Skip to main content
SpringerLink
Log in

Molecular phylogenetic analysis of actin genic regions fromAchlya bisexualis (Oomycota) andCostaria costata (Chromophyta)

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Actin genic regions were isolated and characterized from the heterokont-flagellated protists,Achlya bisexualis (Oomycota) andCostaria costata (Chromophyta). Restriction enzyme and cloning experiments suggested that the genes are present in a single copy and sequence determinations revealed the existence of two introns in theC. costata actin genic region. Phylogenetic analyses of actin genic regions using distance matrix and maximum parsimony methods confirmed the close evolutionary relationship ofA. bisexualis andC. costata suggested by ribosomal DNA (rDNA) sequence comparisons and reproductive cell ultrastructure. The higher fungi, green plants, and animals were seen as monophyletic groups; however, a precise order of branching for these assemblages could not be determined. Phylogenetic frameworks inferred from comparisons of rRNAs were used to assess rates of evolution in actin genic regions of diverse eukaryotes. Actin genic regions had nonuniform rates of nucleotide substitution in different lineages. Comparison of rates of actin and rDNA sequence divergence indicated that actin genic regions evolve 2.0 and 5.3 times faster in higher fungi and flowering plants, respectively, than their rDNA sequences. Conversely, animal actins evolve at approximately one-fifth the rate of their rDNA sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alonso S (1987) Coexpression and evolution of the two sarcomeric actin genes in vertebrates. Biochimie 69:1119–1125

    PubMed  Google Scholar 

  • Amar MFB, Pays A, Tebabi P, Dero B, Seebeck T, Steinert M, Pays E (1988) Structure and transcription of the actin gene ofTrypanosoma brucei. Mol Cell Biol 8:2166–2176

    PubMed  Google Scholar 

  • Andersen RA (1987) Synurophyceae classis nov., a new class of algae. Am J Bot 74:337–353

    Google Scholar 

  • Ariztia EV, Andersen RA, Sogin ML (1991) A new phylogeny for chromophyte algae using 16S-like rRNA sequences fromMallomonas papillosa (Synurophyceae) andTribonema aequale (Xanthophyceae). J Phycol 27:428–436

    Google Scholar 

  • Bhattacharya D, Druehl LD (1988) Phylogenetic comparison of the small-subunit ribosomal DNA sequence ofCostaria costata (Phaeophyta) with those of other algae, vascular plants and oomycetes. J Phycol 24:539–543

    Google Scholar 

  • Bhattacharya D, Druehl LD (1990) Restriction enzyme analysis of variation and taxonomy in the kelp genusLaminaria (Laminariales, Phaeophyta). Hydrobiologia 204/205:105–110

    Google Scholar 

  • Chisholm D (1989) A convenient moderate-scale procedure for obtaining DNA from bacteriophage lambda. Biotechniques 7:21–23

    PubMed  Google Scholar 

  • Clark CG, Tague BW, Ware VC, Gerbi SA (1984)Xenopus laevis 28S ribosomal RNA: a secondary structure model and its evolutionary and functional implications. Nucleic Acids Res 12:6197–6220

    PubMed  Google Scholar 

  • Crain WR Jr, Boshar MF, Cooper AD, Durica DS, Nagy A, Steffen D (1987) The sequence of a sea urchin muscle actin gene suggests a gene conversion with a cytoskeletal actin gene. J Mol Evol 25:37–45

    PubMed  Google Scholar 

  • Cupples CG, Pearlman RE (1986) Isolation and characterization of the actin gene fromTetrahymena thermophila. Proc Natl Acad Sci USA 83:5160–5164

    Google Scholar 

  • Deshler JO, Larson GP, Rossi JJ (1989)Kluyveromyces lactis maintainsSaccharomyces cerevisiae intron-encoded splicing signals. Mol Cell Biol 9:2208–2213

    PubMed  Google Scholar 

  • Dover GA (1987) DNA turnover and the molecular clock. J Mol Evol 26:47–58

    PubMed  Google Scholar 

  • Drouin G, Dover GA (1990) Independent gene evolution in the potato actin gene family demonstrated by phylogenetic procedures for resolving gene conversions and the phylogeny of angiosperm actin genes. J Mol Evol 31:132–150

    PubMed  Google Scholar 

  • Dudler R (1990) The single-copy actin gene ofPhytophthora megasperma encodes a protein considerably diverged from any other known actin. Plant Mol Biol 14:415–422

    PubMed  Google Scholar 

  • Edman U, Meza I, Agabian N (1987) Genomic and cDNA sequences from a virulent strain ofEntamoeba histolytica. Proc Natl Acad Sci USA 84:3024–3028

    PubMed  Google Scholar 

  • Fain SR, Druehl LD, Baillie DL (1988) Repeat and single copy sequences are differentially conserved in the evolution of kelp chloroplast DNA. J Phycol 24:292–302

    Google Scholar 

  • Fidel S, Doonan JH, Morris NR (1988)Aspergillus nidulans contains a single actin gene which has unique intron locations and encodes an actin. Gene 70:283–293

    PubMed  Google Scholar 

  • Fisher DA, Bode HR (1989) Nucleotide sequence of an actin-encoding gene fromHydra attenuata: structural characteristics and evolutionary implications. Gene 84:55–64.

    PubMed  Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees: a method based on mutation distances as estimated from cytochrome C sequences is of general applicability. Science 155:279–284

    PubMed  Google Scholar 

  • Fyrberg EA, Bond BJ, Hershey ND, Mixter KS, Davidson N (1981) The actin genes ofDrosophila: protein coding regions are highly conserved but intron positions are not. Cell 24: 107–116

    PubMed  Google Scholar 

  • Gerbi SA, Jeppesen C, Stebbins-Boaz B, Ares M Jr (1987) Evolution of eukaryotic rRNA: constraints imposed by RNA interactions. Cold Spring Harbor Symp Quant Biol 52:709–719

    PubMed  Google Scholar 

  • Gonzalez-y-Merchand JA, Cox RA (1988) Structure and expression of an actin gene ofPhysarum polycephalum. J Mol Biol 202:161–168

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Gunning P, Ponte P, Okayama H, Blau H, Kedes L (1983) Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol 3:787–795

    PubMed  Google Scholar 

  • Hancock JM, Dover GA (1988) Molecular coevolution among cryptically simple expansion segments of eukaryotic 26S/28S rRNAs. Mol Biol Evol 5:377–391

    Google Scholar 

  • Hancock JM, Dover GA (1990) Compensatory slippage' in the evolution of ribosomal RNA genes. Nucleic Acids Res 18: 5949–5954

    PubMed  Google Scholar 

  • Hightower RC, Meagher RB (1986) The molecular evolution of actin. Genetics 114:315–332

    PubMed  Google Scholar 

  • Hirono M, Endoh H, Okada N, Numata O, Watanabe Y (1987) Cloning and sequencing of theTetrahymena actin gene and identification of its gene product. J Mol Biol 194:181–192

    PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munoro HN (ed) Manual of protein metabolism. Academic Press, New York, p 21

    Google Scholar 

  • Kaine BP, Spear BB (1982) Nucleotide sequence of a macronuclear gene for actin inOxytricha fallax. Nature 295:430–432

    PubMed  Google Scholar 

  • Kamada S, Kukanaga T (1989) The nucleotide sequence of a human smooth muscle alpha-actin (aortic type) cDNA. Nucleic Acids Res 17:1767

    PubMed  Google Scholar 

  • Linares AR, Hancock JM, Dover GA (1991) Secondary structure constraints on the evolution ofDrosophila 28S ribosomal RNA expansion segments. J Mol Biol 219:381–390

    PubMed  Google Scholar 

  • Maleszka R, Clark-Walker GD (1990) Sequence of the gene for the cytoplasmic ribosomal RNA small subunit fromKluyveromyces lactis. Nucleic Acids Res 18:1889

    PubMed  Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY, p 197

    Google Scholar 

  • McElroy D, Rothenberg M, Wu R (1990) Structural characterization of a rice actin gene. Plant Mol Biol 14:163–171

    PubMed  Google Scholar 

  • McLean BG, Eubanks S, Meagher RB (1990) Tissue-specific expression of divergent actins in soybean root. Plant Cell 2: 335–344

    PubMed  Google Scholar 

  • Mertins P, Gallwitz D (1987) A single intronless actin gene in the fission yeastSchizosaccharomyces pombe: nucleotide sequence and transcripts formed in homologous and heterologous yeasts. Nucleic Acids Res 15:7369–7379

    PubMed  Google Scholar 

  • Mounier N, Gaillard J, Prudhomme J-C (1987) Nucleotide sequence of the coding region of two actin genes inBombyx mori. Nucleic Acids Res 15:2781

    PubMed  Google Scholar 

  • Nairn CJ, Winsett L, Ferl RJ (1988) Nucleotide sequence of an actin gene fromArabidopsis thaliana. Gene 65:247–257

    PubMed  Google Scholar 

  • Nellen W, Gallwitz D (1982) Actin genes and actin messenger RNA inAcanthamoeba castellanii: nucleotide sequence of the split actin gene. J Mol Biol 159:1–18

    PubMed  Google Scholar 

  • Neefs J-M, Van de Peer Y, Hendriks L, De Wachter R (1990) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 18S:2237–2319

    Google Scholar 

  • Ng R, Abelson J (1980) Isolation and sequence of the gene for actin inSaccharomyces cerevisiae. Proc Natl Acad Sci USA 77:3912–3916

    PubMed  Google Scholar 

  • Olsen GJ (1988) Phylogenetic analysis using ribosomal RNA. Methods Enzymol 164:793–812

    PubMed  Google Scholar 

  • Page FC (1987) The classification of ‘naked’ amoebae (Phylum Rhizopoda). Arch Protistenkd 133:199–217

    Google Scholar 

  • Ponte P, Ng S-Y, Engel J, Gunning P, Kedes L (1984) Evolutionary conservation in the untranslated regions of actin mRNAs: DNA sequences of a human beta-actin cDNA. Nucleic Acids Res 12:1687–1696

    PubMed  Google Scholar 

  • Romans P, Firtel RA (1985) Organization of the actin multigene family ofDictyostelium discoideum and analysis of variability in the protein coding regions. J Mol Biol 186:321–335

    PubMed  Google Scholar 

  • Scagel RF, Bandoni RJ, Maze JR, Rouse GE, Schofield WB, Stein JR (1982) Nonvascular plants: an evolutionary survey. Wadworth, Belmont, p 308

    Google Scholar 

  • Schuler MA, McOsker P, Keller EB (1983) DNA sequence of two linked actin genes of sea urchin. Mol Cell Biol 3:448–456

    PubMed  Google Scholar 

  • Shah DM, Hightower RC, Meagher RB (1983) Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not. J Mol Appl Genet 2:111–126

    PubMed  Google Scholar 

  • Sogin ML (1989) Evolution of eukaryotic organisms and their small subunit ribosomal RNAs. Am Zool 29:487–499

    Google Scholar 

  • Sogin ML (1991) The phylogenetic significance of sequence diversity and length variations in eukaryotic small subunit ribosomal RNA coding regions. In: Warren L, Koprowski H (eds) New perspectives on evolution. Wiley-Liss, New York, pp 175–188

    Google Scholar 

  • Sogin ML, Gunderson JH (1987) Structural diversity of eukaryotic small subunit ribosomal RNAs: evolutionary implications. In: Endocytobiology III. Ann NY Acad Sci 503:125–139

    PubMed  Google Scholar 

  • Sogin ML, Ingold A, Karlok M, Nielsen H, Engberg J (1986) Phylogenetic evidence for the acquisition of ribosomal RNA introns subsequent to the divergence of some of the majorTetrahymena groups. EMBO J 5:3625–3630

    PubMed  Google Scholar 

  • Sogin ML, Edman U, Elwood HJ (1989) A single kindgom of eukaryotes. In: Fernholm B, Bremer K, Jornvall H (eds) The hierarchy of life: molecules and morphology in phylogenetic analysis. Elsevier, New York, pp 133–143

    Google Scholar 

  • Swofford DL (1990) PAUP. Phylogenetic analysis using parsimony. Version 3.0. Illinois Natural History Survey, Champaign, p 117

    Google Scholar 

  • Vandekerckhove J, Weber K (1978) Mammalian cytoplasmic actins are the products of at least two genes and differ in primary structure in at least 25 identified positions from skeletal muscle actins. Proc Natl Acad Sci USA 75:1106–1110

    PubMed  Google Scholar 

  • Vandekerckhove J, Weber K (1979) The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle and rabbit slow skeletal muscle. Differentiation 14:123–133

    PubMed  Google Scholar 

  • Vandekerckhove J, Weber K (1984) Chordate muscle actins differ distinctly from invertebrate muscle actins. J Mol Biol 179:391–413

    PubMed  Google Scholar 

  • Wesseling JG, de Ree JM, Ponnudurai T, Smits MA, Schoenmakers JGG (1988) Nucleotide sequence and deduced amino acid sequence of aPlasmodium falciparum actin gene. Mol Biochem Parasitol 27:313–320

    PubMed  Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    PubMed  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Marine Biological Laboratory, Center for Molecular Evolution, 02543, Woods Hole, MA, USA

    Debashish Bhattacharya, Shawn K. Stickel & Mitchell L. Sogin

Authors
  1. Debashish Bhattacharya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shawn K. Stickel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitchell L. Sogin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhattacharya, D., Stickel, S.K. & Sogin, M.L. Molecular phylogenetic analysis of actin genic regions fromAchlya bisexualis (Oomycota) andCostaria costata (Chromophyta). J Mol Evol 33, 525–536 (1991). https://doi.org/10.1007/BF02102805

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02102805

Key words

Search

Navigation