Characterization and distribution of retrotransposons and simple sequence repeats in the bovine genome
Edited by James E. Womack, Texas A&M University, College Station, TX, and approved June 19, 2009
Abstract
Interspersed repeat composition and distribution in mammals have been best characterized in the human and mouse genomes. The bovine genome contains typical eutherian mammal repeats, but also has a significant number of long interspersed nuclear element RTE (BovB) elements proposed to have been horizontally transferred from squamata. Our analysis of the BovB repeats has indicated that only a few of them are currently likely to retrotranspose in cattle. However, bovine L1 repeats (L1 BT) have many likely active copies. Comparison of substitution rates for BovB and L1 BT indicates that L1 BT is a younger repeat family than BovB. In contrast to mouse and human, L1 occurrence is not negatively correlated with G+C content. However, BovB, Bov A2, ART2A, and Bov-tA are negatively correlated with G+C, although Bov-tAs correlation is weaker. Also, by performing genome wide correlation analysis of interspersed and simple sequence repeats, we have identified genome territories by repeat content that appear to define ancestral vs. ruminant-specific genomic regions. These ancestral regions, enriched with L2 and MIR repeats, are largely conserved between bovine and human.
Acknowledgments.
We thank the Bovine Genome Sequencing Project for providing segmental duplication data (E. Eichler, Seattle, WA), GLEAN gene models (C. Elsik, Washington, DC), and their coordinates; and the anonymous reviewers who helped improve this report.
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References
1
AF Smit, The origin of interspersed repeats in the human genome. Curr Opin Genet Dev 6, 743–748 (1996).
2
ES Lander, et al., Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).
3
J Jurka, VV Kapitonov, O Kohany, MV Jurka, Repetitive sequences in complex genomes: Structure and evolution. Annu Rev Genom Hum G 8, 241–259 (2007).
4
RH Waterston, et al., Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562 (2002).
5
AFA Smit, AD Riggs, MIRs are classic, transfer-RNA-derived SINEs that amplified before the mammalian radiation. Nucleic Acids Res 23, 98–102 (1995).
6
PL Deininger, JV Moran, MA Batzer, HH Kazazian, Mobile elements and mammalian genome evolution. Curr Opin Genet Dev 13, 651–658 (2003).
7
J Giordano, et al., Evolutionary History of Mammalian Transposons Determined by Genome-Wide Defragmentation. PLoS Comput Biol 3, e137 (2007).
8
HH Kazazian, Mobile elements: Drivers of genome evolution. Science 303, 1626–1632 (2004).
9
HH Kazazian, Mobile elements and disease. Curr Opin Genet Dev 8, 343–350 (1998).
10
PL Deininger, MA Batzer, Alu repeats and human disease. Mol Genet Metab 67, 183–193 (1999).
11
E Birney, et al., Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799–816 (2007).
12
M Krull, M Petrusma, W Makalowski, J Brosius, J Schmitz, Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res 17, 1139–1145 (2007).
13
K Lindblad-Toh, et al., Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438, 803–819 (2005).
14
AJ Gentles, et al., Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res 17, 992–1004 (2007).
15
M Dewannieux, C Esnault, T Heidmann, LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 35, 41–48 (2003).
16
K Ohshima, N Okada, SINEs and LINEs: Symbionts of eukaryotic genomes with a common tail. Cytogenet Genome Res 110, 475–490 (2005).
17
D Kordis, F Gubensek, Horizontal transfer of non-LTR retrotransposons in vertebrates. Genetica 107, 121–128 (1999).
18
D Kordis, F Gubensek, Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. Proc Natl Acad Sci USA 95, 10704–10709 (1998).
19
M Shimamura, H Abe, M Nikaido, K Ohshima, N Okada, Genealogy of families of SINEs in cetaceans and artiodactyls: The presence of a huge superfamily of tRNA(Glu)-derived families of SINEs. Mol Biol Evol 16, 1046–1060 (1999).
20
C Jobse, et al., Evolution and recombination of bovine DNA repeats. J Mol Evol 41, 277–283 (1995).
21
HS Malik, TH Eickbush, The RTE class of non-LTR retrotransposons is widely distributed in animals and is the origin of many SINEs. Mol Biol Evol 15, 1123–1134 (1998).
22
JA Lenstra, JA van Boxtel, KA Zwaagstra, M Schwerin, Short interspersed nuclear element (SINE) sequences of the Bovidae. Anim Genet 24, 33–39 (1993).
23
WJ Kent, R Baertsch, The UCSC Genome Browser Database., Available at http://genome.ucsc.edu/goldenPath/credits.html#cow_credits. (2009).
24
WJ Kent, R Baertsch, A Hinrichs, W Miller, D Haussler, Evolution's cauldron: Duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci USA 100, 11484–11489 (2003).
25
S Schwartz, et al., Human-mouse alignments with BLASTZ. Genome Res 13, 103–107 (2003).
26
JK Pace, C Gilbert, MS Clark, C Feschotte, Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. Proc Natl Acad Sci USA 105, 17023–17028 (2008).
27
S Iwashita, et al., A Tandem Gene Duplication Followed by Recruitment of a Retrotransposon Created the Paralogous Bucentaur Gene (bcntp97) in the Ancestral Ruminant. Mol Biol Evol 23, 798–806 (2006).
28
PD Waters, G Dobigny, PJ Waddell, TJ Robinson, Evolutionary History of LINE-1 in the Major Clades of Placental Mammals. PLoS ONE 2, e158 (2007).
29
DM Sassaman, et al., Many human L1 elements are capable of retrotransposition. Nat Genet 16, 37–43 (1997).
30
H Nakagama, et al., Molecular mechanisms for maintenance of G-rich short tandem repeats capable of adopting G4 DNA structures. Mutat Res-Fund Mol M 598, 120–131 (2006).
31
GE Liu, LK Matukumalli, TS Sonstegard, LL Shade, CP Van Tassell, Genomic divergences among cattle, dog and human estimated from large-scale alignments of genomic sequences. BMC Genomics 7, 140 (2006).
32
K Inoue, JR Lupski, Molecular mechanisms for genomic disorders. Annu Rev Genomics Hum Genet 3, 199–242 (2002).
33
JR Lupski, P Stankiewicz, Genomic Disorders: Molecular Mechanisms for Rearrangements and Conveyed Phenotypes. PLoS Genet 1, e49 (2005).
34
WJ Murphy, G Bourque, G Tesler, P Pevzner, SJ O'Brien, Reconstructing the genomic architecture of mammalian ancestors using multispecies comparative maps. Hum Genomics 1, 30–40 (2003).
35
WJ Murphy, et al., Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309, 613–617 (2005).
36
BA Cohen, RD Mitra, JD Hughes, GM Church, A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat Genet 26, 183–186 (2000).
37
K Kupper, et al., Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma 116, 285–306 (2007).
38
JM Trasler, Gamete imprinting: Setting epigenetic patterns for the next generation. Reprod Fertil Dev 18, 63–69 (2006).
39
RC Edgar, MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797 (2004).
40
RC Edgar, MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
41
RC Edgar, EW Myers, PILER: Identification and classification of genomic repeats. Bioinformatics 21, I152–I158 (2005).
42
CD Smith, et al., Improved repeat identification and masking in Dipterans. Gene 389, 1–9 (2007).
43
AL Price, NC Jones, PA Pevzner, De novo identification of repeat families in large genomes. Bioinformatics 21, I351–I358 (2005).
44
W Gish, DJ States, Identification of protein coding regions by database similarity search. Nat Genet 3, 266–272 (1993).
45
C The UniProt, The Universal Protein Resource (UniProt). Nucl. Acids Res 36, D190–D195 (2008).
46
A Stamatakis, RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
47
PF Arndt, T Hwa, DA Petrov, Substantial regional variation in substitution rates in the human genome: Importance of GC content, gene density, and telomere-specific effects. J Mol Evol 60, 748–763 (2005).
48
TH Jukes, CR Cantor, Evolution of protein molecules. Mammalian Protein Metabolism, ed HN Munro (Academic, New York), pp. 21–123 (1969).
49
K Tamura, J Dudley, M Nei, S Kumar, MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24, 1596–1599 (2007).
50
C Mayer, PHOBOS., Available at http://www.ruhr-uni-bochum.de/spezzoo/cm/cm_phobos.htm. (2008).
51
IJ Nijman, JA Lenstra, Mutation and recombination in cattle satellite DNA: A feedback model for the evolution of satellite DNA repeats. J Mol Evol 52, 361–371 (2001).
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© 2009.
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Received: February 5, 2009
Published online: August 4, 2009
Published in issue: August 4, 2009
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Acknowledgments
We thank the Bovine Genome Sequencing Project for providing segmental duplication data (E. Eichler, Seattle, WA), GLEAN gene models (C. Elsik, Washington, DC), and their coordinates; and the anonymous reviewers who helped improve this report.
Notes
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0901282106/DCSupplemental.
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The authors declare no conflict of interest.
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