Domain-specific regulation of recombination in Caenorhabditis elegans in response to temperature, age and sex

Genetics

Volumn 180, Issue 2, 2008, Pages 715-726

  Lim, Jaclyn G Y ^a,b   Stine, Rachel R W ^a,c,d   Yanowitz, Judith L ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c GOUCHER COLLEGE   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGE DISTRIBUTION; ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME 3; CHROMOSOME MAP; CONTROLLED STUDY; CROSSING OVER; FEMALE; GENETIC RECOMBINATION; HERMAPHRODITISM; MALE; MEIOSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SEX CHROMOSOME; SEX DIFFERENCE; SPERM; TEMPERATURE DEPENDENCE; X CHROMOSOME; AGE; ANIMAL; BIOLOGICAL MODEL; CHROMOSOME; GENE; GENETICS; METABOLISM; PHYSIOLOGY; REPRODUCTION; SPERMATOCYTE; TEMPERATURE;

CAENORHABDITIS ELEGANS;

AGE FACTORS; ANIMALS; CAENORHABDITIS ELEGANS; CHROMOSOME MAPPING; CHROMOSOMES; CROSSING OVER, GENETIC; FEMALE; GENES, HELMINTH; MALE; MODELS, GENETIC; OOCYTES; RECOMBINATION, GENETIC; REPRODUCTION; SPERMATOCYTES; TEMPERATURE; X CHROMOSOME;

EID: 58149335559     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.090142     Document Type: Article

References (69)

1. BARNES, T. M., Y. KOHARA, A. COULSON and S. HEKIMI, 1995 Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141: 159-179.
2. BARTH, S., A. E. MELCHINGER, B. DEVEZI- SAVULA and T. LUBBERSTEDT, 2000 A high-throughput system for genome-wide measurement of genetic recombination in Arabidopsis thaliana based on transgenic markers. Funct. Integr. Genomics 1: 200-206.
3. BAUDAT, F., and A. NICOLAS, 1997 Clustering of meiotic double-strand breaks on yeast chromosome III. Proc. Natl. Acad. Sci. USA 94: 5213-5218.
4. BENDER, L. B., R. CAO, Y. ZHANG and S. STROME, 2004 The MES-2/MES-3/MES-6 complex and regulation of histone H3 methylation in C. elegans. Curr. Biol. 14: 1639-1643.
5. BENDER, L. B., J. SUH, C. R. CARROLL, Y. FONG, I. M. FINGERMAN et al., 2006 MES-4: an autosome-associated histone methyltransferase that participates in silencing the X chromosomes in the C. elegans germ line. Development 133: 3907-3917.
6. BLAT, Y., R. U. PROTACIO, N. HUNTER and N. KLECKNER, 2002 Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111: 791-802.
7. BLITZBLAU, H. G., G. W. BELL, J. RODRIGUEZ, S. P. BELL and A. HOCHWAGEN, 2007 Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Curr. Biol. 17: 2003-2012.
8. BORDE, V., T. C. WU and M. LICHTEN, 1999 Use of a recombination reporter insert to define meiotic recombination domains on chromosome III of Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 4832-4842.
9. BORNER, G. V., N. KLECKNER and N. HUNTER, 2004 Crossover/non-crossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
10. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
11. CARLTON, P. M., A. P. FARRUGGIO and A. F. DERNBURG, 2006 A link between meiotic prophase progression and crossover control. PLoS Genet. 2: 119-128.
12. CHIKASHIGE, Y., C. TSUTSUMI, M. YAMANE, K. OKAMASA, T. HARAGUCHI et al., 2006 Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59-69.
13. COOP, G., X. WEN, C. OBER, J. K. PRITCHARD and M. PRZEWORSKI, 2008 High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319: 1395-1398.
14. DALY, M. J., J. D. RIOUX, S. F. SCHAFFNER, T. J. HUDSON and E. S. LANDER, 2001 High-resolution haplotype structure in the human genome. Nat. Genet. 29: 229-232.
15. DAVIS, M. W., M. HAMMARLUND, T. HARRACH, P. HULLETT, S. OLSEN et al., 2005 Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics 6: 118.
16. DE MASSY, B., 2003 Distribution of meiotic recombination sites. Trends Genet. 19: 14-22.
17. DORMAN, E. R., A. M. BUSHEY and V. G. CORCES, 2007 The role of insulator elements in large-scale chromatin structure in interphase. Semin. Cell Dev. Biol. 18: 682-690.
18. FUKUDA, T., K. KUGOU, H. SASANUMA, T. SHIBATA and K. OHTA, 2008 Targeted induction of meiotic double-strand breaks reveals chromosomal domain-dependent regulation of Spo11 and interactions among potential sites of meiotic recombination. Nucleic Acids Res. 36: 984-997.
19. FUNG, J. C., B. ROCKMILL, M. ODELL and G. S. ROEDER, 2004 Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795-802.
20. GABRIEL, S. B., S. F. SCHAFFNER, H. NGUYEN, J. M. MOORE, J. ROY et al., 2002 The structure of haplotype blocks in the human genome. Science 296: 2225-2229.
21. GARVIN, C., R. HOLDEMAN and S. STROME, 1998 The phenotype of mes-2, mes-3, mes-4, and mes-6, maternal-effect genes required for survival of the germline in Caenorhabditis elegans, is sensitive to chromosome dosage. Genetics 148: 167-185.
22. GERTON, J. L., J. DERISI, R. SHROFF, M. LICHTEN, P. O. BROWN et al., 2000 Inaugural article: global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97: 11383-11390.
23. GLYNN, E. F., P. C. MEGEE, H. G. YU, C. MISTROT, E. UNAL et al., 2004 Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol. 2: E259.
24. GOLDSTEIN, P., 1982 The synaptonemal complexes of Caenorhabditis elegans: pachytene karyotype analysis of male and hermaphrodite wild-type and him mutants. Chromosoma 86: 577-593.
25. HAMMARLUND, M., M. W. DAVIS, H. NGUYEN, D. DAYTON and E. M. JORGENSEN, 2005 Heterozygous insertions alter crossover distribution but allow crossover interference in Caenorhabditis elegans. Genetics 171: 1047-1056.
26. HARPER, L., I. GOLUBOVSKAYA and W. Z. CANDE, 2004 A bouquet of chromosomes. J. Cell Sci. 117: 4025-4032.
27. HASSOLD, T., S. SHERMAN and P. HUNT, 2000 Counting cross-overs: characterizing meiotic recombination in mammals. Hum. Mol. Genet. 9: 2409-2419.
28. HILLERS, K. J., 2004 Crossover interference. Curr. Biol. 14: R1036-R1037.
29. HILLERS, K. J., and A. M. VILLENEUVE, 2003 Chromosome-wide control of meiotic crossing over in C. elegans. Curr. Biol. 13: 1641-1647.
30. HIRSH, D., D. OPPENHEIM and M. KLASS, 1976 Development of the reproductive system of Caenorhabditis elegans. Dev. Biol. 49: 200-219.
31. HODGES, C. A., E. REVENKOVA, R. JESSBERGER, T. J. HASSOLD and P. A. HUNT, 2005 SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat. Genet. 37: 1351-1355.
32. HODGKIN, J., H. R. HORVITZ and S. BRENNER, 1979 Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91: 67-94.
33. HUGHES, S., K. EVASON, C. XIONG and K. KORNFELD, 2007 Genetic and pharmacologic factors that influence reproductive aging in nematodes. PLoS Genet. 3: 254-265.
34. INTERNATIONAL HAPMAP CONSORTIUM, 2007 A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861.
35. JARAMILLO-LAMBERT, A., M. ELLEFSON, A. M. VILLENEUVE and J. ENGEBRECHT, 2005 Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev. Biol. 308: 206-221.
36. KELLY, K. O., A. F. DERNBURG, G. M. STANFIELD and A. M. VILLENEUVE, 2000 Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156: 617-630.
37. KELLY, W. G., and A. FIRE, 1998 Chromatin silencing and the maintenance of a functional germline in Caenorhabditis elegans. Development 125: 2451-2456.
38. KELLY, W. G., C. E. SCHANER, A. F. DERNBURG, M. H. LEE, S. K. KIM et al., 2002 X-chromosome silencing in the germline of C. elegans. Development 129: 479-492.
39. KLASS, M. R., 1977 Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech. Ageing Dev. 6: 413-429.
40. KOVALCHUK, I., O. KOVALCHUK, A. ARKHIPOV and B. HOHN, 1998 Transgenic plants are sensitive bioindicators of nuclear pollution caused by the Chernobyl accident. Nat. Biotechnol. 16: 1054-1059.
41. LACEFIELD, S., and A. W. MURRAY, 2007 The spindle checkpoint rescues the meiotic segregation of chromosomes whose crossovers are far from the centromere. Nat. Genet. 39: 1273-1277.
42. LAMB, B. C., 1969 Related and unrelated changes in conversion and recombination frequencies with temperature in Sordaria fimicola, and their relevance to hybrid-DNA models of recombination. Genetics 62: 67-78.
43. LAMBIE, E. J., and G. S. ROEDER, 1986 Repression of meiotic crossing over by a centromere (CEN3) in Saccharomyces cerevisiae. Genetics 114: 769-789.
44. LENORMAND, T., and J. DUTHEIL, 2005 Recombination difference between sexes: a role for haploid selection. PLoS Biol. 3: e63.
45. LEWIS, J. A., and J. T. FLEMING, 1995 Basic culture methods in Caenorhabditis elegans, pp. 3-29 in Modern Biological Analysis of an Organism, Vol. 48, edited by H. F. EPSTEIN and D. C. SHAKES. Academic Press, San Diego.
46. LITHGOW, G. J., T. M. WHITE, D. A. HINERFELD and T. E. JOHNSON, 1994 Thermotolerance of a long-lived mutant of Caenorhabditis elegans. J. Gerontol. 49: B270-B276.
47. MAVOR, J. W., and H. K. SVENSON, 1923 X-Rays and crossing over. Science 58: 124-126.
48. MENEELY, P. M., A. F. FARAGO and T. M. KAUFFMAN, 2002 Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162: 1169-1177.
49. MULLER, H. J., 1925 The regionally differential effect of X rays on crossing over in autosomes of Drosophila. Genetics 10: 470-507.
50. NABESHIMA, K., A. M. VILLENEUVE and K. J. HILLERS, 2004 Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168: 1275-1292.
51. NICOLAS, A., 1998 Relationship between transcription and initiation of meiotic recombination: toward chromatin accessibility. Proc. Natl. Acad. Sci. USA 95: 87-89.
52. PAIGEN, K., J. P. SZATKIEWICZ, K. SAWYER, N. LEAHY, E. D. PARVANOV et al., 2008 The recombinational anatomy of a mouse chromosome. PLoS Genet. 4: e1000119.
53. PETKOV, P. M., K. W. BROMAN, J. P. SZATKIEWICZ and K. PAIGEN, 2007 Crossover interference underlies sex differences in recombination rates. Trends Genet. 23: 539-542.
54. PLOUGH, H. H., 1917 The effect of temperature on linkage in the second chromosome of Drosophila. Proc. Natl. Acad. Sci. USA 3: 553-555.
55. REINKE, V., H. E. SMITH, J. NANCE, J. WANG, C. VAN DOREN et al., 2000 A global profile of germline gene expression in C. elegans. Mol. Cell 6: 605-616.
56. ROBINE, N., N. UEMATSU, F. AMIOT, X. GIDROL, E. BARILLOT et al., 2007 Genome-wide redistribution of meiotic double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 27: 1868-1880.
57. ROSE, A. M., and D. L. BAILLIE, 1979 The effect of temperature and parental age on recombination and nondisjunction in Caenorhabditis elegans. Genetics 92: 409-418.
58. SALEEM, M., B. C. LAMB and E. NEVO, 2001 Inherited differences in crossing over and gene conversion frequencies between wild strains of Sordaria fimicola from "Evolution Canyon." Genetics 159: 1573-1593.
59. SCHERTHAN, H., 2007 Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64: 117-124.
60. SCHEWE, M. J., D. T. SUZUKI and U. ERASMUS, 1971 The genetic effects of mitomycin C in Drosophila melanogaster. II. Induced meiotic recombination. Mutat. Res. 12: 269-279.
61. SEXTON, T., H. SCHOBER, P. FRASER and S. M. GASSER, 2007 Gene regulation through nuclear organization. Nat. Struct. Mol. Biol. 14: 1049-1055.
62. STERN, C., 1926 An effect of temperature and age on crossing-over in the first chromosome of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 12: 530-532.
63. TSAI, C. J., D. G. METS, M. R. ALBRECHT, P. NIX, A. CHAN et al., 2008 Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev. 22: 194-211.
64. WAGNER, N., and G. KROHNE, 2007 LEM-domain proteins: new insights into lamin-interacting proteins. Int. Rev. Cytol. 261: 1-46.
65. WANG, B. D., and A. STRUNNIKOV, 2008 Transcriptional homogenization of rDNA repeats in the episome-based nucleolus induces genome-wide changes in the chromosomal distribution of condensin. Plasmid 59: 45-53.
66. WANG, J., K. CHUANG, M. AHLUWALIA, S. PATEL, N. UMBLAS et al., 2005 High-throughput SNP genotyping by single-tube PCR with Tm-shift primers. Biotechniques 39: 885-893.
67. WICKS, S. R., R. T. YEH, W. R. GISH, R. H. WATERSTON and R. H. PLASTERK, 2001 Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28: 160-164.
68. ZETKA, M. C., and A. M. ROSE, 1990 Sex-related differences in crossing over in Caenorhabditis elegans. Genetics 126: 355-363.
69. ZETKA, M. C, and A. M. ROSE, 1995 The genetics of meiosis in Caenorhabditis elegans. Trends Genet. 11: 27-31.