scholarly journals Gonadal transcriptomes associated with sex phenotypes provide potential male and female candidate genes of sex determination or early differentiation in Crassostrea gigas, a sequential hermaphrodite mollusc

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Coralie Broquard ◽  
Suwansa-ard Saowaros ◽  
Mélanie Lepoittevin ◽  
Lionel Degremont ◽  
Jean-Baptiste Lamy ◽  
...  

Abstract Background In the animal kingdom, mollusca is an important phylum of the Lophotrochozoa. However, few studies have investigated the molecular cascade of sex determination/early gonadal differentiation within this phylum. The oyster Crassostrea gigas is a sequential irregular hermaphrodite mollusc of economic, physiological and phylogenetic importance. Although some studies identified genes of its sex-determining/−differentiating pathway, this particular topic remains to be further deepened, in particular with regard to the expression patterns. Indeed, these patterns need to cover the entire period of sex lability and have to be associated to future sex phenotypes, usually impossible to establish in this sequential hermaphrodite. This is why we performed a gonadal RNA-Seq analysis of diploid male and female oysters that have not changed sex for 4 years, sampled during the entire time-window of sex determination/early sex differentiation (stages 0 and 3 of the gametogenetic cycle). This individual long-term monitoring gave us the opportunity to explain the molecular expression patterns in the light of the most statistically likely future sex of each oyster. Results The differential gene expression analysis of gonadal transcriptomes revealed that 9723 genes were differentially expressed between gametogenetic stages, and 141 between sexes (98 and 43 genes highly expressed in females and males, respectively). Eighty-four genes were both stage- and sex-specific, 57 of them being highly expressed at the time of sex determination/early sex differentiation. These 4 novel genes including Trophoblast glycoprotein-like, Protein PML-like, Protein singed-like and PREDICTED: paramyosin, while being supported by RT-qPCR, displayed sexually dimorphic gene expression patterns. Conclusions This gonadal transcriptome analysis, the first one associated with sex phenotypes in C. gigas, revealed 57 genes highly expressed in stage 0 or 3 of gametogenesis and which could be linked to the future sex of the individuals. While further study will be needed to suggest a role for these factors, some could certainly be original potential actors involved in sex determination/early sex differentiation, like paramyosin and could be used to predict the future sex of oysters.

2018 ◽  
Author(s):  
Αλέξανδρος Τσακογιάννης

The differences between sexes and the concept of sex determination have always fascinated, yet troubled philosophers and scientists. Among the animals that reproduce sexually, teleost fishes show a very wide repertoire of reproductive modes. Except for the gonochoristic species, fish are the only vertebrates in which hermaphroditism appears naturally. Hermaphroditism refers to the capability of an organism to reproduce both as male and female in its life cycle and there are various forms of it. In sequential hermaphroditism, an individual begins as female first and then can change sex to become male (protogyny), or vice versa (protandry). The diverse sex-phenotypes of fish are regulated by a variety of sex determination mechanisms, along a continuum of environmental and heritable factors. The vast majority of sexually dimorphic traits result from the differential expression of genes that are present in both sexes. To date, studies regarding the sex-specific differences in gene expression have been conducted mainly in sex determination systems of model fish species that are well characterized at the genomic level, with distinguishable heteromorphic sex chromosomes, exhibiting genetic sex determination and gonochorism. Among teleosts, the Sparidae family is considered to be one of the most diversified families regarding its reproductive systems, and thus is a unique model for comparative studies to understand the molecular mechanisms underlying different sexual motifs. In this study, using RNA sequencing, we studied the transcriptome from gonads and brains of both sexes in five sparid species, representatives of four different reproductive styles. Specifically, we explored the sex-specific expression patterns of a gonochoristic species: the common dentex Dentex dentex, two protogynous hermaphrodites: the red porgy Pagrus pagrus and the common pandora Pagellus erythrinus, the rudimentary hermaphrodite sharpsnout seabream Diplodus puntazzo, and the protandrous gilthead seabream Sparus aurata. We found minor sex-related expression differences indicating a more homogeneous and sexually plastic brain, whereas there was a plethora of sex biased gene expression in the gonads. The functional divergence of the two gonadal types is reflected in their transcriptomic profiles, in terms of the number of genes differentially expressed, as well as the expression magnitude (i.e. fold-change differences). The observation of almost double the number of up-regulated genes in males compared to females indicates a male-biased expression tendency. Focusing on the pathways and genes implicated in sex determination/differentiation, we aimed to unveil the molecular pathways through which these non-model fish species develop a masculine or a feminine character. We observed the implicated pathways and major gene families (e.g. Wnt/b-catenin pathway and Retinoic-acid signaling pathway, Notch, TGFβ) behind sex-biased expression and the recruitment of known sex-related genes either to male or female type of gonads in these fish. (e.g Dmrt1, Sox9, Sox3, Cyp19a, Filgla, Ctnnb1, Gsdf9, Stra6 etc.). We also carefully investigated the presence of genes reported to be involved in sex determination/differentiation mechanisms in other vertebrates and fish and compared their expression patterns in the species under study. The expression profiling exposed known candidate molecular-players/genes establishing the common female (Cyp19a1, Sox3, Figla, Gdf9, Cyp26a, Ctnnb1, Dnmt1, Stra6) and male identity (Dmrt1, Sox9, Dnmt3aa, Rarb, Raraa, Hdac8, Tdrd7) of the gonad in these sparids. Additionally, we focused on those contributing to a species-specific manner either to female (Wnt4a, Dmrt2a, Foxl2 etc.) or to male (Amh, Dmrt3a, Cyp11b etc.) characters, and discussed the expression patterns of factors that belong to important pathways and/or gene families in the SD context, in our species gonadal transcriptomes. Taken together, most of the studied genes form part of the cascade of sex determination, differentiation, and reproduction across teleosts. In this study, we focused on genes that are active when sex is established (sex-maintainers), revealing the basic “gene-toolkit” & gene-networks underlying functional sex in these five sparids. Comparing related species with alternative reproductive styles, we saw different combinations of genes with conserved sex-linked roles and some “handy” molecular players, in a “partially- conserved” or “modulated” network formulating the male and female phenotype. The knowledge obtained in this study and tools developed during the process have set the groundwork for future experiments that can improve the sex control of this species and help the in-deep understanding the complex process of sex differentiation in the more flexible multi-component systems as these studied here.


2021 ◽  
Author(s):  
Dieter Mueller ◽  
Enora Gachet ◽  
Olivier Godfroy ◽  
Josselin Gueno ◽  
Guillaume Cossard ◽  
...  

In UV sexual systems, sex is determined during the haploid phase of the life cycle and males have a V chromosome whereas females have a U chromosome. Previous work in the brown algal model Ectocarpus revealed that the V chromosome has a dominant role in male sex determination and suggested that the female developmental program may occur by default, triggered in the absence of the male master sex determination gene(s). Here, we describe the identification of a genetically male giant kelp strain presenting phenotypic features typical of a female, despite lacking the U-specific region. The conversion to the female developmental program is however incomplete, because gametes of this feminised male are unable to produce the sperm-attracting pheromone lamoxirene. We identify the transcriptomic patterns underlying the male and female specific developmental programs, and reveal the faster evolutionary rates of male-biased genes compared to female-biased and unbiased genes. Moreover, we show that the phenotypic feminisation of the variant strain is associated with both feminisation and de-masculinisation of gene expression patterns. Importantly, the feminisation phenotype was associated with the dramatic downregulation of two V-specific genes including a candidate sex-determining gene on the V-specific region. Our results reveal the transcriptional changes associated with sexual differentiation in a UV system with marked sexual dimorphism, and contribute to disentangling the role of sex-linked genes and autosomal gene expression in the initiation of the male and female developmental programs. Overall, the data presented here imply that the U-specific region in the giant kelp is not required to initiate the female developmental program, but is critical to produce fully functional eggs, arguing against the idea that female is the default sex in this species.


Polar Biology ◽  
2019 ◽  
Vol 42 (12) ◽  
pp. 2205-2217
Author(s):  
Leonie Suter ◽  
Andrea Maree Polanowski ◽  
Robert King ◽  
Chiara Romualdi ◽  
Gabriele Sales ◽  
...  

Abstract Antarctic krill (Euphausia superba) is a highly abundant keystone species of the Southern Ocean ecosystem, directly connecting primary producers to high-trophic level predators. Sex ratios of krill vary remarkably between swarms and this phenomenon is poorly understood, as identification of krill sex relies on external morphological differences that appear late during development. Sex determination mechanisms in krill are unknown, but could include genetic, environmental or parasitic mechanisms. Similarly, virtually nothing is known about molecular sex differentiation. The krill genome has to date not been sequenced, and due to its enormous size and large amount of repetitive elements, it is currently not feasible to develop sex-specific DNA markers. To produce a reliable molecular marker for sex in krill and to investigate molecular sex differentiation we therefore focused on identifying sex-specific transcriptomic differences. Through transcriptomic analysis, we found large gene expression differences between testes and ovaries and identified three genes exclusively expressed in female whole krill from early juvenile stages onwards. The sex-specific expression of these three genes persisted through sexual regression, although our regressed samples originated from a krill aquarium and may differ from wild-regressed krill. Two slightly male-biased genes did not display sufficient expression differences to clearly differentiate sexes. Based on the expression of the three female-specific genes we developed a molecular test that for the first time allows the unambiguous sex determination of krill samples lacking external sex-specific features from juvenile stages onwards, including the sexually regressed krill we examined.


2017 ◽  
Author(s):  
Diane Maitre ◽  
Oliver M. Selmoni ◽  
Anshu Uppal ◽  
Lucas Marques da Cunha ◽  
Laetitia G. E. Wilkins ◽  
...  

AbstractFish can be threatened by distorted sex ratios that arise during sex differentiation. It is therefore important to understand sex determination and differentiation, especially in river-dwelling fish that are often exposed to environmental factors that may interfere with sex differentiation. However, sex differentiation is not sufficiently understood in keystone taxa such as the Thymallinae, one of the three salmonid subfamilies. Here we study a wild grayling (Thymallus thymallus) population that suffers from distorted sex ratios. We found sex determination in the wild and in captivity to be genetic and linked to the sdY locus. We therefore studied sex-specific gene expression in embryos and early larvae that were bred and raised under different experimental conditions, and we studied gonadal morphology in five monthly samples taken after hatching. Significant sex-specific changes in gene expression (affecting about 25,000 genes) started around hatching. Gonads were still undifferentiated three weeks after hatching, but about half of the fish showed immature testes around seven weeks after hatching. Over the next few months, this phenotype was mostly replaced by the “testis-to-ovary” or “ovaries” phenotypes. The gonads of the remaining fish, i.e. approximately half of the fish in each sampling period, remained undifferentiated until six months after fertilization. Genetic sexing of the last two samples revealed that fish with undifferentiated gonads were all males, who, by that time, were on average larger than the genetic females (verified in 8-months old juveniles raised in another experiment). Only 12% of the genetic males showed testicular tissue six months after fertilization. We conclude that sex differentiation starts around hatching, goes through an all-male stage for both sexes (which represents a rare case of “undifferentiated” gonochoristic species that usually go through an all-female stage), and is delayed in males who, instead of developing their gonads, grow faster than females during these juvenile stages.Author contributionMRR and CW initiated the project. DM, OS, AU, LMC, LW, and CW sampled the adult fish, did the experimental in vitro fertilizations, and prepared the embryos for experimental rearing in the laboratory. All further manipulations on the embryos and the larvae were done by DM, OS, AU, LMC, and LW. The RNA-seq data were analyzed by OS, JR, and MRR, the histological analyses were done by DM, supervised by SK, and the molecular genetic sexing was performed by DM, OS, AU, and KBM. DM, OS, and CW performed the remaining statistical analyses and wrote the first version of the manuscript that was then critically revised by all other authors.


Science ◽  
2021 ◽  
Vol 371 (6527) ◽  
pp. 396-400 ◽  
Author(s):  
Charalampos Chrysovalantis Galouzis ◽  
Benjamin Prud’homme

Sexual dimorphism in animals results from sex-biased gene expression patterns. These patterns are controlled by genetic sex determination hierarchies that establish the sex of an individual. Here we show that the male-biased wing expression pattern of the Drosophila biarmipes gene yellow, located on the X chromosome, is independent of the fly sex determination hierarchy. Instead, we find that a regulatory interaction between yellow alleles on homologous chromosomes (a process known as transvection) silences the activity of a yellow enhancer functioning in the wing. Therefore, this enhancer can be active in males (XY) but not in females (XX). This transvection-dependent enhancer silencing requires the yellow intron and the chromatin architecture protein Mod(mdg4). Our results suggest that transvection can contribute more generally to the sex-biased expression of X-linked genes.


Author(s):  
M. Balaganesan ◽  
K. Karalmarx ◽  
R. Jeya Shakila

Background: The existence of two distinct forms within a species that differ in one or more characteristics is known as dimorphism. The gonads are the primary organs in teleost to show sexual dimorphism. Lepidocephalus thermalis belongs to the Cobitidae family. No expression study on the developmental stages was done on this species. Since there is no specific primers reported for L. thermalis, the study has been carried out with the help of the specific primers of catfish. Methods: qRT- PCR is an acknowledged method for gene expression analysis due to its precision and reproducibility. In the current study, the expression of 14 different transcription factors involved in sex differentiation of Indian spiny loach during different developmental stages was analyzed using qRT- PCR and has been compared among the different stages of gonadal development for that transcription factor. Results: Gene expression patterns have been obtained from the total RNA isolated from MSG (Meso nephric gonadal complex), medium stage ovary, medium stage testis, large stage ovary and large stage testis. From the study, it has been analyzed that only sf1 has higher expression in testis and all the other transcription factors has shown higher expression in ovary.


Genes ◽  
2021 ◽  
Vol 12 (6) ◽  
pp. 873
Author(s):  
Shahrbanou Hosseini ◽  
Armin Otto Schmitt ◽  
Jens Tetens ◽  
Bertram Brenig ◽  
Henner Simianer ◽  
...  

The transcriptional regulation of gene expression in higher organisms is essential for different cellular and biological processes. These processes are controlled by transcription factors and their combinatorial interplay, which are crucial for complex genetic programs and transcriptional machinery. The regulation of sex-biased gene expression plays a major role in phenotypic sexual dimorphism in many species, causing dimorphic gene expression patterns between two different sexes. The role of transcription factor (TF) in gene regulatory mechanisms so far has not been studied for sex determination and sex-associated colour patterning in zebrafish with respect to phenotypic sexual dimorphism. To address this open biological issue, we applied bioinformatics approaches for identifying the predicted TF pairs based on their binding sites for sex and colour genes in zebrafish. In this study, we identified 25 (e.g., STAT6-GATA4; JUN-GATA4; SOX9-JUN) and 14 (e.g., IRF-STAT6; SOX9-JUN; STAT6-GATA4) potentially cooperating TFs based on their binding patterns in promoter regions for sex determination and colour pattern genes in zebrafish, respectively. The comparison between identified TFs for sex and colour genes revealed several predicted TF pairs (e.g., STAT6-GATA4; JUN-SOX9) are common for both phenotypes, which may play a pivotal role in phenotypic sexual dimorphism in zebrafish.


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