scholarly journals Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex

2019 ◽  
Vol 5 (5) ◽  
pp. eaau3753 ◽  
Author(s):  
Saurav Baral ◽  
Gandhimathi Arumugam ◽  
Riddhi Deshmukh ◽  
Krushnamegh Kunte

doublesex regulates early embryonic sex differentiation in holometabolous insects, along with the development of species-, sex-, and morph-specific adaptations during pupal stages. How does a highly conserved gene with a critical developmental role also remain functionally dynamic enough to gain ecologically important adaptations that are divergent in sister species? We analyzed patterns of exon-level molecular evolution and protein structural homology of doublesex from 145 species of four insect orders representing 350 million years of divergence. This analysis revealed that evolution of doublesex was governed by a modular architecture: Functional domains and female-specific regions were highly conserved, whereas male-specific sequences and protein structures evolved up to thousand-fold faster, with sites under pervasive and/or episodic positive selection. This pattern of sex bias was reversed in Hymenoptera. Thus, highly conserved yet dynamic master regulators such as doublesex may partition specific conserved and novel functions in different genic modules at deep evolutionary time scales.

PLoS Biology ◽  
2021 ◽  
Vol 19 (7) ◽  
pp. e3001330
Author(s):  
Xiao-Jin Pei ◽  
Yong-Liang Fan ◽  
Yu Bai ◽  
Tian-Tian Bai ◽  
Coby Schal ◽  
...  

Insect cuticular hydrocarbons (CHCs) serve as important intersexual signaling chemicals and generally show variation between the sexes, but little is known about the generation of sexually dimorphic hydrocarbons (SDHCs) in insects. In this study, we report the molecular mechanism and biological significance that underlie the generation of SDHC in the German cockroach Blattella germanica. Sexually mature females possess more C29 CHCs, especially the contact sex pheromone precursor 3,11-DimeC29. RNA interference (RNAi) screen against the fatty acid elongase family members combined with heterologous expression of the genes in yeast revealed that both BgElo12 and BgElo24 were involved in hydrocarbon (HC) production, but BgElo24 is of wide catalytic activities and is able to provide substrates for BgElo12, and only the female-enriched BgElo12 is responsible for sustaining female-specific HC profile. Repressing BgElo12 masculinized the female CHC profile, decreased contact sex pheromone level, and consequently reduced the sexual attractiveness of female cockroaches. Moreover, the asymmetric expression of BgElo12 between the sexes is modulated by sex differentiation cascade. Specifically, male-specific BgDsx represses the transcription of BgElo12 in males, while BgTra is able to remove this effect in females. Our study reveals a novel molecular mechanism responsible for the formation of SDHCs and also provide evidences on shaping of the SDHCs by sexual selection, as females use them to generate high levels of contact sex pheromone.


2021 ◽  
Vol 8 ◽  
Author(s):  
Qiong Wang ◽  
Jianjian Lv ◽  
Xianyun Ren ◽  
Jiajia Wang ◽  
Shaoting Jia ◽  
...  

Fenneropenaeus chinensis is a commercially cultured shrimp in China. F. chinensis adults show significant sexual dimorphism, with larger females than males. However, sex determination (SD) of F. chinensis has not yet been elucidated. Clarification of the sex-determining system of F. chinensis could enrich our knowledge of the sex differentiation mechanism in crustaceans and facilitate the study of sex-controlling technologies. Here, we studied the sex-determining system of F. chinensis using the fixation index (FST) between the sexes to detect the genetic differentiation in resequencing data of multiple males and females. We located the candidate sex chromosome in the genome of F. chinensis and concluded the female heterogametic (ZW) SD system. We also assembled female-specific sequences, which could be used as molecular markers to identify the sex of F. chinensis. However, the differentiation of the F. chinensis Z and W chromosome is limited. RNA-seq data detected many genes with male-biased expression in the Z-specific region, which possibly could further intensify the divergency between the Z and W chromosomes.


Genes ◽  
2021 ◽  
Vol 12 (2) ◽  
pp. 315
Author(s):  
Xu Yang ◽  
Kai Chen ◽  
Yaohui Wang ◽  
Dehong Yang ◽  
Yongping Huang

In insects, sex determination pathways involve three levels of master regulators: primary signals, which determine the sex; executors, which control sex-specific differentiation of tissues and organs; and transducers, which link the primary signals to the executors. The primary signals differ widely among insect species. In Diptera alone, several unrelated primary sex determiners have been identified. However, the doublesex (dsx) gene is highly conserved as the executor component across multiple insect orders. The transducer level shows an intermediate level of conservation. In many, but not all examined insects, a key transducer role is performed by transformer (tra), which controls sex-specific splicing of dsx. In Lepidoptera, studies of sex determination have focused on the lepidopteran model species Bombyx mori (the silkworm). In B. mori, the primary signal of sex determination cascade starts from Fem, a female-specific PIWI-interacting RNA, and its targeting gene Masc, which is apparently specific to and conserved among Lepidoptera. Tra has not been found in Lepidoptera. Instead, the B. mori PSI protein binds directly to dsx pre-mRNA and regulates its alternative splicing to produce male- and female-specific transcripts. Despite this basic understanding of the molecular mechanisms underlying sex determination, the links among the primary signals, transducers and executors remain largely unknown in Lepidoptera. In this review, we focus on the latest findings regarding the functions and working mechanisms of genes involved in feminization and masculinization in Lepidoptera and discuss directions for future research of sex determination in the silkworm.


IUCrJ ◽  
2019 ◽  
Vol 6 (1) ◽  
pp. 46-55 ◽  
Author(s):  
Hiroki Noguchi ◽  
Christine Addy ◽  
David Simoncini ◽  
Staf Wouters ◽  
Bram Mylemans ◽  
...  

β-Propeller proteins form one of the largest families of protein structures, with a pseudo-symmetrical fold made up of subdomains called blades. They are not only abundant but are also involved in a wide variety of cellular processes, often by acting as a platform for the assembly of protein complexes. WD40 proteins are a subfamily of propeller proteins with no intrinsic enzymatic activity, but their stable, modular architecture and versatile surface have allowed evolution to adapt them to many vital roles. By computationally reverse-engineering the duplication, fusion and diversification events in the evolutionary history of a WD40 protein, a perfectly symmetrical homologue called Tako8 was made. If two or four blades of Tako8 are expressed as single polypeptides, they do not self-assemble to complete the eight-bladed architecture, which may be owing to the closely spaced negative charges inside the ring. A different computational approach was employed to redesign Tako8 to create Ika8, a fourfold-symmetrical protein in which neighbouring blades carry compensating charges. Ika2 and Ika4, carrying two or four blades per subunit, respectively, were found to assemble spontaneously into a complete eight-bladed ring in solution. These artificial eight-bladed rings may find applications in bionanotechnology and as models to study the folding and evolution of WD40 proteins.


1998 ◽  
Vol 18 (1) ◽  
pp. 450-458 ◽  
Author(s):  
Volker Heinrichs ◽  
Lisa C. Ryner ◽  
Bruce S. Baker

ABSTRACT In Drosophila melanogaster, the fruitless(fru) gene controls essentially all aspects of male courtship behavior. It does this through sex-specific alternative splicing of the fru pre-mRNA, leading to the production of male-specific fru mRNAs capable of expressing male-specificfru proteins. Sex-specific fru splicing involves the choice between alternative 5′ splice sites, one used exclusively in males and the other used only in females. Here we report that the Drosophila sex determination genestransformer (tra) and transformer-2(tra-2) switch fru splicing from the male-specific pattern to the female-specific pattern through activation of the female-specific fru 5′ splice site. Activation of female-specific fru splicing requirescis-acting tra and tra-2 repeat elements that are part of an exonic splicing enhancer located immediately upstream of the female-specific fru 5′ splice site and are recognized by the TRA and TRA-2 proteins in vitro. Thisfru splicing enhancer is sufficient to promote the activation by tra and tra-2 of both a 5′ splice site and the female-specific doublesex (dsx) 3′ splice site, suggesting that the mechanisms of 5′ splice site activation and 3′ splice site activation may be similar.


2020 ◽  
Vol 2020 ◽  
pp. 1-10
Author(s):  
Wencai Wang ◽  
Guoqian Yang ◽  
Xin Deng ◽  
Fengqing Shao ◽  
Yongquan Li ◽  
...  

Eucommia ulmoides, also known as the industrially and medicinally important hardy rubber tree, is the sole species of Eucommiaceae. Nevertheless, its dioecious property hinders sex recognition by traditional morphological observation at very early developmental stages, thus inhibiting breeding and economic cropping. In this study, double-digest restriction site-associated DNA sequencing (ddRAD-seq) was applied to screen sex-linked molecular markers for sex identification and investigation of the sex determination system in 20 male and female E. ulmoides individual plants, respectively. In consequence, five candidate male-specific loci but no female-specific loci were predicated among the 183,752 male and 147,122 female catalogue loci by bioinformatics analysis. Subsequent PCR (polymerase chain reaction) amplification and Sanger sequencing examinations were performed on another 24 individuals, 12 for each sex, from a separate population. One ideal sex-linked locus, MSL4, was identified among the five putative male-specific loci that were found using ddRAD data. MSL4 is 479 bp in length and highly conserved in all the male individuals, suggesting its feature of being stable and repeatable. Our results also indicated that the sex of E. ulmoides is likely determined genetically. In short, this study provides a consistent and reproducible ddRAD marker (MSL4) that is able to discriminate male from female seedlings in E. ulmoides, which will be valuable for rapid breeding practice and better commercial production of this economically important tree.


Weed Science ◽  
2019 ◽  
Vol 67 (4) ◽  
pp. 412-418 ◽  
Author(s):  
Jacob S. Montgomery ◽  
Ahmed Sadeque ◽  
Darci A. Giacomini ◽  
Patrick J. Brown ◽  
Patrick J. Tranel

AbstractWaterhemp [Amaranthus tuberculatus (Moq.) J. D. Sauer] and Palmer amaranth (Amaranthus palmeri S. Watson) are troublesome weeds of row-crop production in the United States. Their dioecious reproductive systems ensure outcrossing, facilitating rapid evolution and distribution of resistances to multiple herbicides. Little is known, however, about the genetic basis of dioecy in Amaranthus species. In this work, we use restriction site–associated DNA sequencing (RAD-Seq) to investigate the genetic basis of sex determination in A. tuberculatus and A. palmeri. For each species, approximately 200 plants of each sex were sampled and used to create RAD-Seq libraries. The resulting libraries were separately bar-coded and then pooled for sequencing with the Illumina platform, yielding millions of 64-bp reads. These reads were analyzed to identify sex-specific and sex-biased sequences. We identified 345 male-specific sequences from the A. palmeri data set and 2,754 male-specific sequences in A. tuberculatus. An unexpected 723 female-specific sequences were identified in a subset of the A. tuberculatus females; subsequent research, however, indicated female specificity of these markers was limited to the population from which they were identified. Primer sets designed to specifically amplify male-specific sequences were tested for accuracy on multiple, geographically distinct populations of A. tuberculatus and A. palmeri, as well as other Amaranthus species. Two primer sets for A. palmeri and four primer sets for A. tuberculatus were each able to distinguish between male and female plants with at least 95% accuracy. In the near term, sex-specific markers will be useful to the A. tuberculatus and A. palmeri research communities (e.g., to predict sex for crossing experiments). In the long-term, this research will provide the foundational tools for detailed investigations into the molecular biology and evolution of dioecy in weedy Amaranthus species.


BMC Genetics ◽  
2020 ◽  
Vol 21 (S2) ◽  
Author(s):  
Pasquale Primo ◽  
Angela Meccariello ◽  
Maria Grazia Inghilterra ◽  
Andrea Gravina ◽  
Giuseppe Del Corsano ◽  
...  

Abstract Background Females of the Mediterranean fruit fly Ceratitis capitata (Medfly) are major agricultural pests, as they lay eggs into the fruit crops of hundreds of plant species. In Medfly, female sex determination is based on the activation of Cctransformer (Cctra). A maternal contribution of Cctra is required to activate Cctra itself in the XX embryos and to start and epigenetically maintain a Cctra positive feedback loop, by female-specific alternative splicing, leading to female development. In XY embryos, the male determining Maleness-on-the-Y gene (MoY) blocks this activation and Cctra produces male-specific transcripts encoding truncated CcTRA isoforms and male differentiation occurs. Results With the aim of inducing frameshift mutations in the first coding exon to disrupt both female-specific and shorter male-specific CcTRA open reading frames (ORF), we injected Cas9 ribonucleoproteins (Cas9 and single guide RNA, sgRNA) in embryos. As this approach leads to mostly monoallelic mutations, masculinization was expected only in G1 XX individuals carrying biallelic mutations, following crosses of G0 injected individuals. Surprisingly, these injections into XX-only embryos led to G0 adults that included not only XX females but also 50% of reverted fertile XX males. The G0 XX males expressed male-specific Cctra transcripts, suggesting full masculinization. Interestingly, out of six G0 XX males, four displayed the Cctra wild type sequence. This finding suggests that masculinization by Cas9-sgRNA injections was independent from its mutagenic activity. In line with this observation, embryonic targeting of Cctra in XX embryos by a dead Cas9 (enzymatically inactive, dCas9) also favoured a male-specific splicing of Cctra, in both embryos and adults. Conclusions Our data suggest that the establishment of Cctra female-specific autoregulation during the early embryogenesis has been repressed in XX embryos by the transient binding of the Cas9-sgRNA on the first exon of the Cctra gene. This hypothesis is supported by the observation that the shift of Cctra splicing from female to male mode is induced also by dCas9. Collectively, the present findings corroborate the idea that a transient embryonic inactivation of Cctra is sufficient for male sex determination.


1970 ◽  
Vol 16 (2) ◽  
pp. 215-224 ◽  
Author(s):  
J. S. Pitton ◽  
E. S. Anderson

SUMMARYA selection offi+resistance factors and transfer factors, when introduced into K 12F+, showed a range of inhibitory activity of lysis by the male-specific phage μ 2. This range can be used to subdivide thefi+factors intofi+1,fi+2,fi+3andfi+4classes, according to the degree of inhibition of μ 2 lysis. To this subdivision can be added restriction of the ‘female-specific’ phage φ 2.Introduction of all thefi+factors tested into K 12 HfrH totally inhibited lysis by μ 2 in spot tests, but with twofi+1and onefi+2factors visible lysis was obtained in agar-layer tests. These three factors caused least inhibition of transfer ofproby HfrH. It can be assumed that both tests reflect lower inhibition of sex fimbrial formation by thesefi+factors than by the remainder.Thefi−factors, when introduced into K 12, can be subdivided on the basis of restrictive effects on phage φ 2.These effects can be added to phage restriction in the salmonellae for the purposes of further classification of the transfer factors and R-factors.


2013 ◽  
Vol 219 (1) ◽  
pp. 39-49 ◽  
Author(s):  
Hiroto Kobayashi ◽  
Saori Yoshida ◽  
Ying-Jie Sun ◽  
Nobuyuki Shirasawa ◽  
Akira Naito

Cholestasis is associated with changes in hepatic cholesterol metabolism and serum estrogen levels. Ueyama and colleagues reported that the gastric estradiol-17β (E2) level in the portal vein is several times higher than that in the artery. This study aimed to clarify the relationships between gastric E2, hepatic estrogen receptor (ER) α and cholesterol metabolism in cholestatic male rats induced by bile duct ligation (BDL). After BDL, serum E2 levels in the portal vein and artery were measured by ELISA. The gene expression of gastric estrogen-synthesizing enzymes and various hepatic enzymes for cholesterol metabolism were measured by real-time RT-PCR, and gastric aromatase and hepatic ERα proteins were determined by immunohistochemistry and western blotting. Portal E2 levels increased by 4.9, 5.0, and 3.6 times that of controls at 2 days after BDL (BDL2d), BDL4d, and BDL7d respectively. The change in arterial E2 levels was positively correlated with that in the portal vein. Under these conditions, the expression of hepatic Ers1 (ERα) mRNA and protein was significantly reduced in a negative correlation with serum E2 levels in the portal vein after BDL. The expression of hepatic male-specific cytochrome P450 (CYP) genes Cyp2c55 and Cyp3a2 decreased and female-specific Cyp2c12 increased after BDL. It is postulated that the increase in gastric E2 levels, which occurs after BDL, results in the reduction of hepatic ERα, the elevation of arterial E2 level and leads to cholesterol metabolism becoming sex steroid dependent.


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