Skip to main content
SpringerLink
Log in

Two different and functional nuclear rDNA genes in the abalone Haliotis tuberculata: tissue differential expression

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Analysis of the 18S rDNA sequences of Haliotis tuberculata tuberculata and H. t. coccinea subtaxa identified two different types of 18S rDNA genes and ITS1 regions. These two different genes were also detected in H. marmorata, H. rugosa and H. diversicolor that are separated from H. tuberculata by 5–65 mya. The mean divergence value between type I and type II sequences ranged from 7.25% for 18S to 80% for ITS1. ITS1 type II is homologous with the ITS1 consensus sequences published for many abalone species, whereas ITS1 type I presented only minor homology with a unique database entry for H. iris ITS1. A phylogenetic analysis makes a clear separation between type I and type II ITS1 sequences and supports grouping H. t. tuberculata, H. t. coccinea and H. marmorata together. The two subtaxa do not show any significant differences between the homologous 18S rDNA sequences. A general structure of the ITS1 transcript was proposed, with four major helices for the two types. The two genes were expressed and, for the first time, a putative differential expression of ITS1 type I was detected in the gills, digestive gland and gonads whereas ITS1 type II was expressed in all tissues.

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

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

Similar content being viewed by others

References

  • Aguilera-Muñoz F, Lafarga-Cruz F, Gallardo-Escárate C (2009) Análisis molecular de gastródos chilenos comerciales basado en secuencias de 16S ARNr, COI y ITS1-5.8S rDNA-ITS2. Gayana 73(1):17–27

    Google Scholar 

  • Altenheim B, Markl J, Lieb B (2002) Gene structure and hemocyanin isoform HtH2 from the mollusc Haliotis tuberculata indicate early and late intron hot spots. Gene 301:53–60

    Article  Google Scholar 

  • Arai K, Wilkins NP (1986) Chromosomes of Haliotis tuberculata L. Aquaculture 58:305–308

    Article  Google Scholar 

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer associates, Sunderland Mas, pp 38–61

    Google Scholar 

  • Benton MJ (1993) The fossil record 2. Chapman and Hall, Mondon, pp 125–270

    Google Scholar 

  • Bonnaud L, Saihi A, Boucher-Rodoni R (2002) Are 28S rDNA and 18S rDNA informative for cephalopod phylogeny? Bull Mar Sci 41(1):197–208

    Google Scholar 

  • Campo D, Machado-Schiaffino G, Horreo JL, Garcia-Vazquez E (2009) Molecular organization and evolution of 5S rDNA in the genus Merluccius and their phylogenetic implications. J Mol Evol 68(3):208–216

    Article  PubMed  CAS  Google Scholar 

  • Carranza S, Giribet G, Ribera J, Baguna J, Riutord M (1996) Evidence that two types of 18S rDNA coexist in the genome of Dugesia schmidtea (Plathelminthes, Turbellaria, Tricladida). Mol Biol Evol 13:824–832

    PubMed  CAS  Google Scholar 

  • Carranza S, Baguna J, Riutort M (1999) Origin and evolution of paralogous rDNA gene clusters within the flatworm family Dugesiidae (Platyhelminthes Tricladida). J Mol Evol 49:250–259

    Article  PubMed  CAS  Google Scholar 

  • Clark NL, Findlay GD, Michael XY, McCoss MJ, Swanson WJ (2007) Duplication and selection on abalone sperm lysin in an allopatric population. Mol Biol Evol 24(9):2081–2090

    Article  PubMed  CAS  Google Scholar 

  • Coleman AW (2009) Is there a molecular key to the level of “biological species” in eukaryotes? A DNA guide Mol. Phyl Evol 50:197–203

    Article  CAS  Google Scholar 

  • Coleman AW, Vacquier VD (2002) Exploring the phylogenetic utility of sequences for animals: a test case for abalone (Haliotis). J Mol Evol 54:246–257

    Article  PubMed  CAS  Google Scholar 

  • Coleman AW, Preparata RM, Mehrotra B, Mai JC (1998) Derivation of the secondary structure of the ITS-1 transcript in Volvocales and its taxonomical correlations. Protist 149:135–146

    Article  Google Scholar 

  • Craft JA, Gilbert JA, Temperton B, Dempsey KE, Ashelford K, Tivari B, Hutchinson TH, Chipman JK (2010) Pyrosequencing of Mytilus galloprovincialis cDNAs: tissue-specific expression pattern. PloS ONE 5:1–10

    Article  Google Scholar 

  • De Zoysa M, Wang I, Lee Y, Lee S, Lee JS, Lee J (2009) Transcriptional analysis of antioxydant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low salinity and hypoxic stress. Comp Biochem Physiol 154(4):387–395

    Article  Google Scholar 

  • Dover G, Coen E (1981) Springcleaning ribosomal DNA: a model for multigene evolution? Nature 290:731–732

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Estes JA, Lindberg DR, Wray C (2005) Evolution of large body size in abalones (Haliotis): patterns and implications. Paleobiology 31(4):591–606

    Google Scholar 

  • Franchini P, Slabbert R, Van Der Merwe M, Roux A, Roodt-Wilding R (2010) Karyotype and Genome Size Estimation of Haliotis midae: Estimators to Assist Future Studies on the Evolutionary History of Haliotidae. J Shellfish Res 29(4):945–950

    Article  Google Scholar 

  • Freire R, Arias A, Insua AM, Mendez J, Eirin-Lopez M (2010) Evolutionary dynamics of the 5S rDNA gene family in the mussel Mytilus: mixed effects of birth-and-death and concerted evolution. J Mol Evol 70(5):413–426

    Article  PubMed  CAS  Google Scholar 

  • Gallardo-Escararte C, Alvarez-Borego J, Rio-Portilla MA, Cross I, Merlo A, Rebordinos L (2005) Fluorescence in situ hybridization of rDNA, telomeric (TTAGGG)n and (GATA)n repeats in the red abalone Haliotis rufescens (Archaeogastropoda: Haliotidae). Hereditas 142:73–79

    Article  Google Scholar 

  • Geiger DL (1999) A total evidence cladistic analysis of the Haliotidae (Gastropoda vetigastropoda). PhD Uni South California, pp. 423

  • Geiger DL (2000) Distribution and biogeography of Haliotidae (Gastropoda: Vetigastropoda) Worldwide. Boll Malacologico 35:57–120

    Google Scholar 

  • Geiger DL, Poppe GT (2000) Haliotidae. In: Poppe GT, Groh K (eds) A conchological iconography. Conchbooks, Hackenheim, pp 66–89

    Google Scholar 

  • Ghatnekar L, Jaarola M, Bengtsson BO (2006) The introgression of a functional nuclear gene from Poa to Festuca ovina. Proc R Soc B 273:395–399

    Article  PubMed  CAS  Google Scholar 

  • Giribet G, Wheeler WC (2002) On bivalve phylogeny in a high-level analysis of the bivalvia (Mollusca) based on combined morphology and DNA sequence analysis. Invert Biol 121:271–324

    Article  Google Scholar 

  • Gottschling M, Hilger HH, Wolf M, Diane N (2001) Secondary structure of the ITS1 transcript and its application in a reconstruction of the phylogeny of Boroginales. Plant Biol 3:629–636

    Article  CAS  Google Scholar 

  • Graur D, Li WH (2000) Fundamentals of molecular evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  • Gunderson JH, Sogin ML, Wollett G, Hollingdale de la Cruz VF, Waters AP, McCutchan TF (1987) Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238:933–937

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Hannan KM, Hannan RD, Rothblum LI (1998) Transcription by RNA polymerase I. Front Biosci 3:376–398

    Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453

    Article  PubMed  CAS  Google Scholar 

  • Jaeger JA, Turner DH, Zucker M (1990) Predicting optimal and sub-optimal secondary structure for mRNA. Methods Enzymol 183:281–306

    Article  PubMed  CAS  Google Scholar 

  • Jarayabhand PLR, Yom R, Pogongviwat A (1998) Karyotypes of marine molluscs in the family Haliotidae found in Thailand. J Shellfish Res 17:761–764

    Google Scholar 

  • Jellen EN, Phillips RL, Rines HW (1994) Chromosomal localization and polymorphisms of ribosomal DNA in oat (Avena spp). Genome 37:23–32

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Ko KS, Jung HS (2002) Three nonorthologous IST types are present in a polypore fungus Trichaptum abietinum. Mol Phyl Evol 23:112–122

    Article  CAS  Google Scholar 

  • Komili S, Farny NG, Roth FP, Silver P (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131:557–571

    Article  PubMed  CAS  Google Scholar 

  • Krieger J, Fuerst PZ (2004) Diversity of nuclear 18S rRNA gene sequences within individuals in Lake sturgeon (Acipenseridae). J Appl Ichthyol 20:433–449

    Article  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 

  • Le Blancq SM, Khramtsov NV, Zamani F, Upton SJ, Wu TW (1997) Ribosomal RNA gene organization in Cryptosporidium parvum. Mol Biochem Parasitol 90:463–478

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Vacquier VD (1995) Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin. Mar Biol 124(2):267–278

    Article  CAS  Google Scholar 

  • Li J, Gutell RR, Damberger SH, Wirtz RA, Kissinger JC, Rogers MJ, Sattabongkot J, McCutchan TH (1997) Regulation and trafficking of three distinct 18S ribosomal RNAs during development of the malaria parasite. J Mol Biol 269:203–213

    Article  PubMed  CAS  Google Scholar 

  • Lieb B, Altenheim B, Markl J, Vincent A, van Olden E, van Holde KE, Miller KI (2001) Structure of two molluscan hemocyanin genes: significance for gene evolution. Proc Natl Acad Sco USA 98(8):4546–4551

    Article  CAS  Google Scholar 

  • Martins C, Galetti PM (2001) Organization of 5S rDNA in species of the fish Leporinus: two different genomic locations are characterized by distinct nontranscribed spacers. Genome 44:903–910

    PubMed  CAS  Google Scholar 

  • Merchant S et al (2007) The Chlamydomonas genome reveals the evolution of key animals and plant functions. Science 318:245–250

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Gu X, Sitnikova T (1997) Evolution ny the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 94:7799–7806

    Article  PubMed  CAS  Google Scholar 

  • Ohta T (1989) Role of gene duplication in evolution. Genome 31:304–310

    Article  PubMed  CAS  Google Scholar 

  • Ohta T (2000) Evolution of gene families. Gene 259:45–52

    Article  PubMed  CAS  Google Scholar 

  • Okumora S, Kinugawa S, Fujimaki A, Kawai W, Maehata H, Yoshioka K, Yoneda R, Yamamori K (1999) Analyse of karyotypes, chromosome banding and nucleolus organizer region of Pacific abalone, Haliotis discuss hannai (Archaeogastopoda: Haliotidae). J Shellfish Res 18:605–609

    Google Scholar 

  • Papillon D, Perez Y, Caubit X, Le Parco Y (2006) Systematics of Chaetognatha under the light of molecular data, using duplicated ribosomal DNA sequences. Mol Phyl Evol 38:621–634

    Article  CAS  Google Scholar 

  • Reedy R, Rothblum LI, Subrahmanyam CS (1983) The nucleotide sequence of 8S rRNA bound to preribosomal RNA of Novikoff Hepatoma. J Biol Chem 258:584–589

    Google Scholar 

  • Rogers MJ, Mc Conkey GA, Li J, Mc Cutchan TF (1995) The ribosomal rDNA in Plasmodium falciparum accumulates mutations independently. J Mol Biol 254:881–891

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP (2004) Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Mol Biol Evol 21(9):1704–1711

    Article  PubMed  CAS  Google Scholar 

  • Schulenburg JHG, Englisch U, Wagele JW (1999) Evolution of ITS1 rDNA in the Digenea (Platyheminthes: Trematoda): 3′ end sequence conservation and its phylogenetic utility. J Mol Evol 48:2–12

    Article  Google Scholar 

  • Schwarzpaul K, Beck LA (2002) Phylogeny of hydrothermal vent limpets (“Archaeogastropoda”) based on morphological and 18S rDNA data—preliminary results. Cahiers de Biologie Marine 43:381–385

    Google Scholar 

  • Streit K, Geiger DL, Lieb B (2006) Molecular phylogeny and the geographic origin of Haliotidae traced by hemocyanin sequences. J Molluscan Stud 72(1):105–110

    Google Scholar 

  • Subrahmanyam NC, Bryngelsson T, Hagberg P, Hagberg A (1994) Differential amplification of rDNA repeats in barley translocation and duplication lines: role of a specific segment. Hereditas 121:157–170

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4. Mol Biol Evol 24: 1996–1599

    Google Scholar 

  • Tröster H, Edström JE, Trendelenburg MF, Hofmann A (1990) Structural organization of Acheta rDNA: Evidence for differential amplification of soma and germ-line-specific rDNA sequences. J Mol Biol 216:533–543

    Article  PubMed  Google Scholar 

  • Vacquier VD, Swanson WJ, Lee YH (1997) Positive Darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? J Mol Evol 44:S15–S22

    Article  PubMed  CAS  Google Scholar 

  • van Holde KE, Miller KL (1995) Hemocyanins. Adv Prot Chem 47:1–81

    Article  Google Scholar 

  • van Nues RW, Rientjes JMJ, Morre SA, Mollec E, Planta RJ, Venema J, Raue HA (1995) Evolutionarily conserved structural elements are critical for processing of internal transcribed spacer 2 from Saccharomyces cerevicae precursor ribosomal RNA. J Mol Biol 250:24–36

    Article  PubMed  Google Scholar 

  • Van Wormhoudt A, Le Bras Y, Huchette S (2009) Haliotis marmorata from Senegal; a sister species of H tuberculata: Morphological and molecular evidence. Biochem Syst Ecol 37:747–757

    Article  Google Scholar 

  • Van Wormhoudt A, Roussel V, Courtois G, Huchette S (2010) Mitochondrial DNA recombination and paternal inheritability within Haliotis tuberculata sub-species. Mar Biotech 12:6 (on line 19/10/10) and (2011) 13(3):563–574

  • Vierna J, Gonzales-Tizon A, Martinez-Lage A (2009) Long-term evolution of S ribosomal DNA seems to be driven by birth-and-death processes and selection in Ensis razor shells (Mollusca: bivalvia). Biochem Genetics 47(9–10):635–644

    Article  CAS  Google Scholar 

  • Wang Y, Guo X (2004) Chromosal rearrangement in Pectinidae revealed by rRNA Loci and implications for Bivalve evolution. Biol Bull 207:247–256

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Ho KC, Yu DH, Ke CH, Mak WY, Chu KH (2004) Lack of genetic divergence in nuclear and mitochondrial DNA between subspecies of two Haliotis species. J Shellfish Res 23:1143–1146

    Google Scholar 

  • Wang S, Bao Z, Li N, Zhang L, Hu J (2007) Analysis of the secondary structure of ITS1 in Pectinidae: implications for phylogenetic reconstruction and structural evolution. Mar Biotech 9:231–242

    Article  CAS  Google Scholar 

  • Wesson DM, Porter CH, Collins FH (1992) Sequence and secondary structure comparisons of the ITS rDNA in mosquitoes (Diptera; Culicidae). Mol Phyl Evol 1:253–269

    Article  CAS  Google Scholar 

  • Zuber M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 3406–3415 (http://mfoldrnaalbanyedu/?q=mfold/RNA-Folding-Form)

Download references

Acknowledgments

This work was supported by the ECC (SUDEVAB n° 222156 “Sustainable development of European SMEs engaged in abalone aquaculture”). The sampling in the Canary Islands has been carried out by G. Courtois from the Canary Grupo de Investigación en Acuicultura (GIA). We thank Samuel Iglesias from the Museum for providing Haliotis diversicolor from Taiwan and Sebastien Trappe for providing Haliotis marmorata from Senegal.

Author information

Authors and Affiliations

  1. CNRS UMR 7208, Station de Biologie Marine du Muséum National d’Histoire Naturelle, 29900, Concarneau, France

    Alain Van Wormhoudt, Béatrice Gaume, Yvan Le Bras & Valérie Roussel

  2. France Haliotis, Kerazan, 29880, Plouguerneau, France

    Sylvain Huchette

Authors
  1. Alain Van Wormhoudt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Béatrice Gaume
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yvan Le Bras
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Valérie Roussel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sylvain Huchette
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alain Van Wormhoudt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Van Wormhoudt, A., Gaume, B., Le Bras, Y. et al. Two different and functional nuclear rDNA genes in the abalone Haliotis tuberculata: tissue differential expression. Genetica 139, 1217–1227 (2011). https://doi.org/10.1007/s10709-011-9623-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9623-8

Keywords

Search

Navigation