Higher-order Genome Organization in Platypus and Chicken Sperm and Repositioning of Sex Chromosomes During Mammalian Evolution

Overview

Journal Chromosoma

Specialty Molecular Biology

Date 2008 Aug 30

PMID 18726609

Citations 9

Authors

Enkhjargal Tsend-Ayush

Natasha Dodge

Julia Mohr

Aaron Casey

Heinz Himmelbauer

Colin L Kremitzki

Kyriena Schatzkamer

Tina Graves

Wesley C Warren

Frank Grutzner

Affiliations

Soon will be listed here.

Abstract

In mammals, chromosomes occupy defined positions in sperm, whereas previous work in chicken showed random chromosome distribution. Monotremes (platypus and echidnas) are the most basal group of living mammals. They have elongated sperm like chicken and a complex sex chromosome system with homology to chicken sex chromosomes. We used platypus and chicken genomic clones to investigate genome organization in sperm. In chicken sperm, about half of the chromosomes investigated are organized non-randomly, whereas in platypus chromosome organization in sperm is almost entirely non-random. The use of genomic clones allowed us to determine chromosome orientation and chromatin compaction in sperm. We found that in both species chromosomes maintain orientation of chromosomes in sperm independent of random or non-random positioning along the sperm nucleus. The distance of loci correlated with the total length of sperm nuclei, suggesting that chromatin extension depends on sperm elongation. In platypus, most sex chromosomes cluster in the posterior region of the sperm nucleus, presumably the result of postmeiotic association of sex chromosomes. Chicken and platypus autosomes sharing homology with the human X chromosome located centrally in both species suggesting that this is the ancestral position. This suggests that in some therian mammals a more anterior position of the X chromosome has evolved independently.

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References

Kimmins S, Sassone-Corsi P . Chromatin remodelling and epigenetic features of germ cells. Nature. 2005; 434(7033):583-9. DOI: 10.1038/nature03368. View

Zalensky A, Breneman J, Zalenskaya I, Brinkley B, Bradbury E . Organization of centromeres in the decondensed nuclei of mature human sperm. Chromosoma. 1993; 102(8):509-18. DOI: 10.1007/BF00368344. View

Habermann F, Cremer M, Walter J, Kreth G, von Hase J, Bauer K . Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res. 2001; 9(7):569-84. DOI: 10.1023/a:1012447318535. View

Kohn M, Kehrer-Sawatzki H, Steinbach P, Marshall Graves J, Hameister H . Recruitment of old genes to new functions: evidences obtained by comparing the orthologues of human XLMR genes in mouse and chicken. Cytogenet Genome Res. 2007; 116(3):173-80. DOI: 10.1159/000098183. View

Waters P, Delbridge M, Deakin J, El-Mogharbel N, Kirby P, Carvalho-Silva D . Autosomal location of genes from the conserved mammalian X in the platypus (Ornithorhynchus anatinus): implications for mammalian sex chromosome evolution. Chromosome Res. 2005; 13(4):401-10. DOI: 10.1007/s10577-005-0978-5. View

Nanda I, Shan Z, Schartl M, Burt D, Koehler M, Nothwang H . 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet. 1999; 21(3):258-9. DOI: 10.1038/6769. View

VAN BRINK J . [Morphological form of digametism in the Sauropsida and the Monotremata]. Chromosoma. 1959; 10(1):1-72. DOI: 10.1007/BF00396564. View

McQueen H, Siriaco G, Bird A . Chicken microchromosomes are hyperacetylated, early replicating, and gene rich. Genome Res. 1998; 8(6):621-30. PMC: 310741. DOI: 10.1101/gr.8.6.621. View

Brinkley B, Brenner S, Hall J, Tousson A, Balczon R, Valdivia M . Arrangements of kinetochores in mouse cells during meiosis and spermiogenesis. Chromosoma. 1986; 94(4):309-17. DOI: 10.1007/BF00290861. View

10.

Oliva R, DIXON G . Chicken protamine genes are intronless. The complete genomic sequence and organization of the two loci. J Biol Chem. 1989; 264(21):12472-81. View

11.

Balhorn R . A model for the structure of chromatin in mammalian sperm. J Cell Biol. 1982; 93(2):298-305. PMC: 2112839. DOI: 10.1083/jcb.93.2.298. View

12.

Hazzouri M, Rousseaux S, Mongelard F, Usson Y, Pelletier R, Faure A . Genome organization in the human sperm nucleus studied by FISH and confocal microscopy. Mol Reprod Dev. 2000; 55(3):307-15. DOI: 10.1002/(SICI)1098-2795(200003)55:3<307::AID-MRD9>3.0.CO;2-P. View

13.

Greaves I, Rens W, Ferguson-Smith M, Griffin D, Marshall Graves J . Conservation of chromosome arrangement and position of the X in mammalian sperm suggests functional significance. Chromosome Res. 2003; 11(5):503-12. DOI: 10.1023/a:1024982929452. View

14.

Melamed E, Arnold A . Regional differences in dosage compensation on the chicken Z chromosome. Genome Biol. 2007; 8(9):R202. PMC: 2375040. DOI: 10.1186/gb-2007-8-9-r202. View

15.

McQueen H, Fantes J, Cross S, Clark V, Archibald A, Bird A . CpG islands of chicken are concentrated on microchromosomes. Nat Genet. 1996; 12(3):321-4. DOI: 10.1038/ng0396-321. View

16.

Ward W, McNeil J, de Lara J, Lawrence J . Localization of three genes in the hook-shaped hamster sperm nucleus by fluorescent in situ hybridization. Biol Reprod. 1996; 54(6):1271-8. DOI: 10.1095/biolreprod54.6.1271. View

17.

Rens W, Grutzner F, OBrien P, Fairclough H, Graves J, Ferguson-Smith M . Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc Natl Acad Sci U S A. 2004; 101(46):16257-61. PMC: 528943. DOI: 10.1073/pnas.0405702101. View

18.

Solovei I, Joffe B, Hori T, Thomson P, Mizuno S, MACGREGOR H . Unordered arrangement of chromosomes in the nuclei of chicken spermatozoa. Chromosoma. 1998; 107(3):184-8. DOI: 10.1007/s004120050295. View

19.

Wallis J, Aerts J, Groenen M, Crooijmans R, Layman D, Graves T . A physical map of the chicken genome. Nature. 2004; 432(7018):761-4. DOI: 10.1038/nature03030. View

20.

Bininda-Emonds O, Cardillo M, Jones K, MacPhee R, Beck R, Grenyer R . The delayed rise of present-day mammals. Nature. 2007; 446(7135):507-12. DOI: 10.1038/nature05634. View