Home LiteratureArticle Details
PMID: 10488235 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae.

The Plant cell ·Vol. 11 ·No. 9 ·1999-09-00 ·Pages 1675-94

Burger G, Saint-Louis D, Gray MW, Lang BF

Abstract

The mitochondrial DNA (mtDNA) of Porphyra purpurea, a circular-mapping genome of 36,753 bp, has been completely sequenced. A total of 57 densely packed genes has been identified, including the basic set typically found in animals and fungi, as well as seven genes characteristic of protist and plant mtDNAs and specifying ribosomal proteins and subunits of succinate:ubiquinone oxidoreductase. The mitochondrial large subunit rRNA gene contains two group II introns that are extraordinarily similar to those found in the cyanobacterium Calothrix sp, suggesting a recent lateral intron transfer between a bacterial and a mitochondrial genome. Notable features of P. purpurea mtDNA include the presence of two 291-bp inverted repeats that likely mediate homologous recombination, resulting in genome rearrangement, and of numerous sequence polymorphisms in the coding and intergenic regions. Comparative analysis of red algal mitochondrial genomes from five different, evolutionarily distant orders reveals that rhodophyte mtDNAs are unusually uniform in size and gene order. Finally, phylogenetic analyses provide strong evidence that red algae share a common ancestry with green algae and plants.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Chlorophyta/genetics Chromosome Mapping Codon/genetics Cyanobacteria/genetics DNA, Bacterial/genetics DNA, Mitochondrial/genetics DNA-Directed DNA Polymerase/genetics Introns Molecular Sequence Data Nucleic Acid Conformation Phylogeny Plants/genetics Polymorphism, Genetic Pseudogenes RNA, Ribosomal, 5S/chemistry,genetics RNA, Transfer/genetics Reading Frames Recombination, Genetic Repetitive Sequences, Nucleic Acid Rhodophyta/genetics Sequence Homology, Amino Acid
Chemicals
Codon DNA, Bacterial DNA, Mitochondrial RNA, Ribosomal, 5S RNA, Transfer DNA-Directed DNA Polymerase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Burger G
Program in Evolutionary Biology, Canadian Institute for Advanced Research, 180 Dundas Street West, Toronto, Ontario M5G 1Z8, Canada. BurgerG@BCH.UMontreal.CA
Saint-Louis D
Gray M W
Lang B F
References (103)
103 references, click to expand
  1. Construction of phylogenetic trees.
    Science. 1967 Jan 20;155(3760):279-84 PMID: 5334057
  2. Nucleotide sequence of Aspergillus nidulans mitochondrial genes coding for ATPase subunit 6, cytochrome oxidase subunit 3, seven unidentified proteins, four tRNAs and L-rRNA.
    Nucleic Acids Res. 1982 Aug 11;10(15):4783-94 PMID: 6290989
  3. Multiple group II self-splicing introns in mobile DNA from Escherichia coli.
    C R Acad Sci III. 1994 Feb;317(2):141-8 PMID: 7994604
  4. The complete mitochondrial DNA sequence of Hansenula wingei reveals new characteristics of yeast mitochondria.
    Curr Genet. 1995 Jun;28(1):39-53 PMID: 8536312
  5. Nonreciprocal recombination between alleles of the chloroplast 23S rRNA gene in interspecific Chlamydomonas crosses.
    Proc Natl Acad Sci U S A. 1987 Jun;84(12):4166-70 PMID: 16593855
  6. Sequence and organization of the human mitochondrial genome.
    Nature. 1981 Apr 9;290(5806):457-65 PMID: 7219534
  7. Isolation and molecular phylogenetic analysis of actin-coding regions from Emiliania huxleyi, a Prymnesiophyte alga, by reverse transcriptase and PCR methods.
    Mol Biol Evol. 1993 May;10(3):689-703 PMID: 7687735
  8. An unusual gene cluster for the cytochrome bc1 complex in Bradyrhizobium japonicum and its requirement for effective root nodule symbiosis.
    Cell. 1989 May 19;57(4):683-97 PMID: 2541921
  9. The gene encoding cytochrome c oxidase subunit II from Rhodobacter sphaeroides; comparison of the deduced amino acid sequence with sequences of corresponding peptides from other species.
    Gene. 1991 May 15;101(1):133-7 PMID: 1648008
  10. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  11. Rapid isolation of nuclei from carrot suspension culture cells using a BioNebulizer.
    Biotechniques. 1994 Jan;16(1):154-9 PMID: 7510981
  12. Genes encoding the same three subunits of respiratory complex II are present in the mitochondrial DNA of two phylogenetically distant eukaryotes.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2328-32 PMID: 8637872
  13. Explosive invasion of plant mitochondria by a group I intron.
    Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14244-9 PMID: 9826685
  14. The wheat mitochondrial gene for apocytochrome b: absence of a prokaryotic ribosome binding site.
    Nucleic Acids Res. 1985 Apr 11;13(7):2281-92 PMID: 2987849
  15. Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns.
    Trends Biochem Sci. 1994 Oct;19(10):402-4 PMID: 7817395
  16. A sequence assembly and editing program for efficient management of large projects.
    Nucleic Acids Res. 1991 Jul 25;19(14):3907-11 PMID: 1861983
  17. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  18. The transcription of DNA in chicken mitochondria initiates from one major bidirectional promoter.
    J Biol Chem. 1991 Jun 15;266(17):10844-50 PMID: 1710214
  19. Nucleotide sequence of the wheat mitochondrial gene for subunit I of cytochrome oxidase.
    Nucleic Acids Res. 1987 Aug 25;15(16):6734 PMID: 2819826
  20. The primary structure of the mitochondrial genome of Saccharomyces cerevisiae--a review.
    Gene. 1986;47(2-3):155-77 PMID: 3549452
  21. Isolation and analysis of the genes for cytochrome c oxidase in Paracoccus denitrificans.
    EMBO J. 1987 Sep;6(9):2825-33 PMID: 16453796
  22. Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos.
    J Mol Biol. 1991 Mar 20;218(2):293-311 PMID: 1849178
  23. A High-Resolution Gene Map of the Chloroplast Genome of the Red Alga Porphyra purpurea.
    Plant Cell. 1993 Apr;5(4):465-475 PMID: 12271072
  24. The nature of the ancestral red alga: inferences from a cladistic analysis.
    Biosystems. 1985;18(3-4):335-46 PMID: 3910138
  25. A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7276-80 PMID: 8041780
  26. The nuclear gene and cDNAs encoding cytosolic glyceraldehyde-3-phosphate dehydrogenase from the marine red alga Gracilaria verrucosa: cloning, characterization and phylogenetic analysis.
    Curr Genet. 1995 Sep;28(4):324-32 PMID: 8590478
  27. A group II intron in a conjugative transposon from the gram-positive bacterium, Clostridium difficile.
    Gene. 1996 Sep 26;174(1):145-50 PMID: 8863741
  28. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria.
    J Biol Chem. 1998 Jul 17;273(29):18003-6 PMID: 9660752
  29. The nucleotide in position 32 of the tRNA anticodon loop determines ability of anticodon UCC to discriminate among glycine codons.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3343-7 PMID: 8475078
  30. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe. The cytochrome b gene has an intron closely related to the first two introns in the Saccharomyces cerevisiae cox1 gene.
    J Mol Biol. 1985 Aug 5;184(3):353-66 PMID: 4046021
  31. The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, and a near-standard genetic code.
    Genetics. 1998 Mar;148(3):1091-108 PMID: 9539427
  32. The wheat cytochrome oxidase subunit II gene has an intron insert and three radical amino acid changes relative to maize.
    EMBO J. 1984 Nov;3(11):2531-6 PMID: 16453565
  33. The ribosomal RNA gene region in Acanthamoeba castellanii mitochondrial DNA. A case of evolutionary transfer of introns between mitochondria and plastids?
    J Mol Biol. 1994 Jun 17;239(4):476-99 PMID: 8006963
  34. Physical map and gene organization of the mitochondrial genome from the unicellular green alga Platymonas (Tetraselmis) subcordiformis (Prasinophyceae).
    Plant Mol Biol. 1995 Dec;29(5):1081-6 PMID: 8555450
  35. Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus: tRNA editing and UAG 'stop' codons recognized as leucine.
    Nucleic Acids Res. 1997 Feb 1;25(3):626-32 PMID: 9016605
  36. The mitochondrial LSU rDNA of the brown alga Pylaiella littoralis reveals alpha-proteobacterial features and is split by four group IIB introns with an atypical phylogeny.
    J Mol Biol. 1995 Aug 18;251(3):378-89 PMID: 7544414
  37. The genes of the Paracoccus denitrificans bc1 complex. Nucleotide sequence and homologies between bacterial and mitochondrial subunits.
    J Biol Chem. 1987 Oct 5;262(28):13805-11 PMID: 2820981
  38. Rapid and sensitive sequence comparison with FASTP and FASTA.
    Methods Enzymol. 1990;183:63-98 PMID: 2156132
  39. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins.
    Cell. 1998 Apr 3;93(1):93-101 PMID: 9546395
  40. Nucleotide sequence of the S-1 mitochondrial DNA from the S cytoplasm of maize.
    EMBO J. 1985 May;4(5):1125-8 PMID: 16453611
  41. Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion).
    Mol Biol Evol. 1995 Jul;12(4):533-45 PMID: 7659010
  42. Genes encoding a subunit of respiratory NADH dehydrogenase (ND1) and a reverse transcriptase-like protein (RTL) are linked to ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA.
    EMBO J. 1988 Nov;7(11):3501-8 PMID: 2463163
  43. The genome sequence of Rickettsia prowazekii and the origin of mitochondria.
    Nature. 1998 Nov 12;396(6707):133-40 PMID: 9823893
  44. The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme.
    Mol Gen Genet. 1989 Aug;218(2):257-65 PMID: 2476655
  45. A rapid, high resolution DNA sequencing gel system.
    Anal Biochem. 1990 Jul;188(1):176-80 PMID: 2221359
  46. The origin of red algae: implications for plastid evolution.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4520-5 PMID: 9114022
  47. Conservation of secondary structure in 5 S ribosomal RNA: a uniform model for eukaryotic, eubacterial, archaebacterial and organelle sequences is energetically favourable.
    Biochimie. 1982 May;64(5):311-29 PMID: 6809061
  48. The ribosomal RNA repeats are non-identical and directly oriented in the chloroplast genome of the red alga Porphyra purpurea.
    Curr Genet. 1993 Nov;24(5):443-50 PMID: 8299161
  49. Kingdom protozoa and its 18 phyla.
    Microbiol Rev. 1993 Dec;57(4):953-94 PMID: 8302218
  50. Genes for a second terminal oxidase in Bradyrhizobium japonicum.
    Arch Microbiol. 1992;158(5):335-43 PMID: 1444719
  51. Nucleotide sequence of the cox3 gene from Chondrus crispus: evidence that UGA encodes tryptophan and evolutionary implications.
    Nucleic Acids Res. 1994 Apr 25;22(8):1400-3 PMID: 8190631
  52. Evidence that eukaryotic triosephosphate isomerase is of alpha-proteobacterial origin.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1270-5 PMID: 9037042
  53. Origin and evolution of retroelements based upon their reverse transcriptase sequences.
    EMBO J. 1990 Oct;9(10):3353-62 PMID: 1698615
  54. Mitochondrial introns as mobile genetic elements: the role of intron-encoded proteins.
    Basic Life Sci. 1986;40:5-27 PMID: 3032144
  55. The complete DNA sequence of the mitochondrial genome of Podospora anserina.
    Curr Genet. 1990 May;17(5):375-402 PMID: 2357736
  56. The mitochondrial DNA of the amoeboid protozoon, Acanthamoeba castellanii: complete sequence, gene content and genome organization.
    J Mol Biol. 1995 Feb 3;245(5):522-37 PMID: 7844823
  57. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  58. A mobile group II intron of a naturally occurring rearranged mitochondrial genome in Kluyveromyces lactis.
    Curr Genet. 1991 Jul;20(1-2):115-20 PMID: 1657410
  59. Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence.
    Nucleic Acids Res. 1998 Nov 15;26(22):5190-8 PMID: 9801318
  60. Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrme oxidase.
    J Biol Chem. 1980 Dec 25;255(24):11927-41 PMID: 6254986
  61. Structure and regulation of SDH3, the yeast gene encoding the cytochrome b560 subunit of respiratory complex II.
    J Biol Chem. 1994 Jun 3;269(22):15469-72 PMID: 8195189
  62. Nucleotide sequence and gene organization of sea urchin mitochondrial DNA.
    J Mol Biol. 1988 Jul 20;202(2):185-217 PMID: 3172215
  63. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. Gene content and genome organization.
    J Mol Biol. 1994 Mar 18;237(1):75-86 PMID: 8133522
  64. Compilation, alignment, and phylogenetic relationships of DNA polymerases.
    Nucleic Acids Res. 1993 Feb 25;21(4):787-802 PMID: 8451181
  65. The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression.
    Curr Genet. 1997 May;31(5):380-95 PMID: 9162109
  66. Cloning, sequencing and deletion from the chromosome of the gene encoding subunit I of the aa3-type cytochrome c oxidase of Rhodobacter sphaeroides.
    Mol Microbiol. 1992 Mar;6(5):635-42 PMID: 1313140
  67. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  68. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature.
    Nature. 1997 May 29;387(6632):493-7 PMID: 9168110
  69. The red algal-higher fungi phylogenetic link: the last ten years.
    Biosystems. 1985;18(3-4):347-56 PMID: 3910139
  70. The marine red alga Chondrus crispus has a highly divergent beta-tubulin gene with a characteristic 5' intron: functional and evolutionary implications.
    Plant Mol Biol. 1995 May;28(2):313-25 PMID: 7599316
  71. Comparative and functional anatomy of group II catalytic introns--a review.
    Gene. 1989 Oct 15;82(1):5-30 PMID: 2684776
  72. Structure and transcription of the gene coding for subunit 3 of cytochrome oxidase in wheat mitochondria.
    Curr Genet. 1990 Jan;17(1):41-7 PMID: 2155710
  73. Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses.
    Nature. 1985 Aug 15-21;316(6029):641-3 PMID: 2412125
  74. Sequence and gene organization of mouse mitochondrial DNA.
    Cell. 1981 Oct;26(2 Pt 2):167-80 PMID: 7332926
  75. Characterization of the gene urf13-T and an unidentified reading frame, ORF 25, in maize and tobacco mitochondria.
    Curr Genet. 1987;12(6):457-63 PMID: 3447748
  76. Elongation factor 1 alpha genes of the red alga Porphyra purpurea include a novel, developmentally specialized variant.
    Plant Mol Biol. 1996 Apr;31(1):77-85 PMID: 8704161
  77. The genetic data environment an expandable GUI for multiple sequence analysis.
    Comput Appl Biosci. 1994 Dec;10(6):671-5 PMID: 7704666
  78. Multiple tertiary interactions involving domain II of group II self-splicing introns.
    J Mol Biol. 1997 Apr 4;267(3):520-36 PMID: 9126835
  79. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome.
    J Biol Chem. 1985 Aug 15;260(17):9759-74 PMID: 4019494
  80. History assignment: when was the mitochondrion founded?
    Curr Opin Genet Dev. 1997 Dec;7(6):792-9 PMID: 9468789
  81. Cloning and DNA sequencing of the fbc operon encoding the cytochrome bc1 complex from Rhodobacter sphaeroides. Characterization of fbc deletion mutants and complementation by a site-specific mutational variant.
    Eur J Biochem. 1990 Dec 12;194(2):399-411 PMID: 2176595
  82. Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization.
    J Mol Biol. 1995 Jul 21;250(4):484-95 PMID: 7616569
  83. Group II self-splicing introns in bacteria.
    Nature. 1993 Jul 22;364(6435):358-61 PMID: 7687328
  84. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles.
    Microbiol Rev. 1983 Mar;47(1):1-45 PMID: 6343825
  85. Transcription initiation and RNA processing in the mitochondria of the red alga Chondrus crispus: convergence in the evolution of transcription mechanisms in mitochondria.
    J Mol Biol. 1998 Oct 30;283(3):549-57 PMID: 9784365
  86. Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function.
    Nucleic Acids Res. 1993 Nov 11;21(22):4991-7 PMID: 8255751
  87. Evolution of linear plasmids.
    J Mol Evol. 1992 Dec;35(6):502-13 PMID: 1474604
  88. Genome structure and gene content in protist mitochondrial DNAs.
    Nucleic Acids Res. 1998 Feb 15;26(4):865-78 PMID: 9461442
  89. Remnants of a DNA polymerase gene in the mitochondrial DNA of Marchantia polymorpha.
    Curr Genet. 1995 Apr;27(5):488-90 PMID: 7586038
  90. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code.
    J Mol Evol. 1985;22(3):252-71 PMID: 3001325
  91. The mitochondrial DNA of Allomyces macrogynus: the complete genomic sequence from an ancestral fungus.
    J Mol Biol. 1996 Feb 9;255(5):688-701 PMID: 8636971
  92. Fungal origin by horizontal transfer of a plant mitochondrial group I intron in the chimeric CoxI gene of Peperomia.
    J Mol Evol. 1995 Nov;41(5):563-72 PMID: 7490770
  93. Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae.
    Mol Microbiol. 1998 Jan;27(1):73-83 PMID: 9466257
  94. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  95. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome.
    J Mol Biol. 1992 Jan 5;223(1):1-7 PMID: 1731062
  96. Primary sequence of wheat mitochondrial 5S ribosomal ribonucleic acid: functional and evolutionary implications.
    Biochemistry. 1981 Jul 7;20(14):4022-9 PMID: 7284306
  97. Cytochrome aa3 of Rhodobacter sphaeroides as a model for mitochondrial cytochrome c oxidase. The coxII/coxIII operon codes for structural and assembly proteins homologous to those in yeast.
    J Biol Chem. 1992 Dec 5;267(34):24273-8 PMID: 1332950
  98. Codon recognition mechanisms in plant chloroplasts.
    Plant Mol Biol. 1990 May;14(5):805-14 PMID: 2102858
  99. Animal mitochondrial DNA: structure and evolution.
    Int Rev Cytol. 1992;141:173-216 PMID: 1452431
  100. The Organelle Genome Database Project (GOBASE).
    Nucleic Acids Res. 1998 Jan 1;26(1):138-44 PMID: 9399818
  101. The plant mitochondrial open reading frame orf221 encodes a membrane-bound protein.
    Plant Mol Biol. 1993 Oct;23(2):287-95 PMID: 8219065
  102. Fate of Parasite and Host Organelle DNA during Cellular Transformation of Red Algae by Their Parasites.
    Plant Cell. 1995 Nov;7(11):1899-1911 PMID: 12242362
  103. DNA sequence, structure, and phylogenetic relationship of the mitochondrial small-subunit rRNA from the red alga Chondrus crispus (Gigartinales rhodophytes).
    J Mol Evol. 1995 Aug;41(2):196-202 PMID: 7666449
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.11.9.1675
Email
burgerg@bch.umontreal.ca
Published
1999-09-00
Pages
1675-94
Language
English
Region
England
NLM ID
9208688
PMCID
PMC144311
Subset
IM
Databases
GENBANK
AF114794, AF116776, AF116777, AF116778
Corrections
CommentIn
PMID: 10488229
External Links
PubMed source DOI: 10.1105/tpc.11.9.1675 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2