Abstract
Dioecious plants vary in whether their sex chromosomes are heteromorphic or homomorphic, but even homomorphic sex chromosomes may show divergence between homologues in the non-recombining, sex-determining region (SDR). Very little is known about the SDR of these species, which might represent particularly early stages of sex-chromosome evolution. Here, we assess the size and content of the SDR of the diploid dioecious herb Mercurialis annua, a species with homomorphic sex chromosomes and mild Y-chromosome degeneration. We used RNA sequencing (RNAseq) to identify new Y-linked markers for M. annua. Twelve of 24 transcripts showing male-specific expression in a previous experiment could be amplified by polymerase chain reaction (PCR) only from males, and are thus likely to be Y-linked. Analysis of genome-capture data from multiple populations of M. annua pointed to an additional six male-limited (and thus Y-linked) sequences. We used these markers to identify and sequence 17 sex-linked bacterial artificial chromosomes (BACs), which form 11 groups of non-overlapping sequences, covering a total sequence length of about 1.5 Mb. Content analysis of this region suggests that it is enriched for repeats, has low gene density, and contains few candidate sex-determining genes. The BACs map to a subset of the sex-linked region of the genetic map, which we estimate to be at least 14.5 Mb. This is substantially larger than estimates for other dioecious plants with homomorphic sex chromosomes, both in absolute terms and relative to their genome sizes. Our data provide a rare, high-resolution view of the homomorphic Y chromosome of a dioecious plant.
Highlights
Most flowering plants are hermaphroditic or monoecious, but dioecy has evolved frequently and is found in about half of all plant families [1,2]
Twelve of the 24 genes that had male-specific expression were consistently amplified in males only, whereas the remaining 12 genes amplified in both sexes
We identified six genomic regions present on the Y-chromosome using genome capture data [31], by identifying sequences that were entirely missing from all females, but present in all males; one of these coincided with a sequence found on the basis of gene expression data, so that, in total, we obtained 17 male-specific polymerase chain reaction (PCR) products
Summary
Most flowering plants are hermaphroditic or monoecious, but dioecy has evolved frequently and is found in about half of all plant families [1,2]. Many plant sex chromosomes are cytologically heteromorphic (currently known for 19 species in four families), but cytological differences between males and females are not evident in others (20 species in 13 families; reviewed in [7,8]). Closely related dioecious species may often differ in terms of their degree of heteromorphism [6,7]. We might expect the magnitude of the cytological difference between homologous sex chromosomes to increase with their age, as the result of the progressive genetic degeneration of the Y or W chromosome (in species with XY or ZW systems, respectively). In Coccinia grandis (Cucurbitaceae), a species that evolved dioecy about three million years ago [10], the X and Y chromosomes are highly divergent, with a 10% elongation of the Y compared to the
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