Advertisement

Genetica

, Volume 139, Issue 10, pp 1217–1227 | Cite as

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

  • Alain Van WormhoudtEmail author
  • Béatrice Gaume
  • Yvan Le Bras
  • Valérie Roussel
  • Sylvain Huchette
Article

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.

Keywords

Abalone Haliotis Two different rDNA genes Differential expression 

Notes

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.

References

  1. 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):17–27Google Scholar
  2. 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 301:53–60CrossRefGoogle Scholar
  3. Arai K, Wilkins NP (1986) Chromosomes of Haliotis tuberculata L. Aquaculture 58:305–308CrossRefGoogle Scholar
  4. Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer associates, Sunderland Mas, pp 38–61Google Scholar
  5. Benton MJ (1993) The fossil record 2. Chapman and Hall, Mondon, pp 125–270Google Scholar
  6. Bonnaud L, Saihi A, Boucher-Rodoni R (2002) Are 28S rDNA and 18S rDNA informative for cephalopod phylogeny? Bull Mar Sci 41(1):197–208Google Scholar
  7. 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):208–216PubMedCrossRefGoogle Scholar
  8. 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 13:824–832PubMedGoogle Scholar
  9. 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 49:250–259PubMedCrossRefGoogle Scholar
  10. 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):2081–2090PubMedCrossRefGoogle Scholar
  11. Coleman AW (2009) Is there a molecular key to the level of “biological species” in eukaryotes? A DNA guide Mol. Phyl Evol 50:197–203CrossRefGoogle Scholar
  12. Coleman AW, Vacquier VD (2002) Exploring the phylogenetic utility of sequences for animals: a test case for abalone (Haliotis). J Mol Evol 54:246–257PubMedCrossRefGoogle Scholar
  13. 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 149:135–146CrossRefGoogle Scholar
  14. 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 5:1–10CrossRefGoogle Scholar
  15. 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):387–395CrossRefGoogle Scholar
  16. Dover G, Coen E (1981) Springcleaning ribosomal DNA: a model for multigene evolution? Nature 290:731–732PubMedCrossRefGoogle Scholar
  17. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  18. Estes JA, Lindberg DR, Wray C (2005) Evolution of large body size in abalones (Haliotis): patterns and implications. Paleobiology 31(4):591–606Google Scholar
  19. 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):945–950CrossRefGoogle Scholar
  20. 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):413–426PubMedCrossRefGoogle Scholar
  21. 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 142:73–79CrossRefGoogle Scholar
  22. Geiger DL (1999) A total evidence cladistic analysis of the Haliotidae (Gastropoda vetigastropoda). PhD Uni South California, pp. 423Google Scholar
  23. Geiger DL (2000) Distribution and biogeography of Haliotidae (Gastropoda: Vetigastropoda) Worldwide. Boll Malacologico 35:57–120Google Scholar
  24. Geiger DL, Poppe GT (2000) Haliotidae. In: Poppe GT, Groh K (eds) A conchological iconography. Conchbooks, Hackenheim, pp 66–89Google Scholar
  25. Ghatnekar L, Jaarola M, Bengtsson BO (2006) The introgression of a functional nuclear gene from Poa to Festuca ovina. Proc R Soc B 273:395–399PubMedCrossRefGoogle Scholar
  26. 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 121:271–324CrossRefGoogle Scholar
  27. 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 3:629–636CrossRefGoogle Scholar
  28. Graur D, Li WH (2000) Fundamentals of molecular evolution. Sinauer Associates, SunderlandGoogle Scholar
  29. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704PubMedCrossRefGoogle Scholar
  30. 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 238:933–937PubMedCrossRefGoogle Scholar
  31. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  32. Hannan KM, Hannan RD, Rothblum LI (1998) Transcription by RNA polymerase I. Front Biosci 3:376–398Google Scholar
  33. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453PubMedCrossRefGoogle Scholar
  34. Jaeger JA, Turner DH, Zucker M (1990) Predicting optimal and sub-optimal secondary structure for mRNA. Methods Enzymol 183:281–306PubMedCrossRefGoogle Scholar
  35. Jarayabhand PLR, Yom R, Pogongviwat A (1998) Karyotypes of marine molluscs in the family Haliotidae found in Thailand. J Shellfish Res 17:761–764Google Scholar
  36. Jellen EN, Phillips RL, Rines HW (1994) Chromosomal localization and polymorphisms of ribosomal DNA in oat (Avena spp). Genome 37:23–32PubMedCrossRefGoogle Scholar
  37. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  38. Ko KS, Jung HS (2002) Three nonorthologous IST types are present in a polypore fungus Trichaptum abietinum. Mol Phyl Evol 23:112–122CrossRefGoogle Scholar
  39. Komili S, Farny NG, Roth FP, Silver P (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131:557–571PubMedCrossRefGoogle Scholar
  40. Krieger J, Fuerst PZ (2004) Diversity of nuclear 18S rRNA gene sequences within individuals in Lake sturgeon (Acipenseridae). J Appl Ichthyol 20:433–449CrossRefGoogle Scholar
  41. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  42. Le Blancq SM, Khramtsov NV, Zamani F, Upton SJ, Wu TW (1997) Ribosomal RNA gene organization in Cryptosporidium parvum. Mol Biochem Parasitol 90:463–478PubMedCrossRefGoogle Scholar
  43. Lee YH, Vacquier VD (1995) Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin. Mar Biol 124(2):267–278CrossRefGoogle Scholar
  44. 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 269:203–213PubMedCrossRefGoogle Scholar
  45. 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):4546–4551CrossRefGoogle Scholar
  46. 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 44:903–910PubMedGoogle Scholar
  47. Merchant S et al (2007) The Chlamydomonas genome reveals the evolution of key animals and plant functions. Science 318:245–250PubMedCrossRefGoogle Scholar
  48. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152PubMedCrossRefGoogle Scholar
  49. 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 94:7799–7806PubMedCrossRefGoogle Scholar
  50. Ohta T (1989) Role of gene duplication in evolution. Genome 31:304–310PubMedCrossRefGoogle Scholar
  51. Ohta T (2000) Evolution of gene families. Gene 259:45–52PubMedCrossRefGoogle Scholar
  52. 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 18:605–609Google Scholar
  53. 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 38:621–634CrossRefGoogle Scholar
  54. Reedy R, Rothblum LI, Subrahmanyam CS (1983) The nucleotide sequence of 8S rRNA bound to preribosomal RNA of Novikoff Hepatoma. J Biol Chem 258:584–589Google Scholar
  55. Rogers MJ, Mc Conkey GA, Li J, Mc Cutchan TF (1995) The ribosomal rDNA in Plasmodium falciparum accumulates mutations independently. J Mol Biol 254:881–891PubMedCrossRefGoogle Scholar
  56. Rooney AP (2004) Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Mol Biol Evol 21(9):1704–1711PubMedCrossRefGoogle Scholar
  57. 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 48:2–12CrossRefGoogle Scholar
  58. Schwarzpaul K, Beck LA (2002) Phylogeny of hydrothermal vent limpets (“Archaeogastropoda”) based on morphological and 18S rDNA data—preliminary results. Cahiers de Biologie Marine 43:381–385Google Scholar
  59. Streit K, Geiger DL, Lieb B (2006) Molecular phylogeny and the geographic origin of Haliotidae traced by hemocyanin sequences. J Molluscan Stud 72(1):105–110Google Scholar
  60. 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 121:157–170CrossRefGoogle Scholar
  61. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4. Mol Biol Evol 24: 1996–1599Google Scholar
  62. 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 216:533–543PubMedCrossRefGoogle Scholar
  63. 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–S22PubMedCrossRefGoogle Scholar
  64. van Holde KE, Miller KL (1995) Hemocyanins. Adv Prot Chem 47:1–81CrossRefGoogle Scholar
  65. 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 250:24–36PubMedCrossRefGoogle Scholar
  66. 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 37:747–757CrossRefGoogle Scholar
  67. 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):563–574Google Scholar
  68. 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):635–644CrossRefGoogle Scholar
  69. Wang Y, Guo X (2004) Chromosal rearrangement in Pectinidae revealed by rRNA Loci and implications for Bivalve evolution. Biol Bull 207:247–256PubMedCrossRefGoogle Scholar
  70. 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 23:1143–1146Google Scholar
  71. 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 9:231–242CrossRefGoogle Scholar
  72. Wesson DM, Porter CH, Collins FH (1992) Sequence and secondary structure comparisons of the ITS rDNA in mosquitoes (Diptera; Culicidae). Mol Phyl Evol 1:253–269CrossRefGoogle Scholar
  73. 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)

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Alain Van Wormhoudt
    • 1
    Email author
  • Béatrice Gaume
    • 1
  • Yvan Le Bras
    • 1
  • Valérie Roussel
    • 1
  • Sylvain Huchette
    • 2
  1. 1.CNRS UMR 7208, Station de Biologie Marine du Muséum National d’Histoire NaturelleConcarneauFrance
  2. 2.France HaliotisPlouguerneauFrance

Personalised recommendations