Abstract.
The mitochondrial genome of the brown alga Pylaiella littoralis contains two different types of group II introns. They each encode complete complex proteins, i.e., with a reverse transcriptase domain, a maturase or X domain, and an endonuclease or H-N-H/zinc finger domain. To our knowledge, this is the first example of the presence in the same genome of introns belonging to subgroups IIA and IIB which both contain multidomained RT-like proteins. We describe the group IIA introns that interrupt the cox1 gene. The RT-like proteins contained in these introns were compared to those of the LSU rDNA group IIB introns. The phylogenetic relationships of these intron ORFs were investigated and the possible evolution of group II introns is discussed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Bauer CC, Ramaswamy KS, Endley S, Golden JW, Haselkon R (1994) Suppression of a heterocyst differentiation in Anabaena sp. strain. (unpublished, U13767)
Bhatthacharya D, Druel LD (1988) Phylogenetic comparison of the small-subunit ribosomal DNA sequence of Costaria costata (Phaeophyta) with those of other algae, vascular plants and oomycetes. J Phycol 24:539–543
Bonitz SG, Coruzzi G, Thalenfeld BE, Tzagoloff A (1980) Assembly of the mitochondrial membrane system structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrome oxidase. J Biol Chem 255:11927–11941
Burger G, Scriven C, Marchleidt W, Werner S (1982) Subunit 1 of cytochrome oxidase from Neurospora crassa: nucleotide sequence of the coding gene and partial amino acids sequence of the protein. EMBO J 1:1385–1391
Burger G, Plante I, Lonergan KM, Gray MW (1995) The mitochondrial DNA of the amoeboid protozoan, Acanthamoeba castellanii: complete sequence, gene content, and genome organization. J Mol Biol 245:522–537
Cummings DJ, Michel F, McNally KL (1989) DNA sequence analysis of 24.5 kilobase pair cytochrome oxydase subunit I mitochondrial gene from Podospora anserina: a gene with sixteen introns. Curr Genet 16:381–406
Costa M, Michel F (1995) Frequent use of the same tertiary motive by self folding RNAs. EMBO J 14:1276–1285
Dalmon J, Loiseaux S (1981) The deoxyribonucleic acids of two brown algae Pylaiella littoralis L. (Kjellm) and Sphacelaria sp. Plant Sci Lett 21:241–251
Delaroque N, Fontaine JM, Kloareg B, Loiseaux-de Goer S (1996) Putative s-70 like promoters in a brown algal mitochondrial genome. C R Acad Sci 319:763–768
Doolittle RF, Feng DF, Johnson MS, Mc Clure MA (1989). Origin and evolutionary relationships of retrovirus. Q Rev Biol 64:1-30 Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ferat JL, Michel F (1993) Group II self splicing introns in bacteria. Nature 364:358–361
Ferat JL, Le Gouar M, Michel F (1994) Multiple group II self splicing introns in mobile DNA from Escherichia coli. C R Acad Sci Paris 317:141–148
Fontaine JM, Rousvoal S, Leblanc C, Kloareg B, Loiseaux-de Goer S (1995a) The mitochondrial LSU rDNA of the brown alga Pylaiella littoralis reveals a-proteobacterial features and is split by four group IIB introns with an atypical phylogeny. J Mol Biol 251:378389
Fontaine JM, Rousvoal S, Delaroque N, Loiseaux-de Goer S (1995b) Characterisation of the cox3, nad7 and atp6 genes from the mitochondrial genome of the brown alga Pylaiella littoralis. Plant Physiol Biochem 33:605–609
Gorbalenya AE (1994) Self splicing group I and group II introns encode homologous (putative) DNA endonucleases of a new family. Protein Sci 3:1117–1120
Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc Natl Acad Sci USA 84:5823–5827
Hardy CM, Clark-Walker GD (1991) Nucleotide sequence of the cox1 gene in Kluyveromyces lactis mitochondrial DNA: evidence for recent horizontal transfert of a group 11 intron. Curr Genet 20:99114
Jacquier A (1990) Self splicing group II and nuclear pre-mRNA introns: how similar are they? Trends Biochem Sci 15:351–354
Jacquier A, Michel F (1990) Base-pairing interactions involving the 5’ and 3’-terminal nucleotides of group II introns. J Mol Biol 213: 437–447
Kuck 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 218:257–265
Kuck U, Godehardt I, Schmidt U (1990) A Self splicing group II intron in the mitochondrial large subunit rRNA (LSUrRNA) gene of the eukaryotic alga Scenedesmus obliquus. Nucleic Acids Res 18:2691–2697
Leblanc C, Boyen C, Richard O, Bonnard G, Grienenberger JM, Kloareg B (1995) Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization. J Mol Biol 250:484–495
Loiseaux-De Goer S, Markowicz Y, Dalmon Y, Audren H (1988) Physical maps of the two circular plastid DNA molecules of the brown alga Pylaiella littoralis (L.) Kjellm. Location of the rRNA genes and of several protein coding regions on both molecules. Curr Genet 14:155–162
Maier UG, Rensing SA, Maerz GLIM (1995) Twintrons are not unique to Euglena chloroplast genome: structure and evolution of a plastome cpn60 gene from a cryptomonad. Mol Gen Gent 246:128–131
McClure M (1991) Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol 8:835–856
Michel F, Dujon B (1983) Conservation of RNA secondary structures in two introns families including mitochondrial, chloroplast and nuclear-encoded members. EMBO J 2:33–38
Michel F, Ferat JL (1995) Structure and activities of group II introns. Annu Rev Biochem 64:435–461
Michel F, Jacquier A (1987) Long-range intron-exon and intron-intron pairings involved in self splicing of class II catalytic introns. Cold Spring Harb Symp Quant Biol 52:201–212
Michel F, Lang BF (1985) Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature 316:641–643
Michel F, Umesono K, Oseki H (1989) Comparative and functional anatomy of group II catalytic introns. Gene 82:5–30
Mohr G, Perlman PS, Lambowitz AM (1993) Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucleic Acids Res 21:4991–4997
Moran JV, Mecklenburg KL, Sass P, Belcher SM, Mahnke D, Lwin A, Perlman PS (1994) Splicing defective mutants of the cox1 gene of yeast mitochondrial DNA: initial definition of the marurase domain of the group II intron AI2. Nucleic Acids Res 22:2057–2064
Moran JV, Zimmerly S, Eskes R, Kennell JC, Lambowitz AM, Butow RN, Perlman PS (1995) Mobile group II introns of yeast mitochondrial DNA are novel site-specific retroelements. Mol Cell Biol 15:2828–2838
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA, a primitive form of plant mitochondrial genome. J Mol Biol 223:1–7
Paquin B, Lang BF (1996) The mitochondrial DNA of Allomyces macrogynus: the complete genomic sequence from an ancestral Fungus. J Mol Biol 255:688–701
Philippe H, Germot A, Leguyadar H, Adoutte A (1995) Que savons nous de l’histoire évolutive des eucaryotes? 1. L’arbre universelle du vivant et les difficultés de la reconstruction phylogénéntique. m/s 11:1–12
Raitio M, Jalli T, Saraste (1987) Isolation of the gene for cytochrome c oxydase in Paracoccus denetrificans. EMBO J 6:2825–22833
Saitou N, Nei M (1987) The Neighbor Joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sachay DJ, Hudspeth DSS, Nadler SA, Hudspeth MES (1993) Oomycete mtDNA: Phytophthora genes for cytochrome c oxidase use a unmodified genetic code and encode proteins most similar to those of plants. Exp Mycol 17:7–23
Sharp PA (1991) Five easy pieces. Science 254:663
Shub DA, Goodrich-Blair H (1994) Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends Biochem Sci 19:402–404
Stoltzfus A, Spencer DF, Zuker M, Logsdon JM, Doolitle WF (1994) Testing the exon theory of genes: the evidence from protein structure. Science 265:202–206
Toh H, Hayashida H, Miyata T (1983) Sequence homology between retroviral reverse transcriptase and putative polymerases of hepatitis B virus and cauliflower mosaic virus. Nature 305:827–829
Weiner AM (1983) mRNA Splicing and autocatalytic introns: distant cousins or products of chemical determinism? Cell 72:161–164
Wolff G, Burger G, Lang BF, Kück U (1993) Mitochondrial genes in the colourless alga Prototheca wickerhamii resemble plant genes in their exons but fungal genes in their introns. Nucleic Acids Res 21:719–726
Wolff G, Plante I, Lang BF, Kuck U, Burger G (1994) Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. Gene content and genome organization. J Mol Biol 237:75–86
Yang J, Zimmerly S, Perlman PS, Lambowitz M (1996) Efficient integration of an intron RNA into double-stranded DNA by reverse splicing. Nature 381:332–335
Zimmerly S, Guo H, Eskes R, Yang J, Perlman PS, Lambowitz A (1995) A group II RNA is a catalytic component of a DNA endonuclease involved in intron mobility. Cell 83:529–538
Author information
Authors and Affiliations
Additional information
Received: 21 May 1996 / Accepted: 4 July 1996
Rights and permissions
About this article
Cite this article
Fontaine, JM., Goux, D., Kloareg, B. et al. The Reverse-Transcriptase-Like Proteins Encoded by Group II Introns in the Mitochondrial Genome of the Brown Alga Pylaiella littoralis Belong to Two Different Lineages Which Apparently Coevolved with the Group II Ribosyme Lineages. J Mol Evol 44, 33–42 (1997). https://doi.org/10.1007/PL00006119
Published:
Issue Date:
DOI: https://doi.org/10.1007/PL00006119