Abstract
BackgroundThe papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. The same populations were used to study nucleotide diversity and population structure in the X-linked region.ResultsDiversity is very low for all genes in the X-linked region in the wild dioecious population, with nucleotide diversity π syn = 0.00017, tenfold lower than the autosomal region (π syn = 0.0017) and 12-fold lower than the Y-linked region (π syn = 0.0021). Analysis of the X-linked sequences shows an undivided population, suggesting a geographically wide diversity-reducing event, whereas two subpopulations were observed in the autosomes separating gynodioecy and dioecy and three subpopulations in the Y-linked region separating three male populations. The extremely low diversity in the papaya X-linked region was probably caused by a recent, strong selective sweep before domestication, involving either the spread of a recessive mutation in an X-linked gene that is beneficial to males or a partially dominant mutation that benefitted females or both sexes. Nucleotide diversity in the domesticated X samples is about half that in the wild Xs, probably due to the bottleneck when hermaphrodites were selected during domestication.ConclusionsThe extreme low nucleotide diversity in the papaya X-linked region is much greater than observed in humans, great apes, and the neo-X chromosome of Drosophila miranda, which show the expected pattern of Y-linked genes < X-linked genes < autosomal genes; papaya shows an unprecedented pattern of X-linked genes < autosomal genes < Y-linked genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1095-9) contains supplementary material, which is available to authorized users.
Highlights
The papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from
Identification of polymorphisms and annotation We studied the same samples of wild males and cultivated hermaphrodites (Additional file 1: Table S1) as for our previous work on the Yh and Y chromosomes: 12 cultivated hermaphrodites, representing a collection of commercial papaya varieties from around the world with varied fruit quality, size, shape, color, and disease resistance and 24 wild male papaya individuals collected from three natural populations in Costa Rica [19, 21]
Identifying variants in the X-linked region is difficult given the highly repetitive nature of the X and its low gene density; overall, across the 3.5-Mb region, we identified a total of 12,555 SNPs not found in any Ylinked sequences, and probably X-specific, and 718 small insertions/deletions (X-specific indels); 193,621 SNPs and 23,825 small indels were found in the pseudo-autosomal regions (PARs) sequences and 3.1 million variants were identified across the autosome
Summary
The papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. Sex chromosomes with recombination-suppressed sexlinked regions are found in all major eukaryotic lineages and have evolved independently numerous times, including in several plant species [1]. The effective population size (Ne) is VanBuren et al Genome Biology (2016) 17:230 processes affect Y-linked sequences more than X-linked ones, but, in species where recombination occurs in both sexes, the X recombines less than autosomal genome regions because it recombines only in females. X-linked sequences are expected to have lower Ne than autosomal ones. Because of their low Ne, Y and X chromosomes are predicted to have lower neutral diversity than autosomes or the pseudo-autosomal region [5]. Lower X-linked than autosomal diversity is found in the fruit flies Drosophila simulans and Drosophila melanogaster [6, 7], and Y linked diversity is low in humans and other mammals, Drosophila miranda, and the plant Silene latifolia [8,9,10,11]
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