Chromosoma

, Volume 102, Issue 2, pp 71–80 | Cite as

Sex chromosomes, recombination, and chromatin conformation

  • Bruce D. McKee
  • Mary Ann Handel
Chromosoma Focus

Abstract

We review what is known about the transcriptional inactivation and condensation of heteromorphic sex chromosomes in contrast to the activation of homomorphic sex chromosomes during meiotic prephase in animals. We relate these cytological and transcriptional features to the recombination status of the sex chromosomes. We propose that sex chromosome condensation is a meiotic adaptation to prevent the initiation of potentially damaging recombination events in nonhomologous regions of the X and Y chromosome.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andina RJ (1978) A study of X chromosome regulation during oogenesis in the mouse. Exp Cell Res 111: 211–218Google Scholar
  2. Avner P, Bishop C, Amar L, Cambrou J, Hatat D, Arnaud D, Mattei M-G (1987) Mapping the mouse X chromosome: possible symmetry in the location of a family of sequences on the mouse X and Y chromosomes. Development 101 [Suppl] 107–116Google Scholar
  3. Baker WK (1958) Crossing over in heterochromatin. Am Nat 92: 59–60Google Scholar
  4. Becak ML, Becak W (1981) Behaviour of the ZW sex bivalent in the snake Bothrops jararaca. Chromosoma 83: 289–293Google Scholar
  5. Bhalla SC (1971) A crossover suppressor-enhancer system in the mosquito Aedes aegyptii. Can J Genet Cytol 13:561–577Google Scholar
  6. Bishop DK, Park D, Xu L, Kleckner N (1992) DMCl: A meiosis-specific yeast homolog of E. coli recA required for recombination synaptonemal complex formation, and cell cycle progression. Cell 69: 439–456Google Scholar
  7. Bonaccorsi S, Pisano C, Puoti F, Gatti M (1988) Y chromosome loops in Drosophila melanogaster. Genetics 120: 1015–1034Google Scholar
  8. Bonaccorsi S, Gatti M, Pisano C, Lohe A (1990) Transcription of a satellite DNA on two Y chromosome loops of Drosophila melanogaster. Chromosoma 99: 260–266Google Scholar
  9. Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin/Cummings, Menlo Park, CaliforniaGoogle Scholar
  10. Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089–1101Google Scholar
  11. Carpenter ATC, Baker B (1982) On the control of the distribution of meiotic exchange in Drosophila melanogaster. Genetics 101: 81–89Google Scholar
  12. Chandley AC, McBeath S (1987) DNase I hypersensitivity characterizes the XY pairing region at meiosis in man. Chromosomes Today 9:196–207Google Scholar
  13. Charlesworth B (1989) The evolution of sex and recombination. Trends Ecol Evol 4:264–267Google Scholar
  14. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23:251–287Google Scholar
  15. Church K (1979) The grasshopper X chromosome. II. Negative heteropycnosis, transcription activities and compartmentalization during spermatogonial stages. Chromosoma 71: 359–370Google Scholar
  16. Cooper KW (1941) An investigation of the aberrant chromosome behavior in the male germ cells of flies parasitic on tropical bats and vultures Yearbook, Am Philos Soc 1941: 122–127Google Scholar
  17. Cooper KW (1950) Normal spermatogenesis in Drosophila. In: Demerec G (ed) The biology of Drosophila. Hafner, New Haven, Connecticut, pp 1–61Google Scholar
  18. Ellis N, Goodfellow PN (1989) The mammalian pseudoautosomal region. Trends Genet 5: 406–410Google Scholar
  19. Emmart EW (1935) Studies of the chromosomes of Anastrepha (Diptera: Trypetidae). Proc Entomol Soc Wash 37: 119–135Google Scholar
  20. Epstein CJ (1969) Mammalian oocytes: X chromosome activity. Science 163: 1078–1079Google Scholar
  21. Fahmy OG (1949) The mechanism of chromosome pairing during meiosis in male Apolipthisa subincana (Mycetophelidae, Diptera). J Genet 49:246–263Google Scholar
  22. Fischer Lindahl K (1991) His and hers recombinational hotspots. Trends Genet 7: 723–280Google Scholar
  23. Fisk JH (1989) Karyotype and achiasmatic female meiosis in Helicoverpa armigera (Hudner) and H. punctigera (Wallengren) (Lepidoptera: Noctuidae). Genome 32:967–971Google Scholar
  24. Forejt J (1982) X-Y involvement in male sterility caused by autosome translocations—a hypothesis. In: Crosignani PG, Rubin BL (eds) Genetic control of gamete production and function. Academic Press, New York, pp 135–151Google Scholar
  25. Game JC, Sitney KC, Cook VE, Mortimer RK (1989) Use of a ring chromosome and pulsed-field gels to study interhomolog recombination, double-strand DNA breaks and sister chromatid exchange in yeast. Genetics 123: 695–713Google Scholar
  26. Gartler SM, Rivest M (1983) Evidence for X-linkage of steroid sulfatase in the mouse: Steroid sulfatase levels in oocytes of XX and XO mice. Genetics 103: 137–141Google Scholar
  27. Gartler SM, Liskay RM, Campbell BK, Sparkes R, Gant N (1972) Evidence for two functional X chromosomes in human oocytes. Cell Differ 1:215–218Google Scholar
  28. Gartler SM, Andina R, Gant N (1975) Ontogeny of X-chromosome inactivation in the female germ line. Exp Cell Res 91:454–457Google Scholar
  29. Gartler SM, Rivest M, Cole RE (1980) Cytological evidence for an inactive X chromosome in murine oogonia. Cytogenet Cell Genet 28:203–207Google Scholar
  30. Gatti M (1982) Sister chromatid exchanges in Drosophila. In: Wolff S (ed) Sister chromatid exchange. Wiley, New York, pp 267–296Google Scholar
  31. Gillies CB (1989) Fertility and chromosome pairing: Recent studies in plants and animals. CRC Press, Boca Raton, FloridaGoogle Scholar
  32. Gold B, Fujimoto H, Kramer JM, Erickson RP, Hecht NB (1983) Haploid accumulation and translational control of phosphoglycerate kinase-2 messenger RNA during mouse spermatogenesis. Dev Biol 98:392–399Google Scholar
  33. Gould-Somero M, Holland L (1974) The timing of RNA synthesis for spermiogenesis in organ cultures of Drosophila melanogaster testes. Wilhelm Roux' Arch 174:133–148Google Scholar
  34. Grunstein M (1990) Nucleosomes: regulators of transcription. Trends Genet 6:395–400Google Scholar
  35. Haber JE, Leung W-Y, Borts RH, Lichten M (1991) The frequency of meiotic recombination in yeast is independent of the number and position of homologous donor sequences: Implications for chromosome pairing. Proc Natl Acad Sci USA 88:1120–1124Google Scholar
  36. Hale DW, Hunt PA, Tucker PK, Eicher EM (1991) Synapsis and obligate recombination between sex chromosomes of male laboratory mice carrying the Y* rearrangement. Cytogenet Cell Genet 57:231–239Google Scholar
  37. Handel MA, Shannon M, Caldwell KA (1993) Sex-chromosome activity during meiosis. In: Meiosis II: Contemporary approaches to the study of meiosis. AAAS Press, Washington, D.C. (in press)Google Scholar
  38. Hartwell LH, Weinert TA (1989) Checkpoints: Controls that ensure the order of cell cycle events. Science 246:629–634Google Scholar
  39. Hawley RS (1988) Exchange and chromosomal segregation in eucaryotes. In: Kucherlapati R, Smith GR (eds) Genetic recombination. American Society for Microbiology, Washington, D.C., pp 497–527Google Scholar
  40. Henderson SA (1964) RNA synthesis during male meiosis and spermiogenesis. Chromosomal 15:345–366Google Scholar
  41. Hennig W (1967) Untersuchungen zur Struktur und Funktion des Lampenborsten-Y-Chromosoms in der Spermatogenese von Drosophila. Chromosoma 22:294–357Google Scholar
  42. Hennig W (1987) The Y chromosomal lampbrush loops of Drosophila. In: Hennig W (ed) Results and problems in cell differentiation, vol. 14. Structure and function of eukaryotic chromosomes. Springer, Berlin Heidelberg New York, pp 133–146Google Scholar
  43. Hennig W (1988) The Y chromosome of Drosophila. In: Adolph KW (ed) Chromosomes: eukaryotic, prokaryotic and viral, vol I. CRC Press, Boca Raton, Florida, pp 213–238Google Scholar
  44. John B (1957) XY segregation in the crane fly Tipula maxima (Diptera: Tipulidae). Heredity 11:209–216Google Scholar
  45. John B (1988) The biology of heterochromatin. In: Verma RS (ed) Molecular and structural aspects of heterochromatin. Cambridge University Press, Cambridge, pp 1–147Google Scholar
  46. John B (1990) Meiosis. Cambridge University Press, CambridgeGoogle Scholar
  47. Johnston PG (1981) X chromosome activity in female germ cells of mice heterozygous for Searle's translocation T(X;16)16H. Genet Res 37:317–322Google Scholar
  48. Joslyn G (1988) Cloning and analysis of spermatogenic genes in Drosophila melanogaster. Ph.D. dissertation, University of California, San DiegoGoogle Scholar
  49. Jost E (1971) Meiosis in the male of Culex pipiens and Aedes albopictus and fertilization in the Culex pipiens complex. Can J Genet Cytol 13:237–250Google Scholar
  50. Kezer J, Sessions SK, Leon P (1989) The meiotic structure and behavior of the strongly heteromorphic X/Y sex chromosome of neotropical plethodontid salamanders of the genus Oedipina. Chromosoma 98:433–442Google Scholar
  51. Kierszenbaum AL, Tres LL (1974a) Nucleolar and perichromosomal RNA synthesis during meiotic prophase in the mouse testis. J Cell Biol 60:39–53Google Scholar
  52. Kierszenbaum AL, Tres LL (1974b) Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J Cell Biol 63:923–935Google Scholar
  53. Kitzmiller JB (1976) Genetics, cytogenetics and evolution of mosquitoes. Adv Genet 18:315–433Google Scholar
  54. Kofman-Alfaro S, Chandley AC (1970) Meiosis in the male mouse. An autoradiographic investigation. Chromosoma 31:404–420Google Scholar
  55. Kratzer PG, Chapman VM (1981) X chromosome reactivation in oocytes of Mus caroli. Proc Natl Acad Sci USA 78:3093–3097Google Scholar
  56. Kremer H, Hennig W, Dijkhof R (1986) Chromatin organization in the male germ line of Drosophila hydei. Chromosoma 94:147–161Google Scholar
  57. Latos-Bielenska A, Vogel W (1992) Demonstration of replication patterns in the last premeiotic S-phase of male Chinese hamsters after BrdU pulse labeling. Chromosoma 101:279–283Google Scholar
  58. LeCalvez J (1947) Morphologie et comportement des chromosomes dans la spermatogenese de quelques mycetophilides. Chromosoma 3:137–165Google Scholar
  59. Lifschytz E, Lindsley DL (1972) The role of X-chromosome inactivation during spermatogenesis. Proc Natl Acad Sci USA 69:182–186Google Scholar
  60. Lindsley DL, Sandler L (1977) The genetic analysis of meiosis in female Drosophila melanogaster. Philos Trans R Soc Lond [Biol] 277:295–312Google Scholar
  61. Lindsley DL, Tokuyasu KT (1980) Spermatogenesis. In: Asburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2d. Academic Press, London, pp 225–294Google Scholar
  62. Martin J (1967) Meiosis in inversion heterozygotes in Chronomidae. Can J Genet Cytol 9:255–268Google Scholar
  63. McCarrey JR, Thomas K (1987) Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326:501–505Google Scholar
  64. Metz CW, Nonidez JF (1924) The behavior of the nucleus and chromosomes during spermatogenesis in the robber fly Lasiopogon birittatus. Biol Bull Woods Hole 46:153–164Google Scholar
  65. Miklos GLG (1974) Sex chromosome pairing and male fertility. Cytogenet Cell Genet 13:558–577Google Scholar
  66. Miklos GLG, Yamamoto M-T, Davies J, Pirrotta V (1988) Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the β-heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci USA 85:2051–2055Google Scholar
  67. Mittwoch V (1983) Heteropycnosis and the activity of X chromosomes: History and prospects. In: Sandberg AA (ed) Cytogenetics of the mammalian X chromosome, Part A. Basic mechanisms of X chromosome behavior. Liss, New York, pp 251–270Google Scholar
  68. Mohr OL (1916) Studien über die Chromatinreifung der männlichen Geschlechtszellen bei Locusta viridissima. Arch Biol (Liege) 29:579Google Scholar
  69. Monesi V (1965) Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma 17:11–21Google Scholar
  70. Monk M, McLaren A (1981) X-chromosome activity in foetal germ cells of the mouse. J Embryol Exp Morphol 63:75–84Google Scholar
  71. Montgomery EA, Huang S-M, Langley CH, Judd BH (1991) Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129:1085–1098Google Scholar
  72. Mukherjee AB, Rees DM (1970) Spermatogenesis in the mosquito Aedes dorsalis. Cytologia 35:213–219Google Scholar
  73. Mukherjee AB, Rees CM, Mukherjee AB (1970) A comparative study of the mosquito karyotypes. Cytologia 35:57–62Google Scholar
  74. Narang N, Narang S, Kitzmiller JB (1972) Karyological studies on four species of Anopheles subgenus Cellia. Caryologia 25:259–274Google Scholar
  75. Nicolas A, Treco D, Schultes NP, Szostak JW (1989) An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature 338:35–39Google Scholar
  76. Nokkala S, Nokkala C (1983) Achiasmatic male meiosis in two species of Saldula (Saldidae. Hemiptera). Hereditas 99:131–134Google Scholar
  77. Nokkala S, Nokkala C (1984) Achiasmatic male meiosis in the Heteropteron genus Nabis (Nabidae, Hemiptera). Hereditas 101:31–35Google Scholar
  78. Nokkala S, Nokkala C (1986a) Achiasmatic male meiosis of collochore type in the Heteropteran family Niridae. Hereditas 105:193–197Google Scholar
  79. Nokkala S, Nokkala C (1986b) Achiasmatic male meiosis in Anthocoris aemorum (L.) (Anthocoridae, Hemiptera). Hereditas 105:287–289Google Scholar
  80. Odartchenko N, Pavillard M (1970) Late DNA replication in male mouse meiotic chromosomes. Science 167:1133–1134Google Scholar
  81. Ohno S (1964) Life history of female germ cells in mammals. In: Proceedings 2nd International Conference on Cytogenetics. Malforma, The National Foundation, New York, pp 36–40Google Scholar
  82. Ohno S, Makino S (1961) The single-X nature of sex chromatin in man. Lancet 1:78–79Google Scholar
  83. Olivieri G, Oliviera A (1965) Autoradiographic study of nucleic acid synthesis during spermatogenesis in Drosophila melanogaster. Mutat Res 2:366–380Google Scholar
  84. Padmore R, Cao L, Kleckner N (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66:1239–1256Google Scholar
  85. Painter TS (1924) Studies in mammalian spermatogenesis. III. The fate of the chromatin-nucleolus in the opossum. J Exp Zool 39:197–247Google Scholar
  86. Petes TD, Hill CW (1988) Recombination between repeated genes in microorganisms. Annu Rev Genet 22:147–168Google Scholar
  87. Raman R, Das P (1991) Mammalian sex chromosomes. III. Activity of pseudoautosomal steroid sulfatase enzyme during spermatogenesis in Mus musculus. Somatic Cell Mol Genet 17:429–433Google Scholar
  88. Raman R, Singh AP, Nanda I (1988) DNase I nick translation in situ on meiotic chromosomes of the mouse, Mus musculus. J Cell Sci 90:629–634Google Scholar
  89. Ribbands CRR (1941) Meiosis in Diptera. I. Prophase associations of non-homologous chromosomes and their relation to mutual attraction between centromeres, centrosomes and chromosome ends. J Genet 41:411–444Google Scholar
  90. Richler C, Uliel E, Kerem B-S, Wahrman J (1987) Regions of active chromatin conformation in “inactive” male meiotic sex chromosomes of the mouse. Chromosoma 95:167–170Google Scholar
  91. Rishikesh N (1959) Chromosome behavior during spermatogenesis of Anopheles stephensi Sensu stricto. Cytologia 24:447–458Google Scholar
  92. Roberts PA (1965) Difference in the behavior of eu- and heterochromatin: crossingover. Nature 205:725–726Google Scholar
  93. Rouyer F, Simmler M-C, Johnson C, Vergnaud G, Cooke H, Weissenbach J (1986) A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature 319:291–295Google Scholar
  94. Sachs L (1954) Sex-linkage and the sex chromosomes in man. Ann Eugen 18:255–261Google Scholar
  95. Separovic ER, Chandley AC (1987) Lack of evidence that the XqYq pairing tips at meiosis in the mouse show hypersensitivity to DNase I. Chromosoma 95:290–294Google Scholar
  96. Shenkar R, Shen M, Arnheim N (1991) DNase I-hypersensitive sites and transcription factor binding motifs within the mouse Eβ meiotic recombination hot spot. Mol Cell Biol 11:1813–1819Google Scholar
  97. Singer-Sam J, Robinson MO, Bellve AR, Simon MI, Riggs AD (1990) Measurement by quantitative PCR of changes in HPRT, PGK-1, PGK-2, APRT, MTase and Zfy gene transcripts during mouse spermatogenesis. Nucleic Acids Res 18:1255–1259Google Scholar
  98. Solari AJ (1974) The behavior of the XY pair in mammals. Int Rev Cytol 38:273–317Google Scholar
  99. Solari AJ (1977) Ultrastructure of the synaptic autosomes and the ZW bivalent in chicken oocytes. Chromosoma 64:155–165Google Scholar
  100. Solari AJ (1989) Sex chromosome pairing and fertility in the heterogametic sex of mammals and birds. In: Gillies CB (ed) Fertility and chromosome pairing: Recent studies in plants and animals. CRC Press, Boca Raton, Florida, pp 77–107Google Scholar
  101. Solari AJ (1992) Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Cell Genet 59:52–56Google Scholar
  102. Soriano P, Keitges EA, Schorderet DF, Harbers K, Gartler SM, Jaenisch R (1987) High rate of recombination and double crossovers in the mouse pseudoautosomal region during male meiosis. Proc Natl Acad Sci USA 84:7218–7220Google Scholar
  103. Stapleton A, Petes TD (1991) The Tn3 β-lactamase gene acts as a hot spot for meiotic recombination in yeast. Genetics 127:39–51Google Scholar
  104. Stevens NM (1980) A study of the germ cells of certain Diptera with reference to the heterochromosomes and the phenomenon of synapsis. J Exp Zool 5:359–374Google Scholar
  105. Stevens NM (1911) Further studies on heterochromosomes in mosquitoes. Biol Bull 20:109–120Google Scholar
  106. Stoppa-Lyonnet D, Carter PE, Meo T, Tosi M (1990) Clusters of intragenic Alu repeats predispose the human C1 inhibitor locus to deleterious rearrangements. Proc Natl Acad Sci USA 87:1551–1555Google Scholar
  107. Sun H, Treco D, Schultes NP, Szostak JW (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338:87–90Google Scholar
  108. Sun H, Treco D, Szostak JW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific doublestrand breaks at the ARG4 recombination initiation site. Cell 64:1155–1161Google Scholar
  109. Takakubo F, Dahl H-HM (1992) The expression pattern of the pyruvate dehydrogenase ELα subunit genes during spermatogenesis in the adult mouse. Exp Cell Res 199:39–49Google Scholar
  110. Thomas BJ, Rothstein R (1991) Sex, maps and imprinting. Cell 64:1–4Google Scholar
  111. Utakoji T (1966) Chronology of nucleic acid synthesis in meiosis of the male Chinese hamster. Exp Cell Res 42:585–596Google Scholar
  112. Wagstaff JE, Klapholz S, Waddell CS, Jensen L, Esposito RE (1985) Meiotic exchange within and between chromosomes requires a common Rec function in Saccharomyces cerevisiae. Mol Cell Biol 5:3532–3544Google Scholar
  113. Weber L, Byers B (1992) A RAD 9-dependent checkpoint blocks meiosis of cdc 13 yeast cells. Genetics 131:55–63Google Scholar
  114. White GB (1980) Academic and applied aspects of mosquito cytogenetics. In: Blackman RL, Hewitt GM, Ashburner M (eds) Insect cytogenetics. Blackwell, Oxford, pp 245–274Google Scholar
  115. White MJD (1933) Tetraploid spermatocytes in a locust, Schistocerca gregaria. Cytologia 5:135–139Google Scholar
  116. White MJD (1938) A new and anomalous type of meiosis in a mantid, Callimantis antillorum Saussune. Proc R Soc Lond [Biol] 125:516–523Google Scholar
  117. White MJD (1965a) Sex chromosomes and meiotic mechanisms in some African and Australian mantids. Chromosoma 16:521–547Google Scholar
  118. White MJD (1965b) Chiasmatic and achiasmatic meiosis in African eumastacid grasshoppers. Chromosoma 16:271–307Google Scholar
  119. White MJD (1973) Animal cytology and evolution, 3rd edition. Cambridge University Press, CambridgeGoogle Scholar
  120. Wolf EB (1950) Die Chromosomen in der Spermatogenese der dipteren Phryne und Mycetobia. Chromosoma 4:148–204Google Scholar
  121. Yen PH, Li X-M, Tsai S-P, Johnson C, Mohondas J, Shapiro LJ (1990) Frequent deletions of the human X chromosomes distal short arm result from recombination between low copy number repetitive elements. Cell 61:603–610Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Bruce D. McKee
    • 1
  • Mary Ann Handel
    • 1
  1. 1.Department of ZoologyUniversity of TennesseeKnoxvilleUSA

Personalised recommendations