent accumulation of chlorophyll in Chlamydomonas reinhardtii. EMBO J 11:1697–1704Google Scholar
  9. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387–395Google Scholar
  10. Douglas S, Turner S (1991) Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. J Mol Evol 33: 267–273Google Scholar
  11. Estable MC (1986) Caractérisation, localisation et identification de gènes sur deux fragments d'ADN chloroplastique de Chlamydomonas moewusii. MSc thesis, Université Laval, Québec, CanadaGoogle Scholar
  12. Ford C, Wang WY (1980a) Three new yellow mutants in Chlamydomonas reinhardtii. Mol Gen Genet 179:259–263Google Scholar
  13. Ford C, Wang WY (1980b) Temperature-sensitive yellow mutants of Chlamydomonas reinhardtii. Mol Gen Genet 180:5–10Google Scholar
  14. Gagné G, Guertin M (1992) The early response to light in the green unicellular alga Chlamydomonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol Biol 18: 429–445Google Scholar
  15. Gantt JS, Baldauf SL, Calie, PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10: 3073–3078Google Scholar
  16. Gray MW (1989) The evolutionary origins of organelles. Trends Genet 5: 294–299Google Scholar
  17. Gray MW (1991) Origin and evolution of plastid genomes and genes. In: Bogorad L, Vasil IK (eds) The molecular biology of plastids. Academic Press, San Diego, pp 303–330Google Scholar
  18. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1–42Google Scholar
  19. Hallick RB, Hong L, Drager RG, Favreau MR, Monford A, Orsat B, Spielmann A, Stutz E (1991) Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res 21:3537–3544Google Scholar
  20. Herrin DL, Battey JF, Greer K, Schmidt GW (1992) Regulation of chlorophyll apoprotein expression and accumulation. J Biol Chem 267:8260–8269Google Scholar
  21. Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of cereals. Mol Gen Genet 217:185–194Google Scholar
  22. Hung MC, Wensink PC (1984) Different restriction enzyme-generated sticky DNA ends can be joined in vitro. Nucleic Acids Res 12:1863–1874Google Scholar
  23. Johanningmeier U (1988) Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur J Biochem 177: 417–424Google Scholar
  24. Karlin-Neumann GA, Kohorn BD, Thornber JP, Tobin EM (1985) A chlorophyll a/b-protein encoded by a gene containing an intron with characteristics of a transposable element. J Mol Appl Genet 3:45–61Google Scholar
  25. Liu X-Q, Xu H, Huang C (1993) Chloroplast chlB gene is required for light-independent chlorophyll accumulation in Chlamydomonas reinhardtii. Plant Mol Biol 23:297–308Google Scholar
  26. Martin W, Cerff R (1986) Prokaryotic features of a nucleus-encoded enzyme. Eur J Biochem 159:323–331Google Scholar
  27. McDonell MW, Simon MN, Studier FW (1977) Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J Mol Biol 110:119–146Google Scholar
  28. Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78Google Scholar
  29. Murphy TM, Thompson WF (1988) Molecular plant development. Prentice Hall, Englewood Cliffs, New JerseyGoogle Scholar
  30. Nédellec P (1991) Etude de la protéine codée par l'ORF563 provenant du génome chloroplastique de Chlamydomonas moewusii. MSc thesis, Université Laval, Québec, CanadaGoogle Scholar
  31. Neuhaus H, Scholz A, Link G (1989) Structure and expression of a split chloroplast gene from mustard (Sinapis alba): ribosomal protein gene rps16 reveals unusual transcriptional features and complex RNA maturation. Curr Genet 15:63–70Google Scholar
  32. Nickelsen J, Link G (1991) RNA-protein interactions at transcript 3′ ends and evidence for trnK-psbA cotranscription in mustard chloroplasts. Mol Gen Genet 228:89–96Google Scholar
  33. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574Google Scholar
  34. Ohyama K, Fukuzawa H, Kohchi T, Sano T, Sano S, Shirai H, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1988) Structure and organization of Marchantia polymorpha chloroplast genome. I. Cloning and gene identification. J Mol Biol 203:281–298Google Scholar
  35. Oliver JL, Marín A, Martínez-Zapater JM (1989) Chloroplast genes transferred to the nuclear plant genome have adjusted to nuclear base composition and codon usage. Nucleic Acid Res 18:65–71Google Scholar
  36. Palmer JD (1985) Comparative organization of chloroplast genomes. Annu Rev Genet 19:325–354Google Scholar
  37. Palmer JD (1986) Isolation and structural analysis of chloroplast DNA. Methods Enzymol 118:167–186Google Scholar
  38. Pichersky E, Tanksley SD (1988) Chloroplast DNA sequences integrated into an intron of a tomato nuclear gene. Mol Gen Genet 215:65–68Google Scholar
  39. Reith M, Munholland J (1993) A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5:465–475Google Scholar
  40. Richard M, Bellemare G (1990) Nucleotide sequence of Chlamydomonas moewusii chloroplastic tRNA-Thr. Nucleic Acids Res 18: 3061Google Scholar
  41. Sambrook J, Maniatis T, Fritsch EF (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  42. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467Google Scholar
  43. Schwartz RM, Dayhoff MO (1978) Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science 199:395–403Google Scholar
  44. Sexton TB, Jones JT, Mullet JE (1990) Sequence and transcriptional analysis of the barley cpDNA region upstream of psbD-psbC encoding trnK(UUU), rps16, trnQ(UUG), psbK, psbI and trnS(GCU) Curr Genet 17:445–454Google Scholar
  45. Shimada H, Sugiura M (1991) Fine structural features of the chloroplast genome: comparison of the sequenced chloroplast genomes. Nucleic Acids Res 19:983–995Google Scholar
  46. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049Google Scholar
  47. Shinogaki K, Hayashida N, Sugiura M (1988) Nicotiana chloroplast genes for components of the photosynthetic apparatus. Photosynthesis Res 18:7–31Google Scholar
  48. Stewart WN (1983) Paleobotany and the evolution of plants. Cambridge University Press, New YorkGoogle Scholar
  49. Suzuki JY, Bauer CE (1992) Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC). Plant Cell 4:929–940Google Scholar
  50. Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40:211–233Google Scholar
  51. Tsudsuki J, Nakashima K, Tsudsuki T, Hiratsuka J, Shibata M, Wakasugi T, Sugiura M (1992) Chloroplast DNA of black pine retains a residual inverted repeat lacking rRNA genes: nucleotide sequences of trnQ, trnK, psbA, trnI and trnH and the absence of rps16. Mol Gen Genet 232:206–214Google Scholar
  52. Turmel M, Bellemare G, Lemieux C (1987) Physical mapping of differences between the chloroplast DNAs of the infertile algae C. eugametos and C. moewusii. Curr Genet 11:543–552Google Scholar
  53. Turmel M, Boudreau E, Boulanger J, Mercier JP, Otis C, Lemieux C (1991) Chloroplast DNA evolution and phylogenetic relationships in Chlamydomonas. In: Dudley EC (ed) The unity of evolutionary biology. Proc 4th Int Congress of Systematics and Evolutionary Biology. Dioscorides Press, Portland, Oregon, pp 816–827Google Scholar
  54. Umesomo K, Inokuchi H, Shiki Y, Takeuchi M, Chang Z, Fukuzawa H, Kohchi T, Shirai H, Ohyama K, Ozeki H (1988) Structure and organization of Marchantia polymorpha chloroplast genome. II. Gene organization of the large single-copy region from rps′ 2 to atpB. J Mol Biol 203:299–331Google Scholar
  55. Weeden NF (1981) Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 17:133–139Google Scholar
  56. Wolfe KH, Sharp PM (1988) Identification of functional open reading frames in chloroplast genomes. Gene 66:215–222Google Scholar
  57. Woodland DW (1991) Contemporary plant systematics. Prentice-Hall, Englewood Cliffs, New JerseyGoogle Scholar
  58. Wu MMJ, Cassidy JR, Pukkila PJ (1983) Polymorphisms in DNA of Coprinus cinereus. Curr Genet 7:385–392Google Scholar
  59. Zsebo KM, Hearst JE (1984) Genetic-physical mapping of a photosynthetic gene cluster from R. capsulata. Cell 37:937–947Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Martine Richard
    • 1
  • Colette Tremblay
    • 1
  • Guy Bellemare
    • 1
  1. 1.Département de Biochimie, Faculté des Sciences et de GénieUniversité LavalQuébecCanada

Personalised recommendations