Skip to main content

Advertisement

Log in

Unique Mitogenomic Features in the Scleractinian Family Pocilloporidae (Scleractinia: Astrocoeniina)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The complete DNA sequences of three mitochondrial (mt) genomes were obtained from the scleractinian corals, Stylophora pistillata, Pocillopora damicornis, and Madracis mirabilis, and were compared to the published mt genomes to elucidate phylogenetically unique features of the family Pocilloporidae. The entire mt genomes of pocilloporid corals ranged from 16,951 to 17,425 bp with the A+T contents of their sense strands ranging from 68.4% to 70.2%. The gene order of protein-coding genes was identical to those of other scleractinian corals. The novel atp8 gene, first described in confamilial Seriatopora corals, was also confirmed using reverse transcription-polymerase chain reaction (RT-PCR), Northern blot, and sequence analyses in other genera of the Pocilloporidae. The intergenic spacer between atp6 and nad4, containing distinct repeated elements, conserved sequence blocks and domains, and functional structures, possesses typical characteristics of a putative control region for the four coral genera. A duplicated trnW, detected in the region close to the cox1 gene and which shares the highly conserved primary and secondary structures of its original counterpart, was discovered in both Seriatopora and Stylophora. These molecular characteristics are unique and provide the phylogenetic information for future evaluation of the status of the family Pocilloporidae in the evolutionary history of scleractinian corals.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Azuma N, Kunihiro Y, Sasaki J, Mihara E, Mihara Y, Yasunaga T, Jin D-H, Abe S (2008) Genetic variation and population structure of hair crab (Erimacrus isenbeckii) in Japan inferred from mitochondrial DNA sequence analysis. Mar Biotechnol 10:39–48

    Article  PubMed  CAS  Google Scholar 

  • Beagley CT, Okada NA, Wolstenholme DR (1996) Two mitochondiral group 1 introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc Natl Acad Sci USA 93:5619–5623

    Article  PubMed  CAS  Google Scholar 

  • Beagley CT, Okimoto R, Wolstenholme DR (1998) The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, a near-standard genetic code. Genetics 148:1091–1108

    PubMed  CAS  Google Scholar 

  • Beagley CT, Okimoto R, Wolstenholme DR (1999) Mytilus mitochondrial DNA contains a functional gene for a tRNASer(UCN) with a dihydrouridine arm-replacement loop and a pseudo-tRNASer(UCN) gene. Genetics 152:573–652

    Google Scholar 

  • Beaton MJ, Roger AJ, Cavalier-Smith T (1998) Sequence analysis of the mitochondrial genome of Sarcophyton glaucum: conserved gene order among octocorals. J Mol Evol 47:697–708

    Article  PubMed  CAS  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  PubMed  CAS  Google Scholar 

  • Blair D, Waycott M, Byrne L, Dunshea G, Smith-Keune C, Neil KM (2006) Molecular discrimination of Perna (Mollusca: Bivalvia) species using the polymerase chain reaction and species-specific mitochondrial primers. Mar Biotechnol 8:380–385

    Article  PubMed  CAS  Google Scholar 

  • Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780

    Article  PubMed  CAS  Google Scholar 

  • Boore JL, Brown WM (1994) Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138:423–443

    PubMed  CAS  Google Scholar 

  • Boore JL, Brown WM (1995) Complete sequence of the mitochondrial DNA of the annelid worm, Lumbricus terrestris. Genetics 141:305–319

    PubMed  CAS  Google Scholar 

  • Bridge D, Cunningham CW, Schierwater B, DeSalle R, Buss LW (1992) Class-level relationships in the phylum Cnidaria: evidence from mitochondrial genome structure. Proc Natl Acad Sci USA 89:8750–8753

    Article  PubMed  CAS  Google Scholar 

  • Brugler MR, France SC (2007) The complete mitochondrial genome of the black coral Chrysopathes formosa (Cnidaria:Anthozoa:Antipatharia) supports classification of antipatharians within the subclass Hexacorallia. Mol Phylogenet Evol 42:776–788

    Article  PubMed  CAS  Google Scholar 

  • Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Ecol Evol 19:709–716

    CAS  Google Scholar 

  • Burridge CP, Versace VL (2007) Population genetic structuring in Acanthopagrus butcheri (Pisces: Sparidae): does low gene flow among estuaries apply to both sexes? Mar Biotechnol 9:33–44

    Article  PubMed  CAS  Google Scholar 

  • Casane D, Dennebouy N, De-Rochambeau H, Mounolou JC, Monnerot M (1994) Genetic analysis of systematic mitochondrial heterplasmy in rabbits. Genetics 138:471–480

    PubMed  CAS  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    PubMed  CAS  Google Scholar 

  • Chen CA, Yu J-K (2000) Universal primers for amplification of mitochondrial small subunit ribosomal RNA-encoding gene in scleractinian corals. Mar Biotechnol 2:146–153

    Article  PubMed  CAS  Google Scholar 

  • Chen CA, Wallace CC, Wolstenholme J (2002) Analysis of the mitochondrial 12S rRNA gene supports a two-clade hypothesis of the evolutionary history of scleractinian corals. Mol Phylogenet Evol 23:137–149

    Article  PubMed  CAS  Google Scholar 

  • Chen C, Dai C-F, Fukami H, Knowlton N, Chen CA (2006) Evolutionary mitogenomics of pocilloporid corals: ATP8 gene loss, a novel open reading frame (ORF) and phylogenetic utility. First Asia Pacific Coral Reef Symposium, Hong Kong, p M39

  • Chen C, Dai C-F, Plathong S, Chiou C-Y, Chen CA (2008) The complete mitochondrial genomes of needle corals, Seriatopora spp. (Scleractinian; Pocilloporidae): an idiosyncratic atp8, duplicated trnW gene, and hypervariable regions used to determine species phylogenies and recently diverged populations. Mol Phylogenet Evol 46:19–33

    Article  PubMed  CAS  Google Scholar 

  • Cho E-S, Jung C-G, Sohn S-G, Kim C-W, Han S-J (2007) Population genetic structure of the ark shell Scapharca broughtonii Schrenck from Korea, China, and Russia based on COI gene sequences. Mar Biotechnol 9:203–216

    Article  PubMed  CAS  Google Scholar 

  • Chuang Y-Y (2006) Mitogenomics and molecular evolution of the group I intron in the cytochrome oxidase I gene of Siderastrea (Cnidaria; Scleractinia; Siderastreidae). Institute of Oceanography. National Taiwan University, Taipei, Taiwan

    Google Scholar 

  • Clayton DA (1991) Replication and transcription of animal mitochondrial DNA. Annu Rev Cell Biol 7:453–478

    Article  PubMed  CAS  Google Scholar 

  • Clayton DA (1992) Transcription and replication of animal mitochondrial DNAs. Int Rev Cytol 141:217–232

    Article  PubMed  CAS  Google Scholar 

  • Devenish RJ, Papakonstantinou T, Galanis M, Law RH, Linnane AW, Nagley P (1992) Structure/function analysis of yeast mitochondrial ATP synthase subunit 8. Ann NY Acad Sci 671:403–414

    Article  PubMed  CAS  Google Scholar 

  • Di Giulio M (1992) On the origin of the transfer RNA molecule. J Theor Biol 159:199–214

    Article  PubMed  Google Scholar 

  • Di Giulio M (2004) The origin of the tRNA molecule: implications for the origin of protein synthesis. J Theor Biol 226:89–93

    Article  PubMed  CAS  Google Scholar 

  • Flot J-F, Tillier S (2007) The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: the putative D-loop and a novel ORF of unknown function. Gene 401:80–87

    Article  PubMed  CAS  Google Scholar 

  • Fukami H, Knowlton N (2005) Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis coral species complex (Cnidaria, Anthozoa, Scleractinia). Coral Reefs 24:410–417

    Article  Google Scholar 

  • Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324–337

    PubMed  CAS  Google Scholar 

  • Gish W, States DJ (1993) Identification of protein coding regions by database similarity search. Nat Genet 3:266–272

    Article  PubMed  CAS  Google Scholar 

  • Gissi C, Pesole G (2003) Transcript mapping and genome annotation of ascidian mtDNA using EST data. Genome Res 13:2203–2212

    Article  PubMed  CAS  Google Scholar 

  • Gissi C, Iannelli F, Pesole G (2004) Complete mtDNA of Ciona intestinalis reveals extensive gene rearrangement and the presence of an atp8 and an extra trnM gene in ascidians. J Mol Biol 58:376–389

    CAS  Google Scholar 

  • Glynn PW (1976) Some physical and biological determinants of coral community structure in the eastern Pacific. Ecol Monogr 46:431–456

    Article  Google Scholar 

  • Gonnet GH, Cohen MA, Benner SA (1992) Exhaustive matching of the entire protein sequence database. Science 256:1443–1445

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Lang BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn TG, Plante I, Rioux P, Saint-Louis D, Zhu Y, Burger G (1998) Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res 26:865–878

    Article  PubMed  CAS  Google Scholar 

  • Grigg RW, Maragos JE (1974) Recolonization of hermatypic corals on submerged larva flows in Hawaii. Ecology 55:387–395

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • He Y, Jones J, Armstrong M, Lamberti F, Moens M (2005) The mitochondrial genome of Xiphinema americanum sensu stricto (Nematoda: Enoplea): considerable economization in the length and structural features of encoded genes. J Mol Biol 61:819–883

    CAS  Google Scholar 

  • Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412

    PubMed  CAS  Google Scholar 

  • Hu M, Chilton NB, Gasser RB (2003) The mitochondrial genome of Strongyloides stercoralis (Nematoda)-idiosyncratic gene order and evolutionary implications. Int J Parasitol 33:1393–1408

    Article  PubMed  CAS  Google Scholar 

  • Ikeguchi K, Ineno T, Itoi S, Kondo H, Kinoshita S, Watabe S (2006) Increased levels of mitochondrial gene transcripts in the thermally selected rainbow trout (Oncorhynchus mykiss) strain during embryonic development. Mar Biotechnol 8:178–188

    Article  PubMed  CAS  Google Scholar 

  • Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Paabo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256

    PubMed  CAS  Google Scholar 

  • Kayal E, Lavrov DV (2008) The mitochondrial genome of Hydra oligactis (Cnidaria, Hydrozoa) sheds new light on animal mtDNA evolution and cnidarian phylogeny. Gene 410:177–186

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydrophobic character of a protein. J Mol Biol 157:105–142

    Article  PubMed  CAS  Google Scholar 

  • Lavrov DV, Brown WM (2001) Trichinella spiralis mtDNA: a nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAs and has a gene arrangement relatable to those of coelomate metazoans. Genetics 157:621–637

    PubMed  CAS  Google Scholar 

  • Le TH, Blair D, Agatsuma T, Humair P-F, Campbell NJH, Iwagami M, Littlewood DTJ, Peacock B, Johnson DA, Bartley J, Rollinson D, Herniou EA, Zarlenga DS, McManus DP (2000) Phylogenies inferred from mitochondrial gene orders-a cautionary tale from the parasitic flatworms. Mol Biol Evol 17:1123–1125

    PubMed  CAS  Google Scholar 

  • Lin G, Lo LC, Zhu ZY, Feng F, Chou R, Yue GH (2006) The complete mitochondrial genome sequence and characterization of single-nucleotide polymorphisms in the control region of the Asian seabass (Lates calcarifer). Mar Biotechnol 8:71–79

    Article  PubMed  CAS  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  PubMed  CAS  Google Scholar 

  • Loya Y (1976) The Red Sea coral Stylophora pistillata is an r strategist. Nature 259:478–480

    Article  Google Scholar 

  • Mahidol C, Na-Nakorn U, Sukmanomon S, Taniguchi N, Nguyen TTT (2007) Mitochondrial DNA diversity of the Asian moon scallop, Amusium pleuronectes (Pectinidae), in Thailand. Mar Biotechnol 9:352–359

    Article  PubMed  CAS  Google Scholar 

  • Majoros WH (2007) Methods for computational gene prediction. Cambridge Univ. Press, Cambridge

    Google Scholar 

  • Masta SE (2000) Mitochondrial sequence evolution in spiders: intraspecific variation in tRNAs lacking the TYC arm. Mol Biol Evol 17:1091–1100

    PubMed  CAS  Google Scholar 

  • Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL (2006) Naked corals: skeleton loss in scleractinia. Proc Natl Acad Sci USA 103:9096–9100

    Article  PubMed  CAS  Google Scholar 

  • Milbury CA, Gaffiney PM (2005) Complete mitochondrial DNA sequence of the eastern oyster Crassostrea virginica. Mar Biotechnol 7:697–612

    Article  PubMed  CAS  Google Scholar 

  • Moriya S, Sato S, Azumaya T, Suzuki O, Urawa S, Urano A, Abe S (2007) Genetic stock identification of chum salmon in the Bering Sea and North Pacific Ocean using mitochondrial DNA microarray. Mar Biotechnol 9:179–191

    Article  PubMed  CAS  Google Scholar 

  • Papakonstantinou T, Galanis M, Nagley P, Devenish RJ (1993) Each of three positively-charged amino acids in the C-terminal region of yeast mitochondrial ATP synthase subunit 8 is required for assembly. Biochim Biophys Acta 1144:22–32

    Article  PubMed  CAS  Google Scholar 

  • Papakonstantinou T, Law RH, Nagley P, Devenish RJ (1996) Non-functional variants of yeast mitochondrial ATP synthase subunit 8 that assemble into the complex. Biochem Mol Biol Int 39:253–260

    PubMed  CAS  Google Scholar 

  • Pont-Kingdon GA, Okada NA, Macfarlane JL, Beagley CT, Wolstenholme DR (1995) A coral mitochondrial mutS gene. Nature 375:109–111

    Article  PubMed  CAS  Google Scholar 

  • Pont-Kingdon G, Okada NA, Macfarlane JL, Beagley CT, Watkins-Sims CD, Cavalier-Smith T, Clark-Walker GD, Wolstenholme DR (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46:419–431

    Article  PubMed  CAS  Google Scholar 

  • Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642

    Article  CAS  Google Scholar 

  • Romano SL, Palumbi SR (1997) Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. J Mol Evol 45:397–411

    Article  PubMed  CAS  Google Scholar 

  • Saito S, Tamura K, Aotsuka T (2005) Replication origin of mitochondrial DNA in insects. Genetics 171:1695–1705

    Article  PubMed  CAS  Google Scholar 

  • Shadel GS, Clayton DA (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66:409–435

    Article  PubMed  CAS  Google Scholar 

  • Shao Z, Graf S, Chaga OY, Lavrov DV (2006) Mitochondrial genome of the moon jelly Aurelia aurita (Cnidaria, Scyphozoa): a linear DNA molecule encoding a putative DNA-dependent DNA polymerase. Gene 381:92–101

    Article  PubMed  CAS  Google Scholar 

  • Shearer TL, van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487

    Article  PubMed  CAS  Google Scholar 

  • Sinniger F, Chevaldonné P, Pawlowski J (2007) Mitochondrial genome of Savalia savaglia (Cnidaria, Hexacorallia) and early metazoan phylogeny. J Mol Evol 64:196–203

    Article  PubMed  CAS  Google Scholar 

  • Stolarski J, Roniewicz E (2001) Towards a new synthesis of evolutionary relationships and classification of scleractinia. J Paleontol 75:1090–1108

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tseng C-C, Wallace CC, Chen CA (2005) Mitogenomic analysis of Montipora cactus and Anacropora matthai (cnidaria; scleractinia; acroporidae) indicates an unequal rate of mitochondrial evolution among Acroporidae corals. Coral Reefs 2005:502–508

    Article  Google Scholar 

  • van Oppen MJH, Willis BL, Miller DJ (1999) Atypical low rate of cytochrome b evolution in the scleractinian coral genus Acropora. Proc R Soc Lond B Biol Sci 266:179–183

    Article  Google Scholar 

  • van Oppen MJH, Catmull J, McDonald BJ, Hislop NR, Hagerman PJ, Miller DJ (2002) The mitochondrial genome of Acropora tenuis (Cnidaria; Scleractinia) contains a large group 1 intron and a candidate control region. J Mol Evol 55:1–13

    Article  PubMed  CAS  Google Scholar 

  • Vaughan TW, Wells JW (1943) Revision of the suborders, families, and genera of the Scleractinia. Geol Soc Am Spec Pap 44:1–363

    Google Scholar 

  • Veron JEN (1995) Corals in space and time: The biogeography and evolution of the scleractinian. University of new South Wales Press, Sydney

    Google Scholar 

  • Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Queensland, Australia

    Google Scholar 

  • Veron JEN, Pichon M (1976) Scleractinia of Eastern Australia. Part I. Thamnasteriidae, Astrocoeniidae and Pocilloporidae. Aust Inst Mar Sci Monogr 1:1–86

    Google Scholar 

  • Wallace CC (1985) Seasonal peaks and annual fluctuations in recruitment of juvenile scleractinian corals. Mar Ecol Prog Ser 21:289–298

    Article  Google Scholar 

  • Wells JW (1956) Scleractinia. In: Moore RC (ed) Treatise on invertebrate paleontolohy, coelenterata. Geological Society of America and University of Kansas Press, pp 328–440

  • Wilkinson GS, Mayer F, Kerth G, Petri B (1997) Evolution of repeated sequence arrays in the D-loop region of bat mitochondrial DNA. Genetics 146:1035–1048

    PubMed  CAS  Google Scholar 

  • Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141:173–216

    Article  PubMed  CAS  Google Scholar 

  • Wolstenholme DR, MacFarlane JL, Okimoto R, Clary DO, Wahleithner JA (1987) Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci USA 84:1324–1328

    Article  PubMed  CAS  Google Scholar 

  • Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3253

    Article  PubMed  CAS  Google Scholar 

  • Yokobori S-i, Ueda T, Feldmaier-Fuchs G, Pääbo S, Ueshima R, Kondow A, Nishikawa K, Watanabe K (1999) Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata). Genetics 153:1851–1862

    PubMed  CAS  Google Scholar 

  • Zuker M (2000) Calculating nucleic acid secondary structure. Curr Opin Struct Biol 10:303–310

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Drs. Hironobu Fukami and Nancy Knowlton for initiating this study and their encouragement, members of the Evolutionary and Ecology Genetics of Coral Reef Discussion Group, Research Center for Biodiversity, Academia Sinica and two anonymous referees for constructive comments. This work was supported by Academia Sinica Thematic Grants (2002–2004), a grant from the Genomic Research Center, Academia Sinica (2006–2007), and a National Science Council (NSC) grant (NSC94-2621-B-001-005), Taiwan to C.A.C., and an NSC grant (NCS94-EPA-Z002-004) to C.-F. Dai. This is the Evolutionary and Ecology Genetics of Coral Reef Group, RCBAS contribution no. 44.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chaolun Allen Chen.

Electronic supplementary material

Appendices are available at Marine Biotechnology online (xxx).

10126_2008_9093_MOESM1_ESM.doc

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, C., Chiou, CY., Dai, CF. et al. Unique Mitogenomic Features in the Scleractinian Family Pocilloporidae (Scleractinia: Astrocoeniina). Mar Biotechnol 10, 538–553 (2008). https://doi.org/10.1007/s10126-008-9093-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-008-9093-x

Keywords

Navigation