期刊论文详细信息
Molecular Cytogenetics
Divergent evolutionary behavior of H3 histone gene and rDNA clusters in venerid clams
Juan J. Pasantes1  Paloma Morán1  Concepción Pérez-García1  Daniel García-Souto1 
[1] Departamento Bioquímica, Xenética e Inmunoloxía, Universidade de Vigo, Vigo, E-36310, Spain
关键词: Ribosomal RNA genes;    Histone genes;    Fluorescent in situ hybridization;    Chromosome;    Venerid clams;   
Others  :  1221601
DOI  :  10.1186/s13039-015-0150-7
 received in 2015-05-08, accepted in 2015-06-09,  发布年份 2015
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【 摘 要 】

Background

Histone H3 gene clusters have been described as highly conserved chromosomal markers in invertebrates. Surprisingly, in bivalves remarkable interspecific differences were found among the eight mussels and between the two clams in which histone H3 gene clusters have already been located. Although the family Veneridae comprises 10 % of the species of marine bivalves, their chromosomes are poorly studied. The clams belonging to this family present 2n = 38 chromosomes and similar karyotypes showing chromosome pairs gradually decreasing in length. In order to assess the evolutionary behavior of histone and rRNA multigene families in bivalves, we mapped histone H3 and ribosomal RNA probes to chromosomes of ten species of venerid clams.

Results

In contrast with the reported conservation of histone H3 gene clusters and their intercalary location in invertebrates, these loci varied in number and were mostly subterminal in venerid clams. On the other hand, while a single 45S rDNA cluster, highly variable in location, was found in these organisms, 5S rDNA clusters showed interspecific differences in both number and location. The distribution patterns of these sequences were species-specific and mapped to different chromosomal positions in all clams but Ruditapes decussatus, in which one of the minor rDNA clusters and the major rDNA cluster co-located.

Conclusion

The diversity in the distribution patterns of histone H3 gene, 5S rDNA and 28S rDNA clusters found in venerid clams, together with their different evolutionary behaviors in other invertebrate taxa, strongly suggest that the control of the spreading of these multigene families in a group of organisms relies upon a combination of evolutionary forces that operate differently depending not only on the specific multigene family but also on the particular taxa. Our data also showed that H3 histone gene and rDNA clusters are useful landmarks to integrate nex-generation sequencing (NGS) and evolutionary genomic data in non-model species.

【 授权许可】

   
2015 García-Souto et al.

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【 参考文献 】
  • [1]Kedes LH. Histone genes and histone messengers. Annu Rev Biochem. 1979; 48:837-70.
  • [2]Long EO, Dawid IB. Repeated genes in eukaryotes. Annu Rev Biochem. 1980; 49:727-64.
  • [3]Eirín-López JM, González-Romero R, Dryhurst D, Méndez J, Ausió J. Long-term evolution of histone families: old notions and new insights into their mechanisms of diversification across eukaryotes. In: Evolutionary Biology. Pontarotti P, editor. Springer, Berlin; 2009: p.139-62.
  • [4]Drouin G, Moniz-de-Sá M. The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Mol Biol Evol. 1995; 12:481-93.
  • [5]Cabrero J, López-León MD, Teruel M, Camacho JPM. Chromosome mapping of H3 and H4 histone gene clusters in 35 species of acridid grasshoppers. Chromosome Res. 2009; 17:397-404.
  • [6]Cabral-de-Mello DC, Cabrero J, López-León MD, Camacho JPM. Evolutionary dynamics of 5S rDNA location in acridid grasshoppers and its relationship with H3 histone gene and 45S rDNA location. Genetica. 2011; 139:921-31.
  • [7]Cabral-de-Mello DC, Moura RC, Martins C. Cytogenetic mapping of rRNAs and histone H3 genes in 14 species of Dichotomius (Coleoptera, Scarabaeidae, Scarabaeinae) beetles. Cytogenet Genome Res. 2011; 134:127-35.
  • [8]Cabral-de-Mello DC, Oliveira SG, de Moura RC, Martins C. Chromosomal organization of the 18S and 5S rRNAs and histone H3 genes in Scarabaeinae coleopterans: insights into the evolutionary dynamics of multigene families and heterochromatin. BMC Genet. 2011; 12:88. BioMed Central Full Text
  • [9]Mandrioli M, Manicardi GC. Chromosomal mapping reveals a dynamic organization of the histone genes in aphids (Hemiptera: Aphididae). Entomología. 2013; 1:e2.
  • [10]Šíchová J, Nguyen P, Dalíková M. Marec F (2013) Chromosomal evolution in tortricid moths: Conserved karyotypes with diverged features. PLoS One. 2013; 8(5):e64520.
  • [11]Drabent B, Kim JS, Albig W, Prats E, Cornudella L, Doenecke D. Mytilus edulis histone gene clusters containing only H1 genes. J Mol Evol. 1999; 49:645-55.
  • [12]Albig W, Warthorst U, Drabent B, Prats E, Cornudella L, Doenecke D. Mytilus edulis core histone genes are organized in two clusters devoid of linker histone genes. J Mol Evol. 2003; 56:597-606.
  • [13]Eirín-López JM, González-Tizón AM, Martínez A, Méndez J. Molecular and evolutionary analysis of mussel histone genes (Mytilus spp): possible evidence of an “orphon origin” for H1 histone genes. J Mol Evol. 2002; 55:272-83.
  • [14]Eirín-López JM, Ruiz MF, González-Tizón AM, Martínez A, Sánchez L, Méndez J. Molecular evolutionary characterization of the mussel Mytilus histone multigene family: first record of a tandemly repeated unit of a five histone genes containing an H1 subtype whit “orphon” features. J Mol Evol. 2004; 58:131-44.
  • [15]Li C, Song L, Zhao J, Zou H, Su J, Zhang H. Genomic organization, nucleotide sequence analysis of the core histone genes cluster in Chlamys farreri and molecular evolution assessment of the H2A and H2B. DNA Seq. 2006; 17:440-51.
  • [16]González-Romero R, Ausió J, Méndez J, Eirín-López JM. Early evolution of histone genes: Prevalence of an ‘orphon’ H1 lineage in Protostomes and birth-and-death process in the H2A family. J Mol Evol. 2008; 66:505-18.
  • [17]Pérez-García C, Cambeiro JM, Morán P, Pasantes JJ. Chromosomal mapping of rDNAs, core histone genes and telomeric sequences in Perumytilus purpuratus (Bivalvia: Mytilidae). J Exp Mar Biol Ecol. 2010; 395:199-205.
  • [18]Pérez-García C, Guerra-Varela J, Morán P, Pasantes JJ. Chromosomal mapping of rRNA genes, core histone genes and telomeric sequences in Brachidontes puniceus and Brachidontes rodriguezi (Bivalvia: Mytilidae). BMC Genet. 2010; 11:109. BioMed Central Full Text
  • [19]Pérez-García C, Morán P, Pasantes JJ. Cytogenetic characterization of the invasive mussel species Xenostrobus securis Lmk. (Bivalvia: Mytilidae). Genome. 2011; 54:771-8.
  • [20]Pérez-García C, Morán P, Pasantes JJ. Karyotypic diversification in Mytilus mussels (Bivalvia: Mytilidae) inferred from chromosomal mapping of rRNA and histone gene clusters. BMC Genet. 2014; 15:84. BioMed Central Full Text
  • [21]Zhang L, Bao Z, Wang S, Huang X, Hu J. Chromosome rearrangements in Pectinidae (Bivalvia; Pteriomorphia) implied based on chromosomal localization of histone H3 gene in four scallops. Genetica. 2007; 130:193-8.
  • [22]Bouilly K, Chaves R, Fernandes M, Guedes-Pinto H. Histone H3 gene in the Pacific oyster, Crassostrea gigas Thunberg, 1793: molecular and cytogenetic characterisations. Comp Cytogen. 2010; 4:111-21.
  • [23]Carrilho J, Pérez-García C, Leitão A, Malheiro I, Pasantes JJ. Cytogenetic characterization and mapping of rDNAs, core histone genes and telomeric sequences in Venerupis aurea and Tapes rhomboides (Bivalvia: Veneridae). Genetica. 2011; 139:823-30.
  • [24]Huber M. Compendium of bivalves. A full-color guide to 3300 of the world’s marine bivalves. A status on Bivalvia after 250 years of research. ConchBooks, Hackenheim; 2010.
  • [25]Canapa A, Marota I, Rollo F, Olmo E. Phylogenetic analysis of Veneridae (Bivalvia): comparison of molecular and paleontological data. J Mol Evol. 1996; 43:517-22.
  • [26]Canapa A, Schiaparelli S, Marota I, Barucca M. Molecular data from the 16S rRNA gene for the phylogeny of Veneridae. Mar Biol. 2003; 142:1125-30.
  • [27]Kappner I, Bieler R. Phylogeny of venus clams (Bivalvia: Venerinae) as inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol. 2006; 40:317-31.
  • [28]Mikkelsen PM, Bieler R, Kappner I, Rawlings TA. Phylogeny of Veneroidea (Mollusca: Bivalvia) based on morphology and molecules. Zool J Linnean Soc. 2006; 148:439-521.
  • [29]Chen J, Li Q, Kong L, Zheng X. Molecular phylogeny of venus clams (Mollusca, Bivalvia, Veneridae) with emphasis on the on the systematic position of taxa along the coast of mainland China. Zoologica Scripta. 2011; 40:260-71.
  • [30]Thiriot-Quiévreux C. Advances in cytogenetics of aquatic organisms. In: Genetics and evolution of aquatic organisms. Beaumont AR, editor. Chapman and Hall, London; 1994: p.369-88.
  • [31]Thiriot-Quiévreux C. Review of the literature on bivalve cytogenetics in the last ten years. Cah Biol. 2002; 43:17-26.
  • [32]Ebied ABM, Aly FM. Cytogenetic studies on metaphase chromosomes of six bivalve species of families Mytilidae and Veneridae (Nucinelloidea, Mollusca). Cytologia. 2004; 69:261-73.
  • [33]Leitão A, Chaves R, Matias D, Joaquim S, Ruano F, Guedes-Pinto H. Restriction enzyme digestion chromosome banding on two commercially important veneroid bivalve species: Ruditapes decussatus and Cerastoderma edule. J Shellfish Res. 2006; 25:857-64.
  • [34]Wang Y, Guo X. Chromosomal mapping of the vertebrate telomeric sequence (TTAGGG) n in four bivalve molluscs by fluorescence in situ hybridization. J Shellfish Res. 2001; 20:1187-90.
  • [35]Wang Y, Guo X. Chromosomal mapping of major ribosomal rRNA genes in the hard clam (Mercenaria mercenaria) using fluorescent hybridization. Mar Biol. 2007; 150:1183-9.
  • [36]Hurtado N, Pasantes JJ. Surface spreading of synaptonemal complexes in the clam Dosinia exoleta (Mollusca, Bivalvia). Chromosome Res. 2005; 13:575-80.
  • [37]Pérez-García C, Hurtado N, Morán P, Pasantes JJ. Evolutionary dynamics of rDNA clusters in chromosomes of five clam species belonging to the family Veneridae (Mollusca, Bivalvia). BioMed Res Int. 2014; 2014:754012.
  • [38]Hurtado N, Pérez-García C, Morán P, Pasantes JJ. Genetic and cytological evidence of hybridization between native Ruditapes decussatus and introduced Ruditapes philippinarum (Mollusca, Bivalvia, Veneridae) in NW Spain. Aquaculture. 2011; 311:123-8.
  • [39]Stankiewicz P, Lupski JR. Genome architecture, rearrangements and genomic disorders. Trends Genet. 2002; 18:74-81.
  • [40]Torres GA, Gong Z, Iovene M, Hirsh CD, Buell CR, Bryan GJ, Novák P, Macas J, Jiang J. Organization and evolution of subtelomeric satellite repeats in the potato genome. G3 (Bethesda). 2011; 1:85-92.
  • [41]Linardopoulou EV, Williams EM, Fan YX, Friedman C, Young JM, Trask BJ. Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature. 2005; 437:94-100.
  • [42]Insua A, Freire R, Ríos R, Méndez J. The 5S rDNA of mussels Mytilus galloprovincialis and M. edulis: sequence, variation and chromosomal location. Chromosome Res. 2001; 9:495-505.
  • [43]Guo X, Wang Y, Xu Z. Genomic analyses using fluorescence in situ hybridization. In: Aquaculture genome technologies. Liu Z, editor. Blackwell Publishing, Oxford; 2007: p.289-311.
  • [44]Leitão A, Chaves R. Banding for chromosomal identification in bivalves. A 20-year history. In Russo R, editor. Aquaculture 1. Dynamic Biochemistry, Process Biotechnology and Molecular Biology 2 (Special Issue 1). Global Science Books; 2008. p. 44–49. http://www. globalsciencebooks.info/Journals/images/GSB_Journal_Information_Stats.pdf webcite
  • [45]Insua A, López-Piñón MJ, Méndez J. Characterization of Aequipecten opercularis (Bivalvia: Pectinidae) chromosomes by different staining techniques and fluorescent in situ hybridization. Genes Genet Syst. 1998; 73:193-200.
  • [46]Wang Y, Guo X. Chromosomal rearrangement in Pectinidae revealed by rRNA loci and implications for bivalve evolution. Biol Bull. 2004; 207:247-56.
  • [47]López-Piñón MJ, Insua A, Méndez J. Chromosome analysis and mapping of ribosomal genes by one- and two-color fluorescent in situ hybridization in Hinnites distortus (Bivalvia: Pectinidae). J Hered. 2005; 96:52-8.
  • [48]Eickbush TH, Eickbush DG. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics. 2007; 175:477-85.
  • [49]WoRMS Editorial Board. World Register of Marine Species. http://www.marinespecies.org/. Accessed 25 Mar 2015.
  • [50]Martínez-Expósito MJ, Pasantes JJ, Méndez J. Proliferation kinetics of mussel (Mytilus galloprovincialis) gill cells. Mar Biol. 1994; 120:41-5.
  • [51]Winnepenninckx B, Backeljau T, Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet. 1993; 9:407.
  • [52]Vilgalys R. http://www.biology.duke.edu/fungi/mycolab/primers.htm. Accessed 25 Mar 2015.
  • [53]Fang BL, De Baere R, Vandenberghe A, De Wachter R. Sequences of three molluscan 5S ribosomal RNAs confirm the validity of a dynamic secondary structure model. Nucleic Acids Res. 1982; 10:4679-85.
  • [54]Giribet G, Distel D. Bivalve phylogeny and molecular data. In: Systematics and Phylogeography of Molluscks. Lydeard C, Lindberg DR, editors. Smithsonian Books, Washington; 2003: p.45-90.
  • [55]Levan A, Fredga K, Sandberg AA. Nomenclature for centromeric position on chromosomes. Hereditas. 1964; 52:201-20.
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