Analysis and Evolution of Two Functional Y-Linked Loci in a Plant Sex Chromosome System

Abstract

White campion (Silene latifolia) is one of the few examples of plants with separate sexes and with X and Y sex chromosomes. The presence or absence of the Y chromosome determines which type of reproductive organs--male or female--will develop. Recently, we characterized the first active gene located on a plant Y chromosome, SlY1, and its X-linked homolog, SlX1. These genes encode WD-repeat proteins likely to be involved in cell proliferation. Here, we report the characterization of a novel Y-linked gene, SlY4, which also has a homolog on the X chromosome, SlX4. Both SlY4 and SlX4 potentially encode fructose-2,6-bisphosphatases. A comparative molecular analysis of the two sex-linked loci (SlY1/SlX1 and SlY4/SlX4) suggests selective constraint on both X- and Y-linked genes and thus that both X- and Y-linked copies are functional. Divergence between SlY4 and SlX4 is much greater than that between the SlY1 and SlX1 genes. These results suggest that, as for human XY-linked genes, the sex-linked plant loci ceased recombining at different times and reveal distinct events in the evolutionary history of the sex chromosomes.

Dioecious Plants. A Key to the Early Events of Sex Chromosome Evolution

“…The outcome is the accumulation on the sex chromosomes of key genetic components (molecular switches) determining sexual dimorphism and, following a controlled arrest of recombination along most regions of X and Y, the concentration of sexrelated genes on sex chromosomes, Y chromosome genetic isolation and erosion, X chromosome dosage compensation, etc. (Charlesworth, 1992;Ellis, 1998;Charlesworth and Guttman, 1999;Mitchell, 2000).…”

“…3a). Such states need to be subsequently enforced by the action of other, genetically linked, sexually antagonistic genes and modifier genes differentially acting on such alleles (Charlesworth, 1992;Rice, 1992).…”

“…Key events appear to be the suppression of meiotic recombination between protosex chromosome regions in the heterogametic sex, Y degeneration, and X chromosome dosage compensation (Charlesworth, 1992;Ellis, 1998). …”

“…In the first case, for example, a molecular characterization of sex-linked loci is required. The first active Y-linked genes described have a very similar X chromosomal copy and the relative age of individual X-Y gene pairs has been measured by nucleotide divergence (Delichère et al, 1999;Filatov et al, 2000;Atanassov et al, 2001). The results indicate, as for human XYlinked genes, that the two loci characterized so far identify Y chromosome regions that have ceased recombining at different times during the evolution of sex chromosomes, namely 5 and 15 million years on the 20-to 25-million year scale since the last common hermaphrodite ancestor.…”

“…The purity of the sorted X and autosomes is high (95%) as estimated by both fluorescence in situ hybridization and PCR reconstruction experiments. The physical mapping is illustrated by the autosomal localization of MROS4, the autosomal and X location of MROS3 (Matsunaga et al, 1996), and the unique position of SlX4 on the X chromosome (Atanassov et al, 2001). 0, Control, no DNA template; A, autosomes; X, X chromosomes; m, male genomic DNA; f, female genomic DNA; M, marker (pBR322/AluI).…”