The role of retrotransposons in gene family expansions: insights from the mouse Abp gene family

BMC Evolutionary Biology

Christina M Laukaitis¹  Robert C Karn¹  Václav Janoušek² 

[1] Department of Medicine, College of Medicine, University of Arizona, Tucson, AZ, USA;Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, Prague 128 43, Czech Republic

关键词: NAHR;    ERVII;    LINE1;    Androgen-binding protein;    Gene duplication;    House mouse;   

Others  :  1087277
DOI  :  10.1186/1471-2148-13-107

 received in 2013-02-24, accepted in 2013-05-14,  发布年份 2013

【 摘 要 】

Background

Retrotransposons have been suggested to provide a substrate for non-allelic homologous recombination (NAHR) and thereby promote gene family expansion. Their precise role, however, is controversial. Here we ask whether retrotransposons contributed to the recent expansions of the Androgen-binding protein (Abp) gene families that occurred independently in the mouse and rat genomes.

Results

Using dot plot analysis, we found that the most recent duplication in the Abp region of the mouse genome is flanked by L1Md_T elements. Analysis of the sequence of these elements revealed breakpoints that are the relicts of the recombination that caused the duplication, confirming that the duplication arose as a result of NAHR using L1 elements as substrates. L1 and ERVII retrotransposons are considerably denser in the Abp regions than in one Mb flanking regions, while other repeat types are depleted in the Abp regions compared to flanking regions. L1 retrotransposons preferentially accumulated in the Abp gene regions after lineage separation and roughly followed the pattern of Abp gene expansion. By contrast, the proportion of shared vs. lineage-specific ERVII repeats in the Abp region resembles the rest of the genome.

Conclusions

We confirmed the role of L1 repeats in Abp gene duplication with the identification of recombinant L1Md_T elements at the edges of the most recent mouse Abp gene duplication. High densities of L1 and ERVII repeats were found in the Abp gene region with abrupt transitions at the region boundaries, suggesting that their higher densities are tightly associated with Abp gene duplication. We observed that the major accumulation of L1 elements occurred after the split of the mouse and rat lineages and that there is a striking overlap between the timing of L1 accumulation and expansion of the Abp gene family in the mouse genome. Establishing a link between the accumulation of L1 elements and the expansion of the Abp gene family and identification of an NAHR-related breakpoint in the most recent duplication are the main contributions of our study.

【 授权许可】

   
2013 Janoušek et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Ohno S: Sex chromosomes and sex-linked genes. Berlin, New York: Springer-Verlag; 1967.
• [2]Ohno S: Evolution by gene duplication. New York: Springer Verlag; 1970.
• [3]Ponting CP: The functional repertoires of metazoan genomes. Nat Rev Genet 2008, 9(9):689-698.
• [4]Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, Scherer S, Scott G, Steffen D, Worley KC, Burch PE: Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004, 428(6982):493-521.
• [5]Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W: Initial sequencing and analysis of the human genome. Nature 2001, 409(6822):860-921.
• [6]Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P: Initial sequencing and comparative analysis of the mouse genome. Nature 2002, 420(6915):520-562.
• [7]Hurst LD, Smith NG: Do essential genes evolve slowly? Curr Biol 1999, 9(14):747-750.
• [8]Birtle Z, Goodstadt L, Ponting C: Duplication and positive selection among hominin-specific PRAME genes. BMC Genomics 2005, 6:120. BioMed Central Full Text
• [9]Emes RD, Riley MC, Laukaitis CM, Goodstadt L, Karn RC, Ponting CP: Comparative evolutionary genomics of androgen-binding protein genes. Genome Res 2004, 14(8):1516-1529.
• [10]Goldstone HM, Stegeman JJ: A revised evolutionary history of the CYP1A subfamily: gene duplication, gene conversion, and positive selection. J Mol Evol 2006, 62(6):708-717.
• [11]Johnston CR, O’Dushlaine C, Fitzpatrick DA, Edwards RJ, Shields DC: Evaluation of whether accelerated protein evolution in chordates has occurred before, after, or simultaneously with gene duplication. Mol Biol Evol 2007, 24(1):315-323.
• [12]Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ: A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 2005, 3(6):e170.
• [13]Ponting CP, Goodstadt L: Separating derived from ancestral features of mouse and human genomes. Biochem Soc Trans 2009, 37(Pt 4):734-739.
• [14]Ostertag EM, Kazazian HH Jr: Biology of mammalian L1 retrotransposons. Annu Rev Genet 2001, 35:501-538.
• [15]Babcock M, Pavlicek A, Spiteri E, Kashork CD, Ioshikhes I, Shaffer LG, Jurka J, Morrow BE: Shuffling of genes within low-copy repeats on 22q11 (LCR22) by Alu-mediated recombination events during evolution. Genome Res 2003, 13(12):2519-2532.
• [16]Bailey JA, Church DM, Ventura M, Rocchi M, Eichler EE: Analysis of segmental duplications and genome assembly in the mouse. Genome Res 2004, 14(5):789-801.
• [17]Bailey JA, Liu G, Eichler EE: An Alu transposition model for the origin and expansion of human segmental duplications. Am J Hum Genet 2003, 73(4):823-834.
• [18]Tuzun E, Bailey JA, Eichler EE: Recent segmental duplications in the working draft assembly of the brown Norway rat. Genome Res 2004, 14(4):493-506.
• [19]Giannuzzi G, D’Addabbo P, Gasparro M, Martinelli M, Carelli FN, Antonacci D, Ventura M: Analysis of high-identity segmental duplications in the grapevine genome. BMC Genomics 2011, 12:436. BioMed Central Full Text
• [20]Liu Y, Qin X, Song XZ, Jiang H, Shen Y, Durbin KJ, Lien S, Kent MP, Sodeland M, Ren Y: Bos taurus genome assembly. BMC Genomics 2009, 10:180. BioMed Central Full Text
• [21]She X, Cheng Z, Zollner S, Church DM, Eichler EE: Mouse segmental duplication and copy number variation. Nat Genet 2008, 40(7):909-914.
• [22]Zhou Y, Mishra B: Quantifying the mechanisms for segmental duplications in mammalian genomes by statistical analysis and modeling. Proc Natl Acad Sci U S A 2005, 102(11):4051-4056.
• [23]Fitch DH, Bailey WJ, Tagle DA, Goodman M, Sieu L, Slightom JL: Duplication of the gamma-globin gene mediated by L1 long interspersed repetitive elements in an early ancestor of simian primates. Proc Natl Acad Sci U S A 1991, 88(16):7396-7400.
• [24]Guo X, Freyer L, Morrow B, Zheng D: Characterization of the past and current duplication activities in the human 22q11.2 region. BMC Genomics 2011, 12:71. BioMed Central Full Text
• [25]Hahn MW, Demuth JP, Han SG: Accelerated rate of gene gain and loss in primates. Genetics 2007, 177(3):1941-1949.
• [26]Murakami H, Aburatani S, Horimoto K: Relationship between segmental duplications and repeat sequences in human chromosome 7. Genome informatics International Conference on Genome Informatics 2005, 16(1):13-21.
• [27]Glusman G, Clifton S, Roe B, Lancet D: Sequence analysis in the olfactory receptor gene cluster on human chromosome 17: recombinatorial events affecting receptor diversity. Genomics 1996, 37(2):147-160.
• [28]Kambere MB, Lane RP: Exceptional LINE density at V1R loci: the Lyon repeat hypothesis revisited on autosomes. J Mol Evol 2009, 68(2):145-159.
• [29]Arnheim N: Concerted evolution of multigene families. In Evolution of Genes and Proteins. Edited by Nei M, RK K. Sunderland: Sinauer; 1983:38-61.
• [30]Hurst GD, Werren JH: The role of selfish genetic elements in eukaryotic evolution. Nat Rev Genet 2001, 2(8):597-606.
• [31]Witherspoon DJ, Watkins WS, Zhang Y, Xing J, Tolpinrud WL, Hedges DJ, Batzer MA, Jorde LB: Alu repeats increase local recombination rates. BMC Genomics 2009, 10:530. BioMed Central Full Text
• [32]Yang S, Arguello JR, Li X, Ding Y, Zhou Q, Chen Y, Zhang Y, Zhao R, Brunet F, Peng L: Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet 2008, 4(1):e3.
• [33]Arnheim N, Calabrese P, Tiemann-Boege I: Mammalian meiotic recombination hot spots. Annu Rev Genet 2007, 41:369-399.
• [34]Jurka J, Kohany O, Pavlicek A, Kapitonov VV, Jurka MV: Clustering, duplication and chromosomal distribution of mouse SINE retrotransposons. Cytogenet Genome Res 2005, 110(1–4):117-123.
• [35]Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SH, Graber JH, Broman KW, Petkov PM: The recombinational anatomy of a mouse chromosome. PLoS Genet 2008, 4(7):e1000119.
• [36]Shifman S, Bell JT, Copley RR, Taylor MS, Williams RW, Mott R, Flint J: A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol 2006, 4(12):e395.
• [37]Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV: Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 2011, 472(7343):375-378.
• [38]Song M, Boissinot S: Selection against LINE-1 retrotransposons results principally from their ability to mediate ectopic recombination. Gene 2007, 390(1–2):206-213.
• [39]Paigen K, Petkov P: Mammalian recombination hot spots: properties, control and evolution. Nat Rev Genet 2010, 11(3):221-233.
• [40]Laukaitis CM, Heger A, Blakley TD, Munclinger P, Ponting CP, Karn RC: Rapid bursts of androgen-binding protein (Abp) gene duplication occurred independently in diverse mammals. BMC Evol Biol 2008, 8:46. BioMed Central Full Text
• [41]Karn RC, Laukaitis CM: The mechanism of expansion and the volatility it created in three pheromone gene clusters in the mouse (Mus musculus) genome. Genome Biol Evol 2009, 1:494-503.
• [42]Laukaitis CM, Critser ES, Karn RC: Salivary androgen-binding protein (ABP) mediates sexual isolation in Mus musculus. Evolution 1997, 51(6):2000-2005.
• [43]Talley HM, Laukaitis CM, Karn RC: Female preference for male saliva: implications for sexual isolation of Mus musculus subspecies. Evolution 2001, 55(3):631-634.
• [44]Laukaitis C, Karn RC: Recognition of subspecies status mediated by androgen-binding protein (ABP) in the evolution of incipient reinforcement on the European house mouse hybrid zone. In Evolution of the House Mouse. Edited by Macholan M, Munclinger P, Baird SJ, Pialek JWN. NY: Cambridge University Press; 2012:150-190.
• [45]Vošlajerová Bímová B, Macholán M, Baird SEB, Munclinger P, Laukaitis CM, Karn RC, Luzynski K, Tucker P, Piálek J: Reinforcement selection acting on the European house mouse hybrid zone. Mol Ecol 2011, 20:2403-2424.
• [46]Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, Roskin KM, Schwartz M, Sugnet CW, Thomas DJ: The UCSC Genome Browser Database. Nucleic Acids Res 2003, 31(1):51-54.
• [47]Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R, Hardison RC, Haussler D, Miller W: Human-mouse alignments with BLASTZ. Genome Res 2003, 13(1):103-107.
• [48]R Development Core Team: R: A Language and Environment for Statistical Computing, Reference Index Version 2.13.1. Vienna, Austria: R Foundation for Statistical Computing; 2011.
• [49]Smit AFA, Hubley R, Green P: RepeatMasker Open-3.0. 1996-2010. http://www.repeatmasker.org/ webcite
• [50]Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 2004, 5:113. BioMed Central Full Text
• [51]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [52]Paradis E, Claude J, Strimmer K: APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 2004, 20(2):289-290.
• [53]Katju V, Lynch M: The structure and early evolution of recently arisen gene duplicates in the Caenorhabditis elegans genome. Genetics 2003, 165(4):1793-1803.