Evolution of the Proto Sex-Chromosome in Solea senegalensis.

María Rodríguez,Laureana Rebordinos,Alberto Arias-Pérez,Belén Molina,Silvia Portela-Bens,Thomas Liehr,Aglaya García-Angulo,Manuel Merlo,Ismael Cross

doi:10.3390/ijms20205111

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.

Highlights

IntroductionTeleosts are the most diversified group among vertebrates [1], colonizing aquatic environments with a wide range of salinity, temperature or photoperiod conditions and displaying a high variety of adaptations
Teleosts are the most diversified group among vertebrates [1], colonizing aquatic environments with a wide range of salinity, temperature or photoperiod conditions and displaying a high variety of adaptations. This variability reaches sex determination systems, of which a great variety of them have been described in fish that can be (i) simple system with heterogametic male as XX/XY, heterogametic female as ZZ/ZW, and homogametic female and male XX/X0 and ZZ/Z0 respectively, and (ii) multiple system with standard as XX/XY1Y2 which was observed in neo tropical fish Hoplias malabaricus in which XY1Y2 is a neo-sex chromosome, or constitution or numerical variations
Pleuronectiformes are a diverse order composed of more than 600 species grouped into 11 families, they have a small genome [3] when compared to other teleost fish, making them an interesting group to study mechanisms of organization and gene expression

Summary

Introduction

Teleosts are the most diversified group among vertebrates [1], colonizing aquatic environments with a wide range of salinity, temperature or photoperiod conditions and displaying a high variety of adaptations This variability reaches sex determination systems, of which a great variety of them have been described in fish that can be (i) simple system with heterogametic male as XX/XY, heterogametic female as ZZ/ZW, and homogametic female and male XX/X0 and ZZ/Z0 respectively, and (ii) multiple system with standard as XX/XY1Y2 which was observed in neo tropical fish Hoplias malabaricus in which XY1Y2 is a neo-sex chromosome, or constitution or numerical variations (revised in [2]). Pleuronectiformes are a diverse order composed of more than 600 species grouped into 11 families, they have a small genome [3] when compared to other teleost fish, making them an interesting group to study mechanisms of organization and gene expression Within this order, both ZZ/ZW (e.g., Cynoglossus semilaevis, [4] and XX/XY (e.g., Solea senegalensis, [5]) sex chromosome determination systems have been described. Sex determination mechanisms involve, in many cases, more than one gene, as well as environmental factors and epigenetic mechanisms [7]

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