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Logical modelling uncovers developmental constraints for primary sex determination of chicken gonads.

ABSTRACT: In the chicken, sex determination relies on a ZZ (male)/ZW (female) chromosomal system, but underlying mechanisms are still not fully understood. The Z-dosage and the dominant W-chromosome hypotheses have been proposed to underlie primary sex determination. We present a modelling approach, which assembles the current knowledge and permits exploration of the regulation of this process in chickens. Relying on published experimental data, we assembled a gene network, which led to a logical model that integrates both the Z-dosage and dominant W hypotheses. This model showed that the sexual fate of chicken gonads results from the resolution of the mutual inhibition between DMRT1 and FOXL2, where the initial amount of DMRT1 product determines the development of the gonads. In this respect, at the initiation step, a W-factor would function as a secondary device, by reducing the amount of DMRT1 in ZW gonads when the sexual fate of the gonad is settled, that is when the SOX9 functional level is established. Developmental constraints that are instrumental in this resolution were identified. These constraints establish qualitative restrictions regarding the relative transcription rates of the genes DMRT1, FOXL2 and HEMGN. Our model further clarified the role of OESTROGEN in maintaining FOXL2 function during ovary development.

SUBMITTER: Sanchez L

PROVIDER: S-EPMC6000168 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Logical modelling uncovers developmental constraints for primary sex determination of chicken gonads.

Sánchez Lucas L Chaouiya Claudine C

Journal of the Royal Society, Interface 20180501 142

In the chicken, sex determination relies on a ZZ (male)/ZW (female) chromosomal system, but underlying mechanisms are still not fully understood. The Z-dosage and the dominant W-chromosome hypotheses have been proposed to underlie primary sex determination. We present a modelling approach, which assembles the current knowledge and permits exploration of the regulation of this process in chickens. Relying on published experimental data, we assembled a gene network, which led to a logical model th ...[more]

PMID: 29792308

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Project description:BackgroundIn chickens, as in most birds, female gonad morphogenesis is asymmetrical. Gonads appear first rather similarly, but only the left one undergoes full differentiation and gives rise to a functional ovary. The right gonad, in which the cortex does not develop, remains restricted to the medulla and finally regresses. Opportunity was taken of this left-right asymmetry to perform a suppression subtractive hybridization screening to select for transcripts preferentially expressed in the developing left ovary as compared to the right one, and thus identify genes that are potentially involved in the process of ovarian differentiation.ResultsOne of these transcripts, named Ovex1 according to its expression profile, corresponds to an endogenous retrovirus that has not been previously characterized. It is transcribed as full-length and singly spliced mRNAs and contains three uninterrupted open reading frames coding potentially for proteins with homology to Gag and Pro-Pol retroviral polyproteins and a third protein showing only a weak similarity with Env glycoproteins. Ovex1 is severely degenerated; it is devoid of typical long terminal repeats and displays some evidence of recombination. An orthologous Ovex1 locus was identified in the genome of zebra finch, a member of a different bird order, and similar sequences were detected in turkey, guinea fowl, and duck DNA. The relationship between these sequences follows the bird phylogeny, suggesting vertical transmission of the endogenous retrovirus for more than 100 million years. Ovex1 is transcribed in chicken gonads with a sex-dependent and left-right asymmetrical pattern. It is first expressed in the cortex of the left indifferent gonads of both sexes. Expression is transient in the left testis and absent in the right one. In developing ovaries, Ovex1 transcription increases sharply in the left cortex and is weakly detected in the medulla. After folliculogenesis, Ovex1-expressing cells constitute the follicular granulosa cell layer. Ovex1 expression highlights a striking desquamation process that leads to profound cortical remodeling associated with follicle morphogenesis.ConclusionEvidence for a selection pressure at the protein level suggests that this endogenous retrovirus, expressed in the ovarian supporting cell lineage, might play an active role in bird ovarian physiology.

Project description:BackgroundThe genetic control of sex determination in teleost species is poorly understood. This is partly because of the diversity of mechanisms that determine sex in this large group of vertebrates, including constitutive genes linked to sex chromosomes, polygenic constitutive mechanisms, environmental factors, hermaphroditism, and unisexuality. Here we use a de novo genome assembly of New Zealand silver trevally (Pseudocaranx georgianus) together with sex-specific whole genome sequencing data to detect sexually divergent genomic regions, identify candidate genes and develop molecular makers.ResultsThe de novo assembly of an unsexed trevally (Trevally_v1) resulted in a final assembly of 579.4 Mb in length, with a N50 of 25.2 Mb. Of the assembled scaffolds, 24 were of chromosome scale, ranging from 11 to 31 Mb in length. A total of 28,416 genes were annotated after 12.8 % of the assembly was masked with repetitive elements. Whole genome re-sequencing of 13 wild sexed trevally (seven males and six females) identified two sexually divergent regions located on two scaffolds, including a 6 kb region at the proximal end of chromosome 21. Blast analyses revealed similarity between one region and the aromatase genes cyp19 (a1a/b) (E-value < 1.00E-25, identity > 78.8 %). Males contained higher numbers of heterozygous variants in both regions, while females showed regions of very low read-depth, indicative of male-specificity of this genomic region. Molecular markers were developed and subsequently tested on 96 histologically-sexed fish (42 males and 54 females). Three markers amplified in absolute correspondence with sex (positive in males, negative in females).ConclusionsThe higher number of heterozygous variants in males combined with the absence of these regions in females support a XY sex-determination model, indicating that the trevally_v1 genome assembly was developed from a male specimen. This sex system contrasts with the ZW sex-determination model documented in closely related carangid species. Our results indicate a sex-determining function of a cyp19a1a-like gene, suggesting the molecular pathway of sex determination is somewhat conserved in this family. The genomic resources developed here will facilitate future comparative work, and enable improved insights into the varied sex determination pathways in teleosts. The sex marker developed in this study will be a valuable resource for aquaculture selective breeding programmes, and for determining sex ratios in wild populations.

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Logical modelling uncovers developmental constraints for primary sex determination of chicken gonads.

Publications

Logical modelling uncovers developmental constraints for primary sex determination of chicken gonads.

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