Gene conversion occurs within the mating-type locus of Cryptococcus neoformans during sexual reproduction

PLoS Genetics

Volumn 8, Issue 7, 2012, Pages

  Sun, Sheng ^a   Hsueh, Yen Ping ^a,b   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BSP2 GENE; CENTROMERE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; FUNGAL GENE; FUNGAL REPRODUCTION; FUNGAL STRAIN; FUNGUS ISOLATION; GC RICH SEQUENCE; GENE CONVERSION; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE LOCATION; GENE LOCUS; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CODE; GENETIC DISTANCE; GENETIC LINE; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC VARIABILITY; MEIOSIS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PROGENY; RPO41 GENE; SEQUENCE ALIGNMENT;

BASE COMPOSITION; CHROMOSOME MAPPING; CHROMOSOME SEGREGATION; CROSSING OVER, GENETIC; CRYPTOCOCCUS NEOFORMANS; DNA, INTERGENIC; EVOLUTION, MOLECULAR; GENE CONVERSION; GENES, MATING TYPE, FUNGAL; GENETICS, POPULATION; HAPLOIDY; HUMANS; MEIOSIS; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC; REPRODUCTION; SEX CHROMOSOMES;

FILOBASIDIELLA NEOFORMANS; FUNGI; MAMMALIA; ZEA MAYS;

EID: 84864584472     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002810     Document Type: Article

References (63)

1. Malkova A, Swanson J, German M, McCusker JH, Housworth EA, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49-63.
2. Copenhaver GP, Housworth EA, Stahl FW, (2002) Crossover interference in Arabidopsis. Genetics 160: 1631-1639.
3. Haubold B, Kroymann J, Ratzka A, Mitchell-Olds T, Wiehe T, (2002) Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana. Genetics 161: 1269-1278.
4. Hilliker AJ, Clark SH, Chovnick A, (1991) The effect of DNA sequence polymorphisms on intragenic recombination in the rosy locus of Drosophila melanogaster. Genetics 129: 779-781.
5. Frisse L, Hudson RR, Bartoszewicz A, Wall JD, Donfack J, et al. (2001) Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. The American Journal of Human Genetics 69: 831-843.
6. Haber JE, Ira G, Malkova A, Sugawara N, (2004) Repairing a double-strand chromosome break by homologous recombination: revisiting Robin Holliday's model. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 359: 79-86.
7. Chen J-M, Cooper DN, Chuzhanova N, Ferec C, Patrinos GP, (2007) Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet 8: 762-775.
8. Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424-430.
9. Nishant KT, Chen C, Shinohara M, Shinohara A, Alani E, (2010) Genetic analysis of baker's yeast Msh4-Msh5 reveals a threshold crossover level for meiotic viability. PLoS Genet 6: e1001083 doi:10.1371/journal.pgen.1001083.
10. Petes TD, (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2: 360-369.
11. Jeffreys AJ, Kauppi L, Neumann R, (2001) Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat Genet 29: 217-222.
12. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P, (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321-324.
13. Hsueh YP, Idnurm A, Heitman J, (2006) Recombination hotspots flank the Cryptococcus mating-type locus: implications for the evolution of a fungal sex chromosome. PLoS Genet 2: e184 doi:10.1371/journal.pgen.0020184.
14. Shi J, Wolf SE, Burke JM, Presting GG, Ross-Ibarra J, et al. (2010) Widespread gene conversion in centromere cores. PLoS Biol 8: e1000327 doi:10.1371/journal.pbio.1000327.
15. Symington LS, Petes TD, (1988) Meiotic recombination within the centromere of a yeast chromosome. Cell 52: 237-240.
16. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, et al. (2003) Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423: 873-876.
17. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, et al. (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825-837.
18. Jill Pecon S, Sanner-Wachter L, O'Brien SJ, (2000) Novel gene conversion between X-Y homologues located in the nonrecombining region of the Y chromosome in Felidae (Mammalia). PNAS 97: 5307-5312.
19. Fullerton SM, Bernardo Carvalho A, Clark AG, (2001) Local rates of recombination are positively correlated with GC content in the human genome. Molecular Biology and Evolution 18: 1139-1142.
20. Eyre-Walker A, Hurst LD, (2001) The evolution of isochores. Nat Rev Genet 2: 549-555.
21. Marsolier-Kergoat M-C, Yeramian E, (2009) GC content and recombination: Reassessing the causal effects for the Saccharomyces cerevisiae genome. Genetics 183: 31-38.
22. Meunier J, Duret L, (2004) Recombination drives the evolution of GC-content in the human genome. Molecular Biology and Evolution 21: 984-990.
23. Perry J, Ashworth A, (1999) Evolutionary rate of a gene affected by chromosomal position. Current Biology 9: 987-S983.
24. Marais G, (2003) Biased gene conversion: implications for genome and sex evolution. Trends in Genetics 19: 330-338.
25. Galtier N, Piganeau G, Mouchiroud D, Duret L, (2001) GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 159: 907-911.
26. Webster MT, Axelsson E, Ellegren H, (2006) Strong regional biases in nucleotide substitution in the chicken genome. Molecular Biology and Evolution 23: 1203-1216.
27. Birdsell JA, (2002) Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Molecular Biology and Evolution 19: 1181-1197.
28. Matallana-Surget S, Meador JA, Joux F, Douki T, (2008) Effect of the GC content of DNA on the distribution of UVB-induced bipyrimidine photoproducts. Photochemical & Photobiological Sciences 7: 794-801.
29. Kauppi L, Barchi M, Baudat F, Romanienko PJ, Keeney S, et al. (2011) Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331: 916-920.
30. Otto SP, Pannell JR, Peichel CL, Ashman T-L, Charlesworth D, et al. (2011) About PAR: The distinct evolutionary dynamics of the pseudoautosomal region. Trends in Genetics 27: 358-367.
31. Alexander I, (2011) Sex and speciation: The paradox that non-recombining DNA promotes recombination. Fungal Biology Reviews 25: 121-127.
32. D'Souza CA, Kronstad JW, Taylor G, Warren R, Yuen M, et al. (2011) Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. mBio 2: e00342-00310.
33. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, et al. (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307: 1321-1324.
34. Shimodaira H, Hasegawa M, (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 1114.
35. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM, (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
36. Muller HJ, (1964) The relation of recombination to mutational advance. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 1: 2-9.
37. Felsenstein J, (1974) The evolutionary advantage of recombination. Genetics 78: 737-756.
38. Galtier N, (2004) Recombination, GC-content and the human pseudoautosomal boundary paradox. Trends in Genetics 20: 347-349.
39. Marra RE, Huang JC, Fung E, Nielsen K, Heitman J, et al. (2004) A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167: 619-631.
40. Sun S, Xu J, (2007) Genetic analyses of a hybrid cross between serotypes A and D strains of the human pathogenic fungus Cryptococcus neoformans. Genetics 177: 1475-1486.
41. Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, et al. (2004) Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2: e384 doi:10.1371/journal.pbio.0020384.
42. Haber JE, (1998) Mating-type gene switching in Saccharomyces cerevisiae. Annual Review of Genetics 32: 561-599.
43. Strathern JN, Klar AJS, Hicks JB, Abraham JA, Ivy JM, et al. (1982) Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31: 183-192.
44. Birky-Jr CW, Walsh JB, (1992) Biased gene conversion, copy number, and apparent mutation rate differences within chloroplast and bacterial genomes. Genetics 130: 677-683.
45. Khakhlova O, Bock R, (2006) Elimination of deleterious mutations in plastid genomes by gene conversion. The Plant Journal 46: 85-94.
46. Connallon T, Clark AG, (2010) Gene duplication, gene conversion and the evolution of the Y chromosome. Genetics 186: 277-286.
47. Marais GAB, Campos PRA, Gordo I, (2010) Can intra-Y gene conversion oppose the degeneration of the human Y chromosome? A simulation study. Genome Biology and Evolution 2: 347-357.
48. Keller PJ, Knop M, (2009) Evolution of mutational robustness in the yeast genome: a link to essential genes and meiotic recombination hotspots. PLoS Genet 5: e1000533 doi:10.1371/journal.pgen.1000533.
49. Stöck M, Horn A, Grossen C, Lindtke D, Sermier R, et al. (2011) Ever-young sex chromosomes in European tree frogs. PLoS Biol 9: e1001062 doi:10.1371/journal.pbio.1001062.
50. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, et al. (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10: e1001241 doi:10.1371/journal.pbio.1001241.
51. Lin X, Litvintseva AP, Nielsen K, Patel S, Floyd A, et al. (2007) αADα hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLoS Genet 3: e186 doi:10.1371/journal.pgen.0030186.
52. Litvintseva AP, Lin X, Templeton I, Heitman J, Mitchell T, (2007) Many globally isolated AD hybrid strains of Cryptococcus neoformans originated in Africa. PLoS Pathog 3: e114 doi:10.1371/journal.ppat.0030114.
53. Litvintseva AP, Marra RE, Nielsen K, Heitman J, Vilgalys R, et al. (2003) Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell 2: 1162-1168.
54. Moore TDE, Edman JC, (1993) The α-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol Cell Biol 13: 1962-1970.
55. Yan Z, Hull CM, Heitman J, Sun S, Xu J, (2004) SXI1α controls uniparental mitochondrial inheritance in Cryptococcus neoformans. Current Biology 14: R743-744.
56. Yan Z, Hull CM, Sun S, Heitman J, Xu JP, (2007) The mating-type specific homeodomain genes SXI1α and SXI2a coordinately control uniparental mitochondrial inheritance in Cryptococcus neoformans. Current Genetics 51: 187-195.
57. Sun S, Xu J, (2009) Chromosomal rearrangements between serotype A and D strains in Cryptococcus neoformans. PLoS ONE 4: e5524 doi:10.1371/journal.pone.0005524.
58. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
59. Maddison D, Maddison W, (1989) Interactive analysis of phylogeny and character evolution using the computer program MacClade. Folia Primatol (Basel) 53: 190-202.
60. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
61. Swofford D, (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
62. Sawyer S, (2007) GENECONV [version 1.81a]: A computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University in St Louis, available athttp://wwwmathwustledu/~sawyer/geneconv/.
63. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, et al. (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174-181.