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Gene Conversion and Positive Selection Driving the Evolution of the Caenorhabditis ssp. ZIM/HIM-8 Protein Family

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Abstract

In C. elegans, four C2H2 zinc-finger proteins (ZIM-1, ZIM-2, ZIM-3, and HIM-8), which are arranged in tandem, mediate chromosome-specific pairing and synapsis during meiosis. The zim/him-8 genes from three Caenorhabditis species were contrasted in an effort to investigate the mechanisms driving their evolution. Here it is shown that the preservation of higher degree of sequence similarity in the N-terminal portion, particularly in several regions within the second exon between paralogous zim genes (especially between zim-1 and zim-3), is due to independent interparalogue gene conversions. However, the evolutionary force is not uniformly strong across species. The present data reveal that more frequent gene conversion events have occurred in C. elegans, whereas only gene conversions between zim-1 and zim-3 are detected in C. remanei. Although gene conversions are predicted to be present among zim-1, zim-2, and zim-3 in C. briggsae, the conversion tracts between zim-1/zim-2 and zim-2/zim-3 are very short. Moreover, positive selection analysis was performed on the basis of the significantly discordant phylogenies reconstructed using the N- and C-terminal sequences, respectively. Several codon sites located in the regions that are supposed not to have experienced gene conversions are predicted to be under the influence of positive selection. In comparison, stronger positive selection has acted on the C-terminal region relative to the N-terminal region. Thus, the zim/him-8 genes that evolve concertedly have also been shown to undergo adaptive diversifying selection.

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References

  • Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18:1585–1592

    PubMed  CAS  Google Scholar 

  • Beisswanger S, Stephan W (2008) Evidence that strong positive selection drives neofunctionalization in the tandemly duplicated polyhomeotic genes in Drosophila. Proc Natl Acad Sci USA 105:55447–55452

    Article  Google Scholar 

  • Blumenthal T, Gleason KS (2003) Caenorhabditis elegans operons: form and function. Nat Rev Genet 4:112–120

    Article  PubMed  CAS  Google Scholar 

  • Blumenthal T, Evans D, Link CD, Guffanti A, Lawson D, Thierry-Mieg J, Thierry-Mieg D, Chiu WL, Duke K, Kiraly M, Kim SK (2002) A global analysis of Caenorhabditis elegans operons. Nature 417:851–854

    Article  PubMed  CAS  Google Scholar 

  • Chen JM, Cooper DN, Chuzhanova N, Férec C, Patrinos GP (2007) Gene conversion: mechanism, evolution and human disease. Nat Genet 8:762–775

    Article  CAS  Google Scholar 

  • Cho S, Jin SW, Cohe A, Ellis RE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14:1207–1220

    Article  PubMed  CAS  Google Scholar 

  • Comeron JM (1995) A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J Mol Evol 41:1152–1159

    Article  PubMed  CAS  Google Scholar 

  • Drouin G, Prat F, Ell M, Clarke GDP (1999) Detecting and characterizing gene conversions between multigene family members. Mol Biol Evol 16:1369–1390

    PubMed  CAS  Google Scholar 

  • Elliott B, Richardson C, Winderbaum J, Nickoloff JA, Jasin M (1998) Gene conversion tracts from double-strand break repair in mammalian cells. Mol Cell Biol 18:93–101

    PubMed  CAS  Google Scholar 

  • Englbrecht CC, Schoof H, Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39

    Article  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Garcia-Muse T, Boulton SJ (2007) Meiotic recombination in Caenorhabditis elegans. Chromosome Res 15:607–621

    Article  PubMed  CAS  Google Scholar 

  • Goldstone HMH, Stegeman JJ (2006) A revised evolutionary history of the CYP1A subfamily: gene duplication, gene conversion, and positive selection. J Mol Evol 62:708–717

    Article  PubMed  CAS  Google Scholar 

  • Holmes EC, Worobey M, Rambaut A (1999) Phylogenetic evidence for recombination in Dengue virus. Mol Biol Evol 16:405–409

    PubMed  CAS  Google Scholar 

  • Hurles ME, Willey D, Matthews L, Hussain SS (2004) Origins of chromosomal rearrangement hotspots in the human genome: evidence from the AZFa deletion hotspots. Genome Biol 5:R55

    Article  PubMed  Google Scholar 

  • Innan H (2003) A two-locus gene conversion model with selection and its application to the human RHCE and RHD genes. Proc Natl Acad Sci USA 100:8793–8798

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Kuma K, Miyata T, Toh H (2005) Improvement in the accuracy of multiple sequence alignment program MAFFT. Genome Inform 16:22–33

    PubMed  CAS  Google Scholar 

  • Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23:1891–1901

    Article  PubMed  Google Scholar 

  • Kruithof EKO, Satta N, Liu JW, Dunoyer-Geindre S, Fish RJ (2007) Gene conversion limits divergence of mammalian TLR1 and TLR6. BMC Evol Biol 7:e148

    Article  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • McKim KS (2007) Meiotic pairing: a place to hook up. Curr Biol 17:R165–R168

    Article  PubMed  CAS  Google Scholar 

  • Mita SD, Ronfort J, McKhann HI, Poncet C, Malki RE, Bataillon T (2007) Investigation of the demographic and selective forces shaping the nucleotide diversity of genes involved in nod factor signaling in Medicago truncatula. Genetics 177:2123–2133

    Article  PubMed  Google Scholar 

  • Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332

    Article  PubMed  CAS  Google Scholar 

  • Moeller DA, Tiffin P (2005) Genetic diversity and the evolutionary history of plant immunity genes in two species of Zea. Mol Biol Evol 22:2480–2490

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Gaut BS (2005) Gene conversion and the evolution of three Leucine-rich repeat gene families in Arabidopsis thaliana. Mol Biol Evol 22:2444–2456

    Article  PubMed  CAS  Google Scholar 

  • Nelms BL, Hanna-Rose W (2006) C. elegans HIM-8 functions outside of meiosis to antagonize EGL-13 Sox protein function. Dev Biol 293:392–402

    Article  PubMed  CAS  Google Scholar 

  • Noonan JP, Grimwood J, Schmutz J, Dickson M, Myers RM (2004) Gene conversion and the evolution of protocadherin gene cluster diversity. Genome Res 14:354–366

    Article  PubMed  CAS  Google Scholar 

  • Ohta T (1997) Role of gene conversion in generating polymorphisms at major histocompatibility complex loci. Hereditas 127:97–103

    Article  PubMed  CAS  Google Scholar 

  • Phillips CM, Dernburg AF (2006) A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 11:817–829

    Article  PubMed  CAS  Google Scholar 

  • Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, Meneely PM, Dernburg AF (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123:1051–1063

    Article  PubMed  CAS  Google Scholar 

  • Posada D (2002) Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717

    PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    PubMed  CAS  Google Scholar 

  • Sengupta S, Farheen S, Mukherjee N, Majumder PP (2007) Patterns of nucleotide sequence variation in ICAMI and TNF genes in twelve ethnic groups of India: roles of demographic history and natural selection. J Genet 86:225–239

    Article  PubMed  CAS  Google Scholar 

  • Shannon M, Hamilton AT, Gordon L, Branscomb E, Stubbs L (2003) Differential expansion of zinc-finger transcription factor loci in homologous human and mouse gene clusters. Genome Res 13:1097–1110

    Article  PubMed  CAS  Google Scholar 

  • Sun H, Nelms BL, Sleiman SF, Chamberlin HM, Hanna-Rose W (2007) Modulation of Caenorhabditis elegans transcription factor activity by HIM-8 and the related zinc-finger ZIM proteins. Genetics 177:1221–1226

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Yang Z (2007) PAML4: A program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

  • Zhang L (2008) Adaptive evolution and frequent gene conversion in the brain expressed X-linked gene family in mammals. Biochem Genet 46:293–311

    Article  PubMed  Google Scholar 

  • Zhao Z, Hewett-Emmett D, Li WH (1998) Frequent gene conversion between human red and green opsin genes. J Mol Evol 46:494–496

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I thank Dr. David Posada and the anonymous referees for their critical and constructive comments on an early draft of the manuscript. Likewise, great gratitude and appreciation are due to Professor Amitabh Joshi (chief editor of Journal of Genetics; Evolutionary and Organismal Biology Unit, Jawaharlal Nehru Centre for Advanced Scientific Research) and Dr. Xin’ai Zhao (Plant Molecular Biology Laboratory, International Rice Research Institute) for their help correcting the writing of the manuscript. This work was supported by an intramural fund from Zhejiang Forestry University (to Q. Liu).

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Correspondence to Qingpo Liu.

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Liu, Q. Gene Conversion and Positive Selection Driving the Evolution of the Caenorhabditis ssp. ZIM/HIM-8 Protein Family. J Mol Evol 68, 217–226 (2009). https://doi.org/10.1007/s00239-009-9203-z

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  • DOI: https://doi.org/10.1007/s00239-009-9203-z

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