Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1993 Apr;5(4):465–475. doi: 10.1105/tpc.5.4.465

A High-Resolution Gene Map of the Chloroplast Genome of the Red Alga Porphyra purpurea.

M Reith 1, J Munholland 1
PMCID: PMC160285  PMID: 12271072

Abstract

Extensive DNA sequencing of the chloroplast genome of the red alga Porphyra purpurea has resulted in the detection of more than 125 genes. Fifty-eight (approximately 46%) of these genes are not found on the chloroplast genomes of land plants. These include genes encoding 17 photosynthetic proteins, three tRNAs, and nine ribosomal proteins. In addition, nine genes encoding proteins related to biosynthetic functions, six genes encoding proteins involved in gene expression, and at least five genes encoding miscellaneous proteins are among those not known to be located on land plant chloroplast genomes. The increased coding capacity of the P. purpurea chloroplast genome, along with other characteristics such as the absence of introns and the conservation of ancestral operons, demonstrate the primitive nature of the P. purpurea chloroplast genome. In addition, evidence for a monophyletic origin of chloroplasts is suggested by the identification of two groups of genes that are clustered in chloroplast genomes but not in cyanobacteria.

Full Text

The Full Text of this article is available as a PDF (981.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. An G., Bendiak D. S., Mamelak L. A., Friesen J. D. Organization and nucleotide sequence of a new ribosomal operon in Escherichia coli containing the genes for ribosomal protein S2 and elongation factor Ts. Nucleic Acids Res. 1981 Aug 25;9(16):4163–4172. doi: 10.1093/nar/9.16.4163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arizmendi J. M., Runswick M. J., Skehel J. M., Walker J. E. NADH: ubiquinone oxidoreductase from bovine heart mitochondria. A fourth nuclear encoded subunit with a homologue encoded in chloroplast genomes. FEBS Lett. 1992 Apr 27;301(3):237–242. doi: 10.1016/0014-5793(92)80248-f. [DOI] [PubMed] [Google Scholar]
  3. Bachmann B., Lüke W., Hunsmann G. Improvement of PCR amplified DNA sequencing with the aid of detergents. Nucleic Acids Res. 1990 Mar 11;18(5):1309–1309. doi: 10.1093/nar/18.5.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baldauf S. L., Manhart J. R., Palmer J. D. Different fates of the chloroplast tufA gene following its transfer to the nucleus in green algae. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5317–5321. doi: 10.1073/pnas.87.14.5317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bryant D. A., Schluchter W. M., Stirewalt V. L. Ferredoxin and ribosomal protein S10 are encoded on the cyanelle genome of Cyanophora paradoxa. Gene. 1991 Feb 15;98(2):169–175. doi: 10.1016/0378-1119(91)90170-g. [DOI] [PubMed] [Google Scholar]
  6. Christopher D. A., Hallick R. B. Euglena gracilis chloroplast ribosomal protein operon: a new chloroplast gene for ribosomal protein L5 and description of a novel organelle intron category designated group III. Nucleic Acids Res. 1989 Oct 11;17(19):7591–7608. doi: 10.1093/nar/17.19.7591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Douglas S. E. Eukaryote-eukaryote endosymbioses: insights from studies of a cryptomonad alga. Biosystems. 1992;28(1-3):57–68. doi: 10.1016/0303-2647(92)90008-m. [DOI] [PubMed] [Google Scholar]
  8. Douglas S. E., Murphy C. A., Spencer D. F., Gray M. W. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature. 1991 Mar 14;350(6314):148–151. doi: 10.1038/350148a0. [DOI] [PubMed] [Google Scholar]
  9. Douglas S. E. Unusual organization of a ribosomal protein operon in the plastid genome of Cryptomonas phi: evolutionary considerations. Curr Genet. 1991 Apr;19(4):289–294. doi: 10.1007/BF00355057. [DOI] [PubMed] [Google Scholar]
  10. Erdmann R., Wiebel F. F., Flessau A., Rytka J., Beyer A., Fröhlich K. U., Kunau W. H. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell. 1991 Feb 8;64(3):499–510. doi: 10.1016/0092-8674(91)90234-p. [DOI] [PubMed] [Google Scholar]
  11. Falk G., Walker J. E. DNA sequence of a gene cluster coding for subunits of the F0 membrane sector of ATP synthase in Rhodospirillum rubrum. Support for modular evolution of the F1 and F0 sectors. Biochem J. 1988 Aug 15;254(1):109–122. doi: 10.1042/bj2540109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fong S. E., Surzycki S. J. Chloroplast RNA polymerase genes of Chlamydomonas reinhardtii exhibit an unusual structure and arrangement. Curr Genet. 1992 May;21(6):485–497. doi: 10.1007/BF00351659. [DOI] [PubMed] [Google Scholar]
  13. Gray M. W., Doolittle W. F. Has the endosymbiont hypothesis been proven? Microbiol Rev. 1982 Mar;46(1):1–42. doi: 10.1128/mr.46.1.1-42.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gray M. W. The evolutionary origins of organelles. Trends Genet. 1989 Sep;5(9):294–299. doi: 10.1016/0168-9525(89)90111-x. [DOI] [PubMed] [Google Scholar]
  15. Hiratsuka J., Shimada H., Whittier R., Ishibashi T., Sakamoto M., Mori M., Kondo C., Honji Y., Sun C. R., Meng B. Y. 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 the cereals. Mol Gen Genet. 1989 Jun;217(2-3):185–194. doi: 10.1007/BF02464880. [DOI] [PubMed] [Google Scholar]
  16. Kessler U., Maid U., Zetsche K. An equivalent to bacterial ompR genes is encoded on the plastid genome of red algae. Plant Mol Biol. 1992 Feb;18(4):777–780. doi: 10.1007/BF00020019. [DOI] [PubMed] [Google Scholar]
  17. Kostrzewa M., Zetsche K. Large ATP synthase operon of the red alga Antithamnion sp. resembles the corresponding operon in cyanobacteria. J Mol Biol. 1992 Oct 5;227(3):961–970. doi: 10.1016/0022-2836(92)90238-f. [DOI] [PubMed] [Google Scholar]
  18. Kusian B., Yoo J. G., Bednarski R., Bowien B. The Calvin cycle enzyme pentose-5-phosphate 3-epimerase is encoded within the cfx operons of the chemoautotroph Alcaligenes eutrophus. J Bacteriol. 1992 Nov;174(22):7337–7344. doi: 10.1128/jb.174.22.7337-7344.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lang J. D., Haselkorn R. Isolation, sequence and transcription of the gene encoding the photosystem II chlorophyll-binding protein, CP-47, in the cyanobacterium Anabaena 7120. Plant Mol Biol. 1989 Oct;13(4):441–457. doi: 10.1007/BF00015556. [DOI] [PubMed] [Google Scholar]
  20. Li S. J., Rock C. O., Cronan J. E., Jr The dedB (usg) open reading frame of Escherichia coli encodes a subunit of acetyl-coenzyme A carboxylase. J Bacteriol. 1992 Sep;174(17):5755–5757. doi: 10.1128/jb.174.17.5755-5757.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Linne von Berg K. H., Kowallik K. V. Structural organization of the chloroplast genome of the chromophytic alga Vaucheria bursata. Plant Mol Biol. 1992 Jan;18(1):83–95. doi: 10.1007/BF00018459. [DOI] [PubMed] [Google Scholar]
  22. Maid U., Zetsche K. A 16 kb small single-copy region separates the plastid DNA inverted repeat of the unicellular red alga Cyanidium caldarium: physical mapping of the IR-flanking regions and nucleotide sequences of the psbD-psbC, rps16, 5S rRNA and rpl21 genes. Plant Mol Biol. 1992 Sep;19(6):1001–1010. doi: 10.1007/BF00040531. [DOI] [PubMed] [Google Scholar]
  23. Margulis L., Obar R. Heliobacterium and the origin of chrysoplasts. Biosystems. 1985;17(4):317–325. doi: 10.1016/0303-2647(85)90047-4. [DOI] [PubMed] [Google Scholar]
  24. Mayes S. R., Barber J. Primary structure of the psbN-psbH-petC-petA gene cluster of the cyanobacterium Synechocystis PCC 6803. Plant Mol Biol. 1991 Aug;17(2):289–293. doi: 10.1007/BF00039508. [DOI] [PubMed] [Google Scholar]
  25. McCarn D. F., Whitaker R. A., Alam J., Vrba J. M., Curtis S. E. Genes encoding the alpha, gamma, delta, and four F0 subunits of ATP synthase constitute an operon in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol. 1988 Aug;170(8):3448–3458. doi: 10.1128/jb.170.8.3448-3458.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Michalowski C. B., Löffelhardt W., Bohnert H. J. An ORF323 with homology to crtE, specifying prephytoene pyrophosphate dehydrogenase, is encoded by cyanelle DNA in the eukaryotic alga Cyanophora paradoxa. J Biol Chem. 1991 Jun 25;266(18):11866–11870. [PubMed] [Google Scholar]
  27. Neumann-Spallart C., Brandtner M., Kraus M., Jakowitsch J., Bayer M. G., Maier T. L., Schenk H. E., Löffelhardt W. The petFI gene encoding ferredoxin I is located close to the str operon on the cyanelle genome of Cyanophora paradoxa. FEBS Lett. 1990 Jul 30;268(1):55–58. doi: 10.1016/0014-5793(90)80971-k. [DOI] [PubMed] [Google Scholar]
  28. O'Toole P. W., Logan S. M., Kostrzynska M., Wadström T., Trust T. J. Isolation and biochemical and molecular analyses of a species-specific protein antigen from the gastric pathogen Helicobacter pylori. J Bacteriol. 1991 Jan;173(2):505–513. doi: 10.1128/jb.173.2.505-513.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Orsat B., Monfort A., Chatellard P., Stutz E. Mapping and sequencing of an actively transcribed Euglena gracilis chloroplast gene (ccsA) homologous to the Arabidopsis thaliana nuclear gene cs(ch-42). FEBS Lett. 1992 Jun 1;303(2-3):181–184. doi: 10.1016/0014-5793(92)80514-h. [DOI] [PubMed] [Google Scholar]
  30. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Reinhold-Hurek B., Shub D. A. Self-splicing introns in tRNA genes of widely divergent bacteria. Nature. 1992 May 14;357(6374):173–176. doi: 10.1038/357173a0. [DOI] [PubMed] [Google Scholar]
  32. Reith M., Munholland J. An hsp70 homolog is encoded on the plastid genome of the red alga, Porphyra umbilicalis. FEBS Lett. 1991 Dec 2;294(1-2):116–120. doi: 10.1016/0014-5793(91)81355-c. [DOI] [PubMed] [Google Scholar]
  33. Reith M., Munholland J. Two amino-acid biosynthetic genes are encoded on the plastid genome of the red alga Porphyra umbilicalis. Curr Genet. 1993 Jan;23(1):59–65. doi: 10.1007/BF00336751. [DOI] [PubMed] [Google Scholar]
  34. Reith M. psaE and trnS(CGA) are encoded on the plastid genome of the red alga Porphyra umbilicalis. Plant Mol Biol. 1992 Feb;18(4):773–775. doi: 10.1007/BF00020018. [DOI] [PubMed] [Google Scholar]
  35. Richard M., Bellemare G. Nucleotide sequence of Chlamydomonas moewusii chloroplastic tRNA(thr). Nucleic Acids Res. 1990 May 25;18(10):3061–3061. doi: 10.1093/nar/18.10.3061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sasaki Y., Nagano Y., Morioka S., Ishikawa H., Matsuno R. A chloroplast gene encoding a protein with one zinc finger. Nucleic Acids Res. 1989 Aug 11;17(15):6217–6227. doi: 10.1093/nar/17.15.6217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shen J. R., Ikeuchi M., Inoue Y. Stoichiometric association of extrinsic cytochrome c550 and 12 kDa protein with a highly purified oxygen-evolving photosystem II core complex from Synechococcus vulcanus. FEBS Lett. 1992 Apr 20;301(2):145–149. doi: 10.1016/0014-5793(92)81235-e. [DOI] [PubMed] [Google Scholar]
  38. Shivji M. S., Li N., Cattolico R. A. Structure and organization of rhodophyte and chromophyte plastid genomes: implications for the ancestry of plastids. Mol Gen Genet. 1992 Mar;232(1):65–73. doi: 10.1007/BF00299138. [DOI] [PubMed] [Google Scholar]
  39. Smith A. G., Wilson R. M., Kaethner T. M., Willey D. L., Gray J. C. Pea chloroplast genes encoding a 4 kDa polypeptide of photosystem I and a putative enzyme of C1 metabolism. Curr Genet. 1991 May;19(5):403–410. doi: 10.1007/BF00309603. [DOI] [PubMed] [Google Scholar]
  40. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Suzuki J. Y., Bauer C. E. Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC). Plant Cell. 1992 Aug;4(8):929–940. doi: 10.1105/tpc.4.8.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Torian B. E., Flores B. M., Stroeher V. L., Hagen F. S., Stamm W. E. cDNA sequence analysis of a 29-kDa cysteine-rich surface antigen of pathogenic Entamoeba histolytica. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6358–6362. doi: 10.1073/pnas.87.16.6358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Urbach E., Robertson D. L., Chisholm S. W. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature. 1992 Jan 16;355(6357):267–270. doi: 10.1038/355267a0. [DOI] [PubMed] [Google Scholar]
  44. Valentin K., Zetsche K. Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta. Plant Mol Biol. 1990 Oct;15(4):575–584. doi: 10.1007/BF00017832. [DOI] [PubMed] [Google Scholar]
  45. Willey D. L., Gray J. C. An open reading frame encoding a putative haem-binding polypeptide is cotranscribed with the pea chloroplast gene for apocytochrome f. Plant Mol Biol. 1990 Aug;15(2):347–356. doi: 10.1007/BF00036920. [DOI] [PubMed] [Google Scholar]
  46. Yamamoto T., Matsui Y., Natori S., Obinata M. Cloning of a housekeeping-type gene (MER5) preferentially expressed in murine erythroleukemia cells. Gene. 1989 Aug 15;80(2):337–343. doi: 10.1016/0378-1119(89)90297-7. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES