Molecular and General Genetics MGG

, Volume 232, Issue 1, pp 65–73

Structure and organization of rhodophyte and chromophyte plastid genomes: implications for the ancestry of plastids

  • M. S. Shivji
  • N. Li
  • R. A. Cattolico
Article

Summary

Plastid genomes of two rhodophytes (Porphyra yezoensis and Griffithsia pacifica) and two chromophytes (Olisthodiscus luteus and Ochromonas danica) were compared with one another and with green plants in terms of overall structure, gene complement and organization. The rhodophyte genomes are moderately co-linear in terms of gene organization, and are distinguished by three rearrangements that can most simply be explained by transpositions and a large (approximately 40 kb) inversion. Porphyra contains two loci for ppcBA and Griffithsia has two loci for rpoA. Although there is little similarity in gene organization between the rhodophytes and consensus green plant genome, certain gene clusters found in green plants appear to be conserved in the rhodophytes. The chromophytes Olisthodiscus and Ochromonas contain relatively large plastid inverted repeats that encode several photosynthetic genes in addition to the rRNA genes. With the exception of rbcS, the plastid gene complement in Olisthodiscus is similar to that of green plants, at least for the subset of genes tested. The Ochromonas genome, in contrast, appears unusual in that several of the green plant gene probes hybridizing to Olisthodiscus DNA did not detect similar sequences in Ochromonas DNA. Gene organization within the chromophytes is scrambled relative to each other and to green plants, despite the presence of putatively stabilizing inverted repeats. However, some gene clusters conserved in green plants and rhodophytes are also present in the chromophytes. Comparison of the entire rhodophyte, chromophyte and green plant plastid genomes suggests that despite diferences in gene organization, there remain overall similarities in architecture, gene content, and gene sequences among in three lineages. These similarities are discussed with reference to the ancestry of the different plastid types.

Key words

Rhodophyte and chromophyte plastid DNA Plastid genome organization Plastid ancestry 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alt J, Morris J, Westhoff P, Herrmann RG (1984) Nucleotide sequence of the clustered genes for the 44 kD chlorophyll a apoprotein and the “32 kD” like protein of the Photosystem II reaction center in the spinach plastid chromosome. Curr Genet 8:597–606Google Scholar
  2. Assali N-E, Mache R, Loiseaux-de Goër S (1990) Evidence for a composite phylogenetic origin of the plastid genome of the brown alga Pylaiella littoralis (L.) Kjellm. Plant Mol Biol 15:307–315Google Scholar
  3. Baldauf SL, Palmer JD (1990) Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature 344:262–265Google Scholar
  4. Bancroft I, Wolk CP, Oren EV (1989) Physical and genetic maps for the genome of the heterocyst forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 171:5940–5948Google Scholar
  5. Boczar BA, Delaney T, Cattolico RA (1989) The gene for the ribulose-1,5-bisphosphate carboxylase (Rubisco) small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci USA 86:4996–4999Google Scholar
  6. Bold HC, Wynne MJ (1985) Introduction to the algae. Prentice Hall, Engelwood Cliffs, New JerseyGoogle Scholar
  7. Boyen C, Somerville CC, Le Gall Y, Kloareg B, De Goër (1991) Physical mapping of the plastid genome from the rhodophyte Chondrus crispus. J Phycol 27:11Google Scholar
  8. Bryant DA, DeLorimer R, Lambert DH, Dubbs JM, Stirewalt VL, Edward Stevens Jr, S, Porter RD, Tam J, Jay E (1985) Molecular cloning and nucleotide sequence of the α and β subunits of allophycocyanin from the cyanelle genome of Cyanophora paradoxa. Proc Natl Acad Sci USA 82:3242–3246Google Scholar
  9. Cavalier-Smith T (1982) The origin of plastids. Biol J Linn Soc 17:289–206Google Scholar
  10. Cavalier-Smith T (1986) The Kingdom Chromista: Origin and systematics. Prog Phycol Res 4:309–347Google Scholar
  11. Cavalier-Smith T (1987) The simultaneous symbiotic origin of mitochondria, chloroplasts and microbodies. Ann NY Acad Sci 503:55–71Google Scholar
  12. Cavalier-Smith T (1989) The Kingdom Chromista. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte algae — Problems and perspectives. Clarendon Press, Oxford pp 382–407Google Scholar
  13. Chesnick JM, Kugrens P, Cattolico RA (1991) The utility of mitochondrial DNA restriction fragment length polymorphisms to cryptomonad phylogenetic assessment. Molec Marine Biol and Biotech 1:18–26Google Scholar
  14. Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kück U, Bennoun P, Rochaix J-D (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52:903–913Google Scholar
  15. Coleman AW, Goff LJ (1991) DNA analysis of eukaryotic algal species. J Phycol 27:463–473Google Scholar
  16. Delaney TP (1989) Evolution, structure and organization of chloroplast ribosomal DNA in selected non-chlorophytic algae. PhD Thesis, University of WashingtonGoogle Scholar
  17. Delaney TP, Cattolico RA (1989) Chloroplast ribosomal DNA organization in the chromophytic alga Olisthodiscus luteus. Curr Genet 15:221–229Google Scholar
  18. Douglas SE (1988) Physical mapping of the plastid genome from the chlorophyll c-containing alga, Cryptomonas φ. Curr Genet 14:591–598Google Scholar
  19. Douglas SE, Durnford D, Morden CW (1990) Nucleotide sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from Cryptomonas φ: Evidence supporting the polyphyletic origins of plastids. J Phycol 26:500–508Google Scholar
  20. Dryden SC, Kaplan S (1990) Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res 18:7267–7270Google Scholar
  21. Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13Google Scholar
  22. Gabrielson PW, Garbary DJ, Scagel RF (1985) The nature of the ancestral red alga: Inferences from a cladistic analysis. BioSystems 18:335–346Google Scholar
  23. Gibbs SP (1981) The chloroplast of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann NY Acad Sci 361:193–207Google Scholar
  24. Gouy M, Li W-H (1990) Arachaebacterial or eocyte tree? Nature 343:419Google Scholar
  25. Gray MW (1988) Organelle origins and ribosomal RNA. Biochem Cell Biol 66:325–348Google Scholar
  26. Gray MW (1989) The evolutionary origins of organelles. Trends Genet 5:11–16Google Scholar
  27. Groning BR, Frischmuth T, Jeske H (1990) Replicative form DNA of abutilon mosaic virus is present in plastids. Mol Gen Genet 220:485–488Google Scholar
  28. Hara Y, Inouye I, Chihara (1985) Morphology and ultrastructure of Olisthodiscus luteus (Raphidophyceae) with special reference to the taxonomy. Bot Mag Tokyo 98:251–262Google Scholar
  29. Hardison LK, Boczar BA, Reynolds AE, Cattolico RA (1991) A description of the Rubisco large subunit gene and its transcript in Olisthodiscus luteus. Plant Molec Biol (in press)Google Scholar
  30. Hudson GS, Mason JG, Holtan TA, Koller B, Cox GB, Whitfeld PR, Bottomley W (1987) A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and three CF0 subunits of the H+-ATP synthase complex and the ribosomal protein S2. J Mol Biol 196:283–298Google Scholar
  31. Hwang S-R, Tabita FR (1989) Cloning and expression of the chloroplast encoded trbcL and rrbcS genes from the marine diatom Cylindrotheca sp. strain N1. Plant Mol Biol 13:69–70Google Scholar
  32. Kostrzewa M, Valentin K, Maid U, Radetzky R, Zetsche K (1990) Structure of the Rubisco operon from the multicellular red alga Antithamnion spec. Curr Gen 18:465–469Google Scholar
  33. Kowallik KV (1989) Molecular aspects and phylogenetic implications of plastid genomes of certain chromophytes. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte Algae — Problems and perspectives. Clarendon Press, Oxford pp 101–124Google Scholar
  34. Kück U (1989) The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme. Mol Gen Genet 218:257–265Google Scholar
  35. Lake JA (1990) Archaebacterial or eocyte tree? Nature 343:419Google Scholar
  36. Lemaux PG, Grossman AR (1984) Isolation and characterization of a gene for a major light-harvesting polypeptide from Cyanophora paradoxa. Proc Natl Acad Sci USA 81:4100–4104Google Scholar
  37. Li N (1989) Characterization of chloroplast genomes from the rhodophytic alga Griffithsia pacifica and the chrysophytic alga Ochromonas danica PhD Thesis, University of WashingtonGoogle Scholar
  38. Li N, Cattolico RA (1987) Chloroplast genome characterization in the red alga Griffithsia pacifica. Mol Gen Genet 209:343–351Google Scholar
  39. Loiseaux-de Goër S, Markowicz Y, Dalmon J, Audren H (1988) Physical maps of the two circular plastid DNA molecules of the brown alga Pylaiella littoralis (L.) Kjellan. Curr Genet 14:155–162Google Scholar
  40. Manhart JR, Kelly K, Dudock BS, Palmer JD (1989) Unusual characteristics of Codium fragile chloroplast DNA revealed by physical and gene mapping. Mol Gen Genet 216:417–421Google Scholar
  41. Manhart JR, Hoshaw RW, Palmer JD (1990) Unique chloroplast genome in Spirogyra maxima (Chlorophyta) revealed by physical and gene mapping. J Phycol 26:490–494Google Scholar
  42. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  43. Markowicz Y, Loiseaux-de Goër S, Mache R (1988) Presence of a 16S rRNA pseudogene in the bimolecular plastid genome of the primitive brown alga Pylaiella littoralis. Curr Genet 14:599–608Google Scholar
  44. Mazel D, Houmard J, Tandeau de Marsac N (1988) A multigene family in Calothrix sp PCC 7601 encodes phycocyanin, the major component of the cyanobacterial light-harvesting proteins. Mol Gen Genet 211:296–304Google Scholar
  45. Miller DJ, McMillan J, Miles A, ten Lohuis M, Mahony T (1990) Nucleotide sequence of the histone H3-encoding gene from the scleractinian coral Acropora formosa (Cnidaria: Scleractinia). Gene 93:319–320Google Scholar
  46. Mishler BD, Bremer K, Humphries CJ, Churchill SP (1988) The use of nucleic acid sequence data in phylogenetic reconstruction. Taxon 37:391–395Google Scholar
  47. Morden CW, Golden SS (1989) psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337:382–385Google Scholar
  48. Newman S, Cattolico RA (1990) Ribulose bisphosphate carboxylase in algae: Synthesis, enzymology and evolution. Photosyn Res 27:69–76Google Scholar
  49. Ohme M, Tanaka M, Chunwongse K, Shinozaki K, Sugiura M (1986) A tobacco chloroplast DNA sequence possibly coding for a polypeptide similar to E. coli RNA polymerase β-subunit. FEBS Lett 200:87–90Google Scholar
  50. Oishi KK, Shapiro DR, Tewari KK (1984) Sequence organization of a pea chloroplast DNA gene coding for a 34,500 Dalton protein. Mol Cell Biol 4:2556–2563Google Scholar
  51. Palmer JD (1985) Evolution of chloroplast and mitochondrial DNA in plants and algae. In: RJ MacIntyre (ed), Molecular evolutionary genetics, Plenum, New York, pp 131–240Google Scholar
  52. Palmer JD, Nugent JM, Herbon LA (1987) Unusual structure of geranium chloroplast DNA: A triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. Proc Natl Acad Sci USA 84:769–773Google Scholar
  53. Palmer JD, Osorio B, Thompson WF (1988) Evolutionary significance of inversions in legume chloroplast DNAs. Curr Genet 14:65–74Google Scholar
  54. Raven PH (1970) A multiple origin for plastids and mitochondria. Science 169:641–645Google Scholar
  55. Reith M, Cattolico RA (1986) Inverted repeat of Olisthodiscus luteus chloroplast DNA contains genes for both subunits of ribulose-1,5-bisphosphate carboxylase and the 32,000 dalton QB protein: Phylogenetic implications. Proc Natl Acad Sci USA 83:8599–8603Google Scholar
  56. Rochaix JD, Dron M, Rahire M, Malnoe P (1984) Sequence homology between the 32K dalton and the D2 chloroplast membrane polypeptides of Chlamydomonas reinhardii. Plant Mol Biol 3:363–370Google Scholar
  57. Rohlf FJ, Chang WS, Sokal RR, Kim J (1990) Accuracy of estimated phylogenies: effects of tree topology and evolutionary model. Evolution 44:1671–1684Google Scholar
  58. Schoelz JE, Zaitlin M (1989) Tobacco mosaic virus RNA enters chloroplast in vivo. Proc Natl Acad Sci USA 86:4496–4500Google Scholar
  59. Shinozaki K, Hayashida N, Sugiura M (1988) Nicotiana chloroplast genes for components of the photosynthetic apparatus. Photosynth Res 18:7–31Google Scholar
  60. Shivji M (1991) Organization of the chloroplast genome in the red alga Porphyra yezoensis. Curr Genet 19:49–54Google Scholar
  61. Sijben-Muller G, Hallick RB, Alt J, Westhoff P, Herrmann RG (1986) Spinach plastid genes coding for initiation factor IF-1, ribosomal protein S-11 and RNA polymerase — subunit. Nucleic Acids Res 14:1029–1044Google Scholar
  62. Sugiura M (1989) The chloroplast chromosomes in land plants. Annu Rev Cell Biol 5:51–70Google Scholar
  63. Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher plants. Proc Natl Acad Sci USA 87:8526–8530Google Scholar
  64. Turner S, Burger-Wiersma T, Giovannoni SJ, Mur LR, Pace NR (1989) The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337:380–382Google Scholar
  65. Valentin K, Zetsche K (1990 a) Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222:425–430Google Scholar
  66. Valentin K, and Zetsche K (1990 b) Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta. Plant Mol Biol 15:575–584Google Scholar
  67. Van de Peer Y, Neefs JM, De Wachter R (1990) Small ribisomal subunit RNA sequences, evolutionary relationships among different life forms, and mitochondrial origins. J Mol Evol 30:463–476Google Scholar
  68. Wilhelm C (1987) The existence of chlorophyll c in the chl b-containing, light-harvesting complex of the green alga Mantoniella squamata (Prasinophyceae). Botanica Acta 101:7–10Google Scholar
  69. Willey DL, Auffret AD, Gray JC (1984) Structure and topology of cytochrome f in pea chloroplast membranes. Cell 36:555–562Google Scholar
  70. Zurawski G, Bottomley W, Whitfield PR (1982) Structures of the genes for the B and E subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79:6260–6264Google Scholar
  71. Zurawski G, Bottomley W, Whitfield PR (1986) Sequence of the genes for the B and E subunits of ATP synthase from pea chloroplasts. Nucleic Acids Res 14:3974Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • M. S. Shivji
    • 1
  • N. Li
    • 2
  • R. A. Cattolico
    • 3
  1. 1.School of Fisheries, HF-10University of WashingtonSeattleUSA
  2. 2.Department of Botany, KB-15University of WashingtonSeattleUSA
  3. 3.Departments of Botany and OceanographyUniversity of WashingtonSeattleUSA
  4. 4.Tetra Tech, Inc.BellevueUSA
  5. 5.USDA/ARS/PS1Plant Molecular Biology LaboratoryBeltsvilleUSA

Personalised recommendations