Evolution of the Proto Sex-Chromosome in Solea senegalensis

Abstract

Solea senegalensis is a flatfish belonging to the Soleidae family within the Pleuronectiformes order. It has a karyotype of 2n = 42 (FN = 60; 6M + 4 SM + 8 St + 24 T) and a XX/XY system. The first pair of metacentric chromosomes has been proposed as a proto sex-chromosome originated by a Robertsonian fusion between acrocentric chromosomes. In order to elucidate a possible evolutionary origin of this chromosome 1, studies of genomic synteny were carried out with eight fish species. A total of 88 genes annotated within of 14 BACs located in the chromosome 1 of S. senegalensis were used to elaborate syntenic maps. Six BACs (BAC5K5, BAC52C17, BAC53B20, BAC84K7, BAC56H24, and BAC48P7) were distributed in, at least, 5 chromosomes in the species studied, and a group of four genes from BAC53B20 (grsf1, rufy3, slc4a4 and npffr2) and genes from BAC48K7 (dmrt2, dmrt3, dmrt1, c9orf117, kank1 and fbp1) formed a conserved cluster in all species. The analysis of repetitive sequences showed that the number of retroelements and simple repeat per BAC showed its highest value in the subcentromeric region where 53B20, 16E16 and 48K7 BACs were localized. This region contains all the dmrt genes, which are associated with sex determination in some species. In addition, the presence of a satellite “chromosome Y” (motif length: 860 bp) was detected in this region. These findings allowed to trace an evolutionary trend for the large metacentric chromosome of S. senegalensis, throughout different rearrangements, which could be at an initial phase of differentiation as sex chromosome.

Development of whole-genome multiplex assays and construction of an integrated genetic map using SSR markers in Senegalese sole

“…semilaevis . In S. senegalensis , it has been hypothesized that the largest metacentric chromosome arose from a robertsonian fusion of two acrocentric chromosomes followed by pericentric inversions 16 , 59 . Our data also support this fusion and chromosome rearrangements between chromosomes 3 and 20 of C. semilaevis (Table 3 ).…”

“…In fact, a sex determination XX-XY system was proposed in this species with the female as homogametic sex 8 , 61 . Although the SseLG01 has been proposed as a sex proto-chromosome due to the location of some key sex-determining genes and repetitive sequences 12 , 16 , the spreading of Z/W sequences through the genome indicates that a further experimental validation is required to identify a putative major loci for sex determination.…”

“…Moreover, an integrated map using BAC clones and repetitive DNA families was developed using multiple fluorescence in situ hybridization that comprised 64 BACs mapped through all genome except in the submetacentric chromosome five 15 . Although Senegalese sole has not morphologically heteromorphic sex chromosomes, the largest metacentric chromosome was proposed as a proto-sex chromosome originated from the fusion of two acrocentric chromosomes during flatfish evolution 12 , 16 .…”

A Comprehensive Integrated Genetic Map of the Complete Karyotype of Solea senegalensis (Kaup 1858)

“…Similarly, it has been possible to characterize and locate the BAC clones with other types of sequences of interest, such as miRNAs or transposons [ 6 , 28 , 33 , 34 ]. As a result of these studies, evidence has accumulated that the pair of major metacentric chromosomes of S. senegalensis could be a pair of sex proto-chromosomes, which have followed a specific evolutionary pattern involving, among other events, Robertsonian fusion [ 33 , 35 , 36 , 37 ].…”

The genomic structure of the highly-conserved dmrt1 gene in Solea senegalensis (Kaup, 1868) shows an unexpected intragenic duplication

“…In particular, the number of retroelements and simple repeats per region shows its highest value in the subcentromeric region of the chromosome on which the dmrt gene family is localized. This region contains all the dmrt genes, which are associated with sex determination in some species [ 35 ]. Hence a detailed analysis of the dmrt1 gene could contribute to the discovery of the master sex gene in the species.…”