fshr: a fish sex-determining locus shows variable incomplete penetrance across flathead grey mullet populations

Ferraresso, Serena; Bargelloni, Luca; Babbucci, Massimiliano; Cannas, Rita; Follesa, María Cristina; Carugati, Laura; Melis, Riccardo; Cau, Angelo; Koutrakis, Manos; Sapounidis, A.; Crosetti, Donatella; Patarnello, Tomaso

doi:10.1016/j.isci.2020.101886

Cited by 16 publications

(8 citation statements)

References 29 publications

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“…In adult Ot female specimens, however, banf2w expression was not observed, which may be explained by a limited time window of expression of this gene in Ot. Similarly, a male-specific MKR for SD, fshry, has been reported for Mugil cephalus with no observed expression in males (40 dph to adulthood) [8,62]. Sry in mammalian males is constitutively expressed from early embryonic stages to adulthood in different tissues, implicating its role as a housekeeping gene [63].…”

Section: Discussionmentioning

confidence: 85%

Gene Variant of Barrier to Autointegration Factor 2 (Banf2w) Is Concordant with Female Determination in Cichlids

Curzon

Shirak

Benet-Perlberg

et al. 2021

IJMS

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Oreochromis fishes exhibit variability of sex-determination (SD) genes whose characterization contributes to understanding of the sex differentiation network, and to effective tilapia farming, which requires all-male culture. However, O. niloticus (On) amh is the only master-key regulator (MKR) of SD that has been mapped (XY/XX SD-system on LG23). In O. aureus (Oa), LG3 controls a WZ/ZZ SD-system that has recently been delimited to 9.2 Mbp, with an embedded interval rich with female-specific variation, harboring two paics genes and banf2. Developing genetic markers within this interval and using a hybrid Oa stock that demonstrates no recombination repression in LG3, we mapped the critical SD region to 235 Kbp on the orthologous On physical map (p < 1.5 × 10−26). DNA-seq assembly and peak-proportion analysis of variation based on Sanger chromatograms allowed the characterization of copy-number variation (CNV) of banf2. Oa males had three exons capable of encoding 90-amino-acid polypeptides, yet in Oa females, we found an extra copy with an 89-amino-acid polypeptide and three non-conservative amino acid substitutions, designated as banf2w. CNV analysis suggested the existence of two to five copies of banf2 in diploidic Cichlidae. Disrupting the Hardy–Weinberg equilibrium (p < 4.2 × 10−3), banf2w was concordant with female determination in Oa and in three cichlids with LG3 WZ/ZZ SD-systems (O. tanganicae, O. hornorum and Pelmatolapia mariae). Furthermore, exclusive RNA-seq expression in Oa females strengthened the candidacy of banf2w as the long-sought LG3 SD MKR. As banf genes mediate nuclear assembly, chromatin organization, gene expression and gonad development, banf2w may play a fundamental role inducing female nucleus formation that is essential for WZ/ZZ SD.

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Section: Discussionmentioning

confidence: 85%

Gene Variant of Barrier to Autointegration Factor 2 (Banf2w) Is Concordant with Female Determination in Cichlids

Curzon

Shirak

Benet-Perlberg

et al. 2021

IJMS

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“…This latter gene would point to a similar SD system as reported in the turbot (Martínez et al 2021). The syntenic relationships between Senegalese sole and other flatfish adds evidence of the huge heterogeneity of SD systems in Pleuronectiformes, even between closely related species (Drinan et al 2018;Einfeldt et al 2021;Martínez et al 2021;Ferchaud et al 2022), but also highlights the recruitment of major SD drivers from common gene families (e.g., fshr, dmrt, amh or sox) across different fish and vertebrate species (Ferraresso et al 2021;Martínez et al 2021;Ferchaud et al 2022).…”

Section: Diversification Of the Sd Gene In Pleuronectiformesmentioning

confidence: 88%

“…Pleuronectiformes, even between closely related species (Drinan et al 2018; Einfeldt et al 2021; Martínez et al 2021; Ferchaud et al 2022), but also highlights the recruitment of major SD drivers from common gene families (e.g., fshr, dmrt, amh or sox ) across different fish and vertebrate species (Ferraresso et al 2021; Martínez et al 2021; Ferchaud et al 2022).…”

Section: Discussionmentioning

confidence: 99%

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

Herrán

Hermida

Rubiolo

et al. 2022

Preprint

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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.

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“…After analyzing the hot region in SseLG18, the fshr appeared as a putative candidate for sex determination. The fshr locus was recently associated with male sex in flatfhead grey mullet with an incomplete penetrance as observed in sole 64 . These authors proposed that fshr might act as a proxy for the genetic transduction of environmental factors such as temperature Under this hypothesis, sex determination would not rely on a single genetic cascade but a continuum of environmental and genetic factors.…”

Section: Discussionmentioning

confidence: 99%

Chromosome anchoring in Senegalese sole (Solea senegalensis) reveals sex-associated markers and genome rearrangements in flatfish

Guerrero-Cózar

Gómez‐Garrido

Berbel

et al. 2021

Sci Rep

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The integration of physical and high-density genetic maps is a very useful approach to achieve chromosome-level genome assemblies. Here, the genome of a male Senegalese sole (Solea senegalensis) was de novo assembled and the contigs were anchored to a high-quality genetic map for chromosome-level scaffolding. Hybrid assembled genome was 609.3 Mb long and contained 3403 contigs with a N50 of 513 kb. The linkage map was constructed using 16,287 informative SNPs derived from ddRAD sequencing in 327 sole individuals from five families. Markers were assigned to 21 linkage groups with an average number of 21.9 markers per megabase. The anchoring of the physical to the genetic map positioned 1563 contigs into 21 pseudo-chromosomes covering 548.6 Mb. Comparison of genetic and physical distances indicated that the average genome-wide recombination rate was 0.23 cM/Mb and the female-to-male ratio 1.49 (female map length: 2,698.4 cM, male: 2,036.6 cM). Genomic recombination landscapes were different between sexes with crossovers mainly concentrated toward the telomeres in males while they were more uniformly distributed in females. A GWAS analysis using seven families identified 30 significant sex-associated SNP markers located in linkage group 18. The follicle-stimulating hormone receptor appeared as the most promising locus associated with sex within a region with very low recombination rates. An incomplete penetrance of sex markers with males as the heterogametic sex was determined. An interspecific comparison with other Pleuronectiformes genomes identified a high sequence similarity between homologous chromosomes, and several chromosomal rearrangements including a lineage-specific Robertsonian fusion in S. senegalensis.

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fshr: a fish sex-determining locus shows variable incomplete penetrance across flathead grey mullet populations

Cited by 16 publications

References 29 publications

Gene Variant of Barrier to Autointegration Factor 2 (Banf2w) Is Concordant with Female Determination in Cichlids

Gene Variant of Barrier to Autointegration Factor 2 (Banf2w) Is Concordant with Female Determination in Cichlids

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

Chromosome anchoring in Senegalese sole (Solea senegalensis) reveals sex-associated markers and genome rearrangements in flatfish

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