Academic journal article Genetics

Evolutionary History of Silene Latifolia Sex Chromosomes Revealed by Genetic Mapping of Four Genes

Academic journal article Genetics

Evolutionary History of Silene Latifolia Sex Chromosomes Revealed by Genetic Mapping of Four Genes

Article excerpt

ABSTRACT

The sex chromosomes of dioecious white campion, Silene latifolia (Caryophyllaceae), are of relatively recent origin (10-20 million years), providing a unique opportunity to trace the origin and evolution of sex chromosomes in this genus by comparing closely related Silene species with and without sex chromosomes. Here I demonstrate that four genes that are X-linked in S. latifolia are also linked in nondioecious S. vulgaris, which is consistent with OHNO'S (1967) hypothesis that sex chromosomes evolve from a single pair of autosomes. I also report a genetic map for four S. latifolia X-linked genes, SlX1, DD44X, SIX4, and a new X-linked gene SlssX, which encodes spermidine synthase. The order of the genes on the S. latifolia X chromosome and divergence between the homologous X- and Y-linked copies of these genes supports the "evolutionary strata" model, with at least three consecutive expansions of the nonrecombining region on the Y chromosome (NRY) in this plant species.

IT has been suggested that sex chromosomes evolve from a pair of homologous autosomes (proto sex chromosomes), which stop recombining with each other and gradually diverge into mostly nonhomologous X and Y chromosomes (OHNO 1967; BULL 1983). Alternatively, sex chromosomes could have evolved in several stages, through consecutive translocations of autosomal fragments to the (proto-) sex chromosomes and gradual expansion of the nonrecombining region. Y-linked genes advantageous in males and detrimental in females may possess a selective advantage, promoting translocation of autosomal regions containing sexually antagonistic genes to the Y chromosome, as well as further expansion of the nonrecombining region on the Y chromosome (CHARLESWORTH and CHARLESWORTH 1980; BULL 1983; RICE 1987). Indeed, the distal regions of the human sex chromosomes are autosomal in marsupials (SPENCER et al 1991), suggesting that modern mammalian sex chromosomes have formed due to translocations of fragments of autosomes to the sex chromosomes (WATSON et al. 1991). The Drosophila Y chromosome also appears to contain a patchwork of genes translocated from autosomes (CARVALHO 2002), casting doubts on the generality of OHNO 's (1967) hypothesis that sex chromosomes evolve from a single pair of autosomes.

Genes with homologous X- and Y-linked copies on the human sex chromosomes fall into four groups, depending on silent X/Y divergence (K3), suggesting that different genes spent different amounts of time in the nonrecombining region of the Y chromosome, the NRY (LAHN and PAGE 1999). On the basis of this observation, it was suggested that the cessation of recombination on the mammalian Y was not a single event, but occurred in several stages spanning a timescale of 240-350 MY and creating four "evolutionary strata" with differing levels of divergence between the X- and Y-linked homologs (LAHN and PAGE 1999). Mouse (SANDSTEDT and TUCKER 2004) and bird (HANDLEY et al 2004) sex chromosomes were also reported to have evolutionary strata. It is not clear, however, whether the stepwise formation of the sex chromosomes is a general process or is confined to mammals and birds.

Studying the origins of sex chromosomes in model organisms, such as Drosophila, mouse, human, and chicken is extremely difficult, as they arose hundreds of millions of years ago. The Y (or W in chicken) chromosomes in these species have diverged from the X (or Z) and lost almost all functional genes due to such processes as Muller's ratchet and genetic hitchhiking, leading to the accumulation of deleterious mutations and gene loss in the nonrecombining regions (CHARLESWORTH and CHARLESWORTH 2000). Many organisms, however, have much younger sex chromosomes [e.g., plants Silène latifolia (FlLATOV et al. 2000) and Carica papaya (LlU et al. 2004) and the stickleback fish (PEICHEL et al 2004)]. In particular, the plant genus Silène is very convenient for studying the early stages of sex chromosome evolution because sex chromosomes in this genus have been found only in a small cluster of dioecious Silène species (section Elisanthe: S. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.