Evolution and organization of the ten sex chromosome system in platypus

Abstract

Platypus sex chromosomes have been controversial for over three decades. To solve the platypus chromosome puzzle we have generated whole chromosome paints for all platypus chromosomes. Hybridization on mitotic chromosomes of males and females and male meiotic cells revealed that platypus have five Ys and five X chromosomes, which form the meiotic chain adopting an XY alternating pattern. With remarkable accuracy the chain segregates into XXXXX-female determining and YYYYY-male determining sperm. The largest X chromosome, with homology to the human X, lies at one end of the chain (X1). At the other end of the chain we mapped the gene DMRT1 onto X5. DMRT1 is a Z-linked candidate sex-determining gene in chicken. This suggests an unexpected link between mammal and bird sex chromosome systems that were thought to have evolved independently. Moreover we found that Y1 is not very degraded and shares significant homology with the short arm of X1, indicating that X1Y1 is the most recent addition to the chain. In contrast, the tiny Y5 at the other end of the chain is very degraded and X5 showed no detectable homology with Y5. Therefore we conclude that X5Y5 is the original sex chromosome pair. Using the paints and sex chromosome specific BAC clones we have analyzed meiotic chromatin condensation and chromosome pairing of the ten sex chromosomes in platypus. Our results show that, as in other mammals, platypus sex chromosomes are condensed and pair late at pachytene, indicating that meiotic sex chromosome inactivation may occur as in other mammals.