A chromosome-level genome assembly enables the identification of the follicle stimulating hormone receptor as the master sex determining gene in Solea senegalensis

Abstract

Sex determination (SD) mechanisms are exceptionally diverse and show high evolutionary rates in fish. Pleuronectiformes is an emblematic fish group characterized by its adaptation to demersal life and its compact genomes. Here, we present a chromosome-level genome assembly of Senegalese sole, a promising European aquaculture species. We combined long- and short-read sequencing and a highly dense genetic map to obtain a contiguous assembly of 613 Mb (N50 = 29.0 Mb, 99% of the assembly in the n = 21 chromosomes of its karyotype). The correspondence between this new assembly and the Senegalese sole chromosomes was established by fluorescence in situ hybridization with BAC probes. Orthology within Pleuronectiformes was assessed by using the chromosome-level genomes of six important commercial flatfishes covering a broad phylogenetic spectrum of the order. A total of 7936 single-gene orthologues, shared by the six species, were used to identify syntenies in Pleuronectiformes and to explore chromosome evolutionary patterns in the order. Whole genome resequencing of six males and six females enabled the identification of 41 fixed allelic variants in the follicle stimulating hormone receptor (fshr) gene, homozygous in females and heterozygous in males, consistent with an XX / XY chromosome system. The observed association between fshr SNPs and sex was confirmed at the species level in a broad sample, which allowed tuning up a molecular sexing tool. Fshr demonstrated differential gene expression between male and female gonads since 86 days post-fertilization, when the gonad was still an undifferentiated primordium, concomitant with the activation of other testis and ovary marker genes, such as amh and cyp19a1a genes, respectively. Interestingly, the Y-linked fshr allele, which included 24 non-synonymous variants, expressed to a higher level than the X-linked allele at all stages. We hypothesize a molecular mechanism hampering the action of the follicle stimulating hormone that would drive the undifferentiated gonad toward testis.

A chromosome‐level genome assembly enables the identification of the follicule stimulating hormone receptor as the master sex‐determining gene in the flatfish Solea senegalensis

“…Consistent chromosome orthology has been recently reported within flatfishes taking advantage of their chromosome‐level genome assemblies facilitated by their compact genomes (de la Herrán et al, 2022; Jasonowicz et al, 2022; Lü et al, 2021; Martínez et al, 2021). According to this information, the SD gene‐bearing chromosome of S. senegalensis , Sse C12, would not be orthologous to any other consistently proven SD chromosome in flatfish species.…”

Non-synonymous variation and protein structure of candidate genes associated with selection in farm and wild populations of turbot (Scophthalmus maximus)

“…Previous studies on allozyme variation in the turbot supported much lower variation for this fraction of protein coding genes than in other flatfishes (~ fivefold lower), unlike the very similar diversity observed with microsatellites, which was interpreted as an ancient bottleneck in this species 11 . If this observation could be extrapolated to all protein coding genes, this would mean that a much higher NSV would occur in other flatfish, which is supported by the ~ 10 million SNPs detected in Senegalese sole vs ~ 3 million SNPs in turbot obtained from the recent whole genome resequencing of 12 sole individuals 86 .…”

“…If this observation could be extrapolated to all protein coding genes, this would mean that a much higher NSV would occur in other flatfish, which is supported by the ~ 10 million SNPs detected in Senegalese sole vs ~ 3 million SNPs in turbot obtained from the recent whole genome resequencing of 12 sole individuals 86 .…”

The broad shell colour variation in common cockle (Cerastoderma edule) from Northeast Atlantic relies on a major QTL revealed by GWAS using a new high-density genetic map

“…The common cockle genetic map here constructed comprehends 13,874 markers with an inter-marker distance of 0.16 cM and comprises the 19 expected LGs matching with the haploid karyotype of the species (Insua & Thiriot-Quiévreux, 1991), being, to our knowledge, the denser genetic map published to date in molluscs. Besides its importance for genomic screening, the common cockle genetic map is an invaluable tool for genome scaffolding, as has been previously reported in other species (Martínez et al, 2021; de la Herrán et al, 2022), and in fact, five of the seven mollusc genomes assembled at chromosome-level took advantage of high-density linkage maps (Hollenbeck & Johnston, 2018).…”

“…GBS methods have been recently applied to understand adaptive variation of common cockle from Northeast Atlantic, and consistent signals of adaptive variation were detected both at microgeographic (dd-RAD; Coscia et al, 2020) and macrogeographic (2b-RAD; Vera et al, 2022) scales. GBS have facilitated the construction of high-resolution linkage maps (Maroso et al, 2018; Dong et al, 2019; de la Herrán et al, 2022), which are important tools for genome scaffolding and assembly (Fierst, 2015), and have aided to disentangle the genetic basis of relevant evolutionary or productive traits through quantitative trait locus (QTL) screening (Aslam et al, 2020; Yin & Hedgecock, 2021). Genetic maps have been used to study the genetic architecture of traits of interest in various bivalve species, such as growth in Zhikong scallop ( Chlamys farreri ; Zhan et al, 2009), bay scallop ( Argopecten irradians ; Li et al, 2012) or Crassostrea gigas (Li et al, 2018), various pearl-quality traits in triangle sail mussel ( Hyriopsis cumingii ; Bai et al, 2016) and resistance to pathologies (Harrang et al, 2015).…”