Skip to main content
Log in

Low Levels of LTR Retrotransposon Deletion by Ectopic Recombination in the Gigantic Genomes of Salamanders

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

Abstract

Across the tree of life, species vary dramatically in nuclear genome size. Mutations that add or remove sequences from genomes—insertions or deletions, or indels—are the ultimate source of this variation. Differences in the tempo and mode of insertion and deletion across taxa have been proposed to contribute to evolutionary diversity in genome size. Among vertebrates, most of the largest genomes are found within the salamanders, an amphibian clade with genome sizes ranging from ~14 to ~120 Gb. Salamander genomes have been shown to experience slower rates of DNA loss through small (i.e., <30 bp) deletions than do other vertebrate genomes. However, no studies have addressed DNA loss from salamander genomes resulting from larger deletions. Here, we focus on one type of large deletion—ectopic-recombination-mediated removal of LTR retrotransposon sequences. In ectopic recombination, double-strand breaks are repaired using a “wrong” (i.e., ectopic, or non-allelic) template sequence—typically another locus of similar sequence. When breaks occur within the LTR portions of LTR retrotransposons, ectopic-recombination-mediated repair can produce deletions that remove the internal transposon sequence and the equivalent of one of the two LTR sequences. These deletions leave a signature in the genome—a solo LTR sequence. We compared levels of solo LTRs in the genomes of four salamander species with levels present in five vertebrates with smaller genomes. Our results demonstrate that salamanders have low levels of solo LTRs, suggesting that ectopic-recombination-mediated deletion of LTR retrotransposons occurs more slowly than in other vertebrates with smaller genomes.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • AmphibiaWeb (2014) Information on amphibian biology and conservation. Berkeley, California. http://amphibiaweb.org/. Accessed 5 Oct 2014

  • Baudat F, de Massy B (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15(5):565–577

    Article  CAS  PubMed  Google Scholar 

  • Baudat F, Imai Y, de Massy B (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Gen 14:794–806

    Article  CAS  Google Scholar 

  • Bennetzen JL, Kellogg EA (1997) Do plants have a one-way ticket to genomic obesity? Plant Cell 9:1509

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bensasson D, Petrov DA, Zhang DX, Hartl DL, Hewitt GM (2001) Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol Biol Evol 18:246

    Article  CAS  PubMed  Google Scholar 

  • Blass E, Bell M, Boissinot S (2012) Accumulation and rapid decay of non-LTR retrotransposons in the genome of the threespine stickleback. Gen Biol Evol 4(5):687–702

    Article  Google Scholar 

  • Borde V, de Massy B (2013) Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr Opin Genet Dev 23:147–155

    Article  CAS  PubMed  Google Scholar 

  • Cole F, Keeney S, Jasin M (2010) Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol Cell 39:700–710

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dion V, Gasser SM (2013) Chromatin movement in the maintenance of genome stability. Cell 152:1355–1364

    Article  CAS  PubMed  Google Scholar 

  • El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Gen Biol Evol 5:954–965

    Article  Google Scholar 

  • Furano AV, Duvernell DD, Boissinot S (2004) L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. Trends Genet 20:9–14

    Article  CAS  PubMed  Google Scholar 

  • Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Gen 6:477–487

    Article  CAS  Google Scholar 

  • Gregory TR (2005) The evolution of the genome. Academic Press, New York

    Google Scholar 

  • Gregory TR (2014) Animal genome size database. http://www.genomesize.com

  • Hellsten U et al (2010) The genome of the western clawed frog Xenopus tropicalis. Science 328:633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jurka J, Vapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467

    Article  CAS  PubMed  Google Scholar 

  • Kadyk LC, Hartwell LH (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387–402

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27:873–886

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384

    Article  CAS  PubMed  Google Scholar 

  • Kvikstad EM, Tyekucheva S, Chiaromonte F, Makova KD (2007) A macaque’s-eye view of human insertions and deletions: differences in mechanisms. PLoS Comp Biol 3:e176

    Article  Google Scholar 

  • Kvikstad EM, Chiaromonte F, Makova KD (2009) Ride the wavelet: a multiscale analysis of genomic contexts flanking small insertions and deletions. Genome Res 19:1153–1164

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lichten M, de Massy B (2011) The impressionistic landscape of meiotic recombination. Cell 147:267–270

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lynch M (2007) The origins of genome architecture. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Mani R-S, Chinnaiyan AM (2010) Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat Rev Gen 11:819–829

    Article  CAS  Google Scholar 

  • Marjanović D, Laurin M (2007) Fossils, molecules, divergence times, and the origin of lissamphibians. Syst Biol 56:369–388

    Article  PubMed  Google Scholar 

  • Mine-Hattab J, Rothstein R (2012) Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 14:510–517

    Article  CAS  PubMed  Google Scholar 

  • Mladenov E, Iliakis G (2011) Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat Res 711:61–72

    Article  CAS  PubMed  Google Scholar 

  • Moynahan ME, Jasin M (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 11:196–207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nam K, Ellegren H (2012) Recombination drives vertebrate genome contraction. PLoS Genet 8:e1002680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paigen K, Petkov P (2010) Mammalian recombination hot spots: properties, control and evolution. Nat Rev Gen 11:221–233

    Article  CAS  Google Scholar 

  • Pan J et al (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144:719–731

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Petrov DA (2002) Mutational equilibrium model of genome size evolution. Theor Popul Biol 61:533–546

    Article  Google Scholar 

  • Petrov DA, Sangster TA, Johnston JS, Hartl DL, Shaw KL (2000) Evidence for DNA loss as a determinant of genome size. Science 287:1060–1062

    Article  CAS  PubMed  Google Scholar 

  • Petrov DA, Aminetzach YT, Davis J, Bensasson D, Hirsch AE (2003) Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 20:880–892

    Article  CAS  PubMed  Google Scholar 

  • Petrov DA, Fiston-Lavier A-S, Lipatov M, Lenkov K, González J (2011) Population genomics of transposable elements in Drosophila melanogaster. Mol Biol Evol 28:1633–1644

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pyron RA (2011) Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Syst Biol 60:466–481

    Article  PubMed  Google Scholar 

  • Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11:2600–2621

    Article  CAS  PubMed  Google Scholar 

  • Roehl AC et al (2010) Intrachromosomal mitotic nonallelic homologous recombination is the major molecular mechanism underlying type-2 NF1 deletions. Hum Mutat 31:1163–1173

    Article  CAS  PubMed  Google Scholar 

  • Sessions SK (2008) Evolutionary cytogenetics in salamanders. Chrom Res 16:183–201

    Article  CAS  PubMed  Google Scholar 

  • Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472:375–378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith J et al (2009) Genic regions of a large salamander genome contain long introns and novel genes. BMC Genom 10:19

    Article  CAS  Google Scholar 

  • Sun C, Mueller RL (2014) Hellbender genome sequences shed light on genome expansion at the base of crown salamanders. Gen Biol Evol 6:1818–1829

    Article  CAS  Google Scholar 

  • Sun C, Arriaza JRL, Mueller RL (2012a) Slow DNA loss in the gigantic genomes of salamanders. Gen Biol Evol 4:1340–1348

    Article  Google Scholar 

  • Sun C et al (2012b) LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders. Gen Biol Evol 4:168–183

    Article  Google Scholar 

  • Tian Z et al (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res 19:2221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Webster MT, Hurst LD (2012) Direct and indirect consequences of meiotic recombination: implications for genome evolution. Trends Genet 28:101–109

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Wake DB (2009) Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. Mol Phylogen Evol 53:492–508

    Article  CAS  Google Scholar 

  • Zheng Y, Peng R, Kuro-o M, Zeng X (2011) Exploring patterns and extent of bias in estimating divergence time from mitochondrial DNA sequence data in a particular lineage: a case study of salamanders (Order Caudata). Mol Biol Evol 28:2521–2535

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation (REU supplement to NSF-DEB 1021489 to R.L.M.). We thank members of the Mueller lab and two anonymous reviewers for helpful comments and discussion.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rachel Lockridge Mueller.

Additional information

Matthew Blake Frahry and Cheng Sun have contributed equally.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental File 1

Terminal to internal (T:I) ratios of individual LTR retrotransposon families for fully sequenced vertebrate genomes and all salamanders based on datasets of equivalent sizes (118,164 reads). Each data point represents one LTR retrotransposon family; families contain different numbers of elements. Outliers are excluded. Supplementary material 1 (PDF 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Frahry, M.B., Sun, C., Chong, R.A. et al. Low Levels of LTR Retrotransposon Deletion by Ectopic Recombination in the Gigantic Genomes of Salamanders. J Mol Evol 80, 120–129 (2015). https://doi.org/10.1007/s00239-014-9663-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-014-9663-7

Keywords

Navigation