Chromosomal location and gene paucity of the male specific region on papaya Y chromosome

Abstract

Sex chromosomes in flowering plants evolved recently and many of them remain homomorphic, including those in papaya. We investigated the chromosomal location of papaya's small male specific region of the hermaphrodite Y (Yh) chromosome (MSY) and its genomic features. We conducted chromosome fluorescence in situ hybridization mapping of Yh-specific bacterial artificial chromosomes (BACs) and placed the MSY near the centromere of the papaya Y chromosome. Then we sequenced five MSY BACs to examine the genomic features of this specialized region, which resulted in the largest collection of contiguous genomic DNA sequences of a Y chromosome in flowering plants. Extreme gene paucity was observed in the papaya MSY with no functional gene identified in 715 kb MSY sequences. A high density of retroelements and local sequence duplications were detected in the MSY that is suppressed for recombination. Location of the papaya MSY near the centromere might have provided recombination suppression and fostered paucity of genes in the male specific region of the Y chromosome. Our findings provide critical information for deciphering the sex chromosomes in papaya and reference information for comparative studies of other sex chromosomes in animals and plants.

The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)

“…Re-analysis of the repetitive DNA content of the MSY BACs, to include the new papaya-specific repeat families identified herein, increased the average repeat sequence to 85.6%, with 54.1% Gypsy and 1.9% Copia retro-elements (Supplementary Table 10). This compares with an earlier estimate of 17.9% using the Arabidopsis repeat database alone 28 . The SunUp genome has presented an opportunity to analyse transgene insertion sites critically.…”

“…The average gene density would be one gene per 19.5 kb, lower than the estimated genome average of one gene per 14.3 kb. By contrast, among seven completely sequenced MSY BACs totalling 1.2 Mb, a total of four expressed genes were found on two of the BACs 14,28 . The somewhat lower-than-average gene density in the X-specific scaffolds is accompanied by more repetitive DNA (58.3%) than the genome-wide average, perhaps because this region is near the centromere 28 .…”

“…By contrast, among seven completely sequenced MSY BACs totalling 1.2 Mb, a total of four expressed genes were found on two of the BACs 14,28 . The somewhat lower-than-average gene density in the X-specific scaffolds is accompanied by more repetitive DNA (58.3%) than the genome-wide average, perhaps because this region is near the centromere 28 . Re-analysis of the repetitive DNA content of the MSY BACs, to include the new papaya-specific repeat families identified herein, increased the average repeat sequence to 85.6%, with 54.1% Gypsy and 1.9% Copia retro-elements (Supplementary Table 10).…”

The role of repetitive DNA in structure and evolution of sex chromosomes in plants

“…The MSY region has lost many genes, and the YY genotype is lethal. Despite the short period of time for the divergence of the X and Y, the MSY region of the Y chromosome is already enriched for local segmental duplications, TEs and plastid DNA insertions compared with its X partner (Liu et al, 2004;Yu et al, 2007).…”

Sex chromosome evolution: A ‘missing link’ in the evolution of sex chromosomes

“…Of interest is that the plant models, in particular, tend to span various stages during the early events in sex chromosome evolution. For example, the sex determining loci in papaya, in which males are heterogametic, are found in a non-recombining region of the Y chromosome (NRY) that is confined to an approximately 8 Mbp region around the centromere of a pair of homomorphic sex chromosomes (Yu et al, 2007). Estimates of the age of the papaya sex chromosomes suggest that they emerged less than 2 mya (Yu et al, 2008).…”