Abstract
Saccharomyces species have five TPO genes, TPO1 through TPO5, coding for proteins that are involved in up taking or excreting intracellular spermine, putrescine or spermidine. Here, we investigate the evolutionary fate and functional impacts of gene conversions between these genes. Our results show that gene conversions occurred only between the TPO2 and TPO3 genes of the six Saccharomyces species we studied. They also show that these gene conversions occurred independently in all six species. The facts that they only occur between closely related genes having similar function, and that they are limited to the transmembrane domain of these proteins, suggest that they have little functional impact. These gene conversions therefore likely represent neutral mutations which are not subject to purifying selection.
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References
Alberts B, Bray D, Lewis J (2007) Molecular biology of the cell, 5th edn. Garland Science, New York
Benovoy D, Drouin G (2009) Ectopic gene conversions in the human genome. Genomics 93:27–32
Bischof JM, Chiang AP, Scheetz TE, Stone EM, Casavant TL, Sheffield VC, Braun TA (2006) Genome-wide identification of pseudogenes capable of disease-causing gene conversion. Hum Mutat 27:545–552
Casola C, Zekonyte U, Phillips AD, Cooper DN, Hahn MW (2012) Interlocus gene conversion events introduce deleterious mutations in at least 1% of human genes associated with inherited disease. Genome Res 22:429–435
Chen J-M, Cooper DN, Chuzhanova N, Férec C, Patrinos GP (2007) Gene conversion: mechanisms, evolution and human disease. Nature Rev Genet 8:762–775
Cherry JM, Adler C, Ball C, Chervitz SA, Dwight SS, Hester ET, Jia Y, Juvik G, Roe TY, Schroeder M, Weng S, Botstein D (1998) SGD: saccharomyces genome database. Nucleic Acids Res 26:73–79
Drouin G (2002) Characterization of the gene conversions between the multigene family members of the yeast genome. J Mol Evol 55:14–23
Drouin G, Prat F, Ell M, Clarke GD (1999) Detecting and characterizing gene conversions between multigene family members. Mol Biol Evol 16:1369–1390
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Sys Biol 52:696–704
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Hiwatashi T, Mikami A, Katsumura T, Suryobroto B, Perwitasari-Farajallah D, Malaivijitnond S, Siriaroonrat B, Oota H, Goto S, Kawamura S (2011) Gene conversion and purifying selection shape nucleotide variation in gibbon L/M opsin genes. BMC Evol Biol 11:312
Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48:506–512
Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160
Morris RT, Drouin G (2010) Ectopic gene conversions in the genome of ten hemiascomycete yeast species. Int J Evol Biol 2011:970768
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
Petronella N, Drouin G (2011) Gene conversions in the growth hormone gene family of primates: stronger homogenizing effects in the Hominidae lineage. Genomics 98:173–181
Petronella N, Drouin G (2014) Purifying selection against gene conversions in the folate receptor genes of primates. Genomics 103:40–47
Poulin R, Casero RA, Soulet D (2012) Recent advances in the molecular biology of metazoan polyamine transport. Amino Acids 42:711–723
Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804
Sawyer SA (1999) GENECONV: A computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University in St. Louis. Available at http://www.math.wustl.edu/~sawyer
Tachihara K, Uemura T, Kashiwagi K, Igarashi K (2005) Excretion of putrescine and spermidine by the protein encoded by YKL174c (TPO5) in Saccharomyces cerevisiae. J Biol Chem 280:12637–12642
The UniProt Consortium (2014) Activities at the universal protein resource (UniProt). Nucleic Acids Res 42:D191–D198
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific GAP penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tomitori H, Kashiwagi K, Sakata K, Kakinuma Y, Igarashi K (1999) Identification of a gene for a polyamine transport protein in yeast. J Biol Chem 274:3265–3267
Tomitori H, Kashiwagi K, Asakawa T, Yoshimi K, Michael AJ, Kazuei I (2001) Multiple polyamine transport systems on the vacuolar membrane in yeast. Biochem J 352:681–688
Uemura T, Tachihara K, Tomitori H, Kashiwagi K, Igarashi K (2005) Characteristics of the polyamine transporter TPO1 and regulation of its activity and cellular localization by phosphorylation. J Biol Chem 280:9646–9652
Xu S, Clark T, Zheng H, Vang S, Li R, Wong GK, Wang J, Zheng X (2008) Gene conversion in the rice genome. BMC Genom 9:93
Zid M, Drouin G (2013) Gene conversions are under purifying selection in the carcinoembryonic antigen immunoglobulin gene families of primates. Genomics 102:301–309
Zid M, Drouin G (2014) Gene conversions are frequent but not under positive selection in the Siglec gene families of primates. Genome (in press)
Acknowledgments
We thank the two anonymous referees for their constructive comments. This work was supported by a Discovery Grant from the Natural Science and Engineering Research Council of Canada to G. D. and by an Undergraduate Research Opportunity Program scholarship from the University of Ottawa to G.S. and G.D.
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Communicated by S. Hohmann.
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Sampathkumar, G., Drouin, G. Purifying selection against gene conversions between the polyamine transport (TPO) genes of Saccharomyces species. Curr Genet 61, 67–72 (2015). https://doi.org/10.1007/s00294-014-0445-y
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DOI: https://doi.org/10.1007/s00294-014-0445-y