A Strong Deletion Bias in Nonallelic Gene Conversion
Gene conversion is the unidirectional transfer of genetic information between orthologous (allelic) or paralogous (nonallelic) genomic segments. Though a number of studies have examined nucleotide replacements, little is known about length difference mutations produced by gene conversion. Here, we investigate insertions and deletions produced by nonallelic gene conversion in 338 Drosophila and 10,149 primate paralogs. Using a direct phylogenetic approach, we identify 179 insertions and 614 deletions in Drosophila paralogs, and 132 insertions and 455 deletions in primate paralogs. Thus, nonallelic gene conversion is strongly deletion-biased in both lineages, with almost 3.5 times as many conversion-induced deletions as insertions. In primates, the deletion bias is considerably stronger for long indels and, in both lineages, the per-site rate of gene conversion is orders of magnitudes higher than that of ordinary mutation. Due to this high rate, deletion-biased nonallelic gene conversion plays a key role in genome size evolution, leading to the cooperative shrinkage and eventual disappearance of selectively neutral paralogs.
Vyšlo v časopise:
A Strong Deletion Bias in Nonallelic Gene Conversion. PLoS Genet 8(2): e32767. doi:10.1371/journal.pgen.1002508
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002508
Souhrn
Gene conversion is the unidirectional transfer of genetic information between orthologous (allelic) or paralogous (nonallelic) genomic segments. Though a number of studies have examined nucleotide replacements, little is known about length difference mutations produced by gene conversion. Here, we investigate insertions and deletions produced by nonallelic gene conversion in 338 Drosophila and 10,149 primate paralogs. Using a direct phylogenetic approach, we identify 179 insertions and 614 deletions in Drosophila paralogs, and 132 insertions and 455 deletions in primate paralogs. Thus, nonallelic gene conversion is strongly deletion-biased in both lineages, with almost 3.5 times as many conversion-induced deletions as insertions. In primates, the deletion bias is considerably stronger for long indels and, in both lineages, the per-site rate of gene conversion is orders of magnitudes higher than that of ordinary mutation. Due to this high rate, deletion-biased nonallelic gene conversion plays a key role in genome size evolution, leading to the cooperative shrinkage and eventual disappearance of selectively neutral paralogs.
Zdroje
1. KooninEV 2005 Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39 309 338
2. GojoboriTLiWHGraurD 1982 Patterns of nucleotide substitution in pseudogenes and functional genes. J Mol Evol 18 360 369
3. Alvarez-ValinFLamolleaGBernardiG 2002 Isochores, GC3 and mutation biases in the human genome. Gene 300 161 168
4. EcholsNHarrisonPBalasubramanianSLuscombeNMBertoneP 2002 Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. Nucleic Acids Res 30 2515 2523
5. PetrovDA 2002 Mutational Equilibrium Model of Genome Size Evolution. Theor Popul Biol 61 531 544
6. MaraisG 2003 Biased gene conversion: implications for genome and sex evolution. Trends Genet 19 330 338
7. ManceraEBourgonRBrozziAHuberWSteinmetzLM 2008 High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454 479 485
8. LiuGLiH 2008 The correlation between recombination rate and dinucleotide bias in Drosophila melanogaster. J Mol Evol 67 358 367
9. BerglundJPollardKSWebsterMT 2009 Hotspots of biased nucleotide substitutions in human genes. PLoS Biol 7 e1000026 doi:10.1371/journal.pbio.1000026
10. RokasAHollandPW 2000 Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15 454 459
11. BaptesteEPhilippeH 2002 The potential value of indels as phylogenetic markers: position of trichomonads as a case study. Mol Biol Evol 19 972 977
12. BelinkyFCohenOHuchonD 2009 Large-scale parsimony analysis of metazoan indels in protein-coding genes. Mol Biol Evol 27 441 451
13. SmithNGCEyre-WalkerA 2003 Human disease genes: patterns and predictions. Gene 318 169 175
14. LazzaroB 2005 Elevated polymorphism and divergence in the class c scavenger receptors of Drosophila melanogaster and D. simulans. Genetics 169 2023 2034
15. ChenFCLiWH 2001 Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68 444 456
16. EstoupATailliezCCornuetJMSolignacM 1995 Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Mol Biol Evol 12 1074 1084
17. GarzaJCFreimerNB 1996 Homoplasy for size at microsatellite loci in humans and chimpanzee. Genome Res 6 211 217
18. AngersBBernatchezL 1997 Complex evolution of a salmonid microsatellite locus and its consequences in inferring allelic divergence from size information. Mol Biol Evol 14 230 238
19. van OppenMJHRicoCTurnerGFHewittGM 2000 Extensive homoplasy, nonstepwise mutations, and shared ancestral polymorphism at a complex microsatellite locus in Lake Malawi cichlids. Mol Biol Evol 17 489 498
20. LukacsovichTWaldmanAS 1999 Suppression of intrachromosomal gene conversion in mammalian cells by small degrees of sequence divergence. Genetics 151 1559 1568
21. HastingsPJ 2010 Mechanisms of ectopic gene conversion. Gene 1 427 439
22. McGrathCLCasolaCHahnMW 2009 Minimal effect of ectopic gene conversion among recent duplicates in four mammalian genomes. Genetics 182 615 622
23. KatjuVLynchM 2003 The structure and early evolution of recently arisen gene duplicates in the Caenorhabditis elegans genome. Genetics 165 1793 1803
24. PetrovDAHartlDL 1998 High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol 15 293 302
25. ZhangZSchwartzSWagnerLMillerW 2000 A greedy algorithm for aligning DNA sequences. J Comput Biol 7 203 214
26. KondrashovASAssisR 2010 Bridges: a tool for identifying local similarities in long sequences. Bioinformatics 26 2055 2056
27. AltschulSFGishWMillerWMyersEWLipmanDJ 1990 Basic local alignment search tool. J Mol Biol 215 403 410
28. EdgarRC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797
29. Fiston-LavierASSinghNDLipatovMPetrovDA 2010 Drosophila melanogaster recombination rate calculator. Gene 463 18 20
30. The International HapMap Consortium 2003 The international HapMap project. Nature 426 789 796
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 2
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