The Sex Determination Cascade in the Silkworm

Xu, Yang; Chen, Kai; Wang, Yaohui; Yang, Dehong; Huang, Yongping

doi:10.3390/genes12020315

Cited by 17 publications

(27 citation statements)

References 101 publications

(81 reference statements)

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“…Thus, a possible function of AllWSEX2 and the transposase-like sequence located to the 3′ of AllWSEX2 should be further studied, including the possibility of their involvement in female transposon silencing. However, repression of transposable elements has been shown to participate in sex determination only in invertebrates (Yang et al, 2021); and transposable elements are over-expressed in testes of fish with no obvious association to sex determination (Dechaud et al, 2021).…”

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confidence: 99%

Cross‐species conservation of a transposase‐linked element enables genetic sexing of commercial populations of Russian sturgeon (Acipenser gueldenstaedtii)

et al. 2022

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All-female culture of sturgeon is essential for efficient caviar production.However, Russian sturgeon (Acipenser gueldenstaedtii) does not exhibit external sexual dimorphism, and therefore, commercial farms apply gonadal endoscopy or ultrasound at the earliest age of 4-5 years to separate the sexes, with ~90% accuracy. Recently, a dominant genomic marker (AllWSEX2) has been found with association to femaleness in sturgeons. We developed a duplex PCR (dAllWSEX2) with the adjacent bmp7 gene as an internal control, to validate an effective PCR. Robust amplification of control fragments was observed for all samples of our commercial A. gueldenstaedtii stock (n = 337). The dAllWSEX2 assay was significantly associated with sex (n = 43, p < 1.6 × 10 −8 ), yet four (18%) of the endoscopy-determined females were genetic males. To examine whether some females display a male genetic profile, we tested 96 eggproducing females, which were all verified as genetic females, indicating that the observed mismatches may be attributed to wrong sexing by endoscopy. Application of dAllWSEX2 on 100 7-month-old fish showed no sex-dependent differences in body weight, indicating that weighing is not an applicable tool for sorting females at a young age. Sanger sequencing of the bmp7 fragment revealed octaploidy and sex-independent variation, suggesting that the critical sex-determining region harboring AllWSEX2 is small. In keeping with a model of a single-ploidy encoding female determination, AllWSEX2 showed no variation despite being a transposase-linked repetitive element. Cross-species conservation of AllWSEX2, and absence of annotated sex-determination genes in this region suggests that, in sturgeons, the sex-determining mechanism is different from mechanisms identified in other fish.

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confidence: 99%

Cross‐species conservation of a transposase‐linked element enables genetic sexing of commercial populations of Russian sturgeon (Acipenser gueldenstaedtii)

et al. 2022

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“…In Drosophila, mutation of Dart5 (homolog of Prmt5) leads to a failure in the sDMA modification of PIWIs and Tudors, which compromises their ability to interact with other proteins and to be properly localized in the cells, eventually resulting in severe defects in oogenesis [35,36]. However, our previous studies have shown that mutation of either PIWIs or Tudors basically barely affects male fertility in B, mori [52,53]. In this study, as mutation of BmPrmt5 does not affect the protein stability of Previous studies have demonstrated that morphology defects in the bundles of either eupyrene or apyrene sperm compromise their physiological function [14,16,54].…”

Section: Discussionmentioning

confidence: 99%

The Prmt5-Vasa module is essential for dichotomous spermatogenesis in Bombyx mori

Yang

2022

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Spermatogenesis is a key process for the sexual reproduction species. In lepidopteran insects, dichotomous spermatogenesis is a notable feature, which produces eupyrene (nucleate) and apyrene (anucleate) spermatozoa. Both sperm morphs are essential for fertilization, as eupyrene sperm fertilizes the egg, while apyrene sperm is necessary for eupyrene sperm migration. In Drosophila, Prmt5 acts as a type II arginine methyltransferase to catalyze the symmetrical dimethylation of arginine residues (sDMA) in Vasa. However, Prmt5 is involved in regulating spermatogenesis, but Vasa is not. To date, the functional genetic study on dichotomous spermatogenesis in the lepidopteran model Bombyx mori has been limited, thus the underlying mechanism remains largely unknown. In this study, we report that both BmPrmt5 and BmVasa act as essential components in the regulation of dichotomous spermatogenesis in Bombyx mori. The loss-of-function mutants of BmPrmt5 (△BmPrmt5) and BmVasa (△BmVasa) derived from CRISPR/Cas9-based gene editing show similar male and female-sterile phenotypes. Through immunofluorescence staining analysis, we found that the morphs of both △BmPrmt5 and △BmVasa sperm show severe defects, indicating an essential role for both BmPrmt5 and BmVasa in the regulation of dichotomous spermatogenesis. RNA-seq analyses indicate that the defects in dichotomous spermatogenesis observed for △BmPrmt5 and △BmVasa mutants could be attributed to the reduced expression of the spermatogenesis-related genes including Sex-lethal (BmSxl), implying that BmSxl may act downstream of Prmt5 and Vasa in regulating apyrene sperm development. These findings suggest that BmPrmt5 and BmVasa constitute an integral regulatory module essential for dichotomous spermatogenesis in Bombyx mori, in which BmPrmt5 may promote BmVasa activity through sDMA modification.

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“…Chen et al, 2020;S. Chen et al, 2020;Li et al, 2018;Yang et al, 2021). For example, BmMael is involved in the regulation of both morphs of sperm development, while BmPnldc1 is required for eupyrene sperm development.…”

Section: Morimentioning

confidence: 99%

“…Mutations in piRNA biogenesis pathway typically result in sterility with stereotypical phenotypes in the female or male germline (Juliano et al, 2011). In B. mori , the biochemical functions of the components involved in piRNA biogenesis such as PIWIs (Siwi and BmAgo3), and BmPnldc1, BmHen1 and BmPapi are well studied in ovary-derived cells (BmN) (Sakakibara and Siomi, 2018), and some of them have been physiologically characterized in vivo (Chen et al, 2019; K. Chen et al, 2020; S. Chen et al, 2020; Li et al, 2018; Yang et al, 2021). For example, BmMael is involved in the regulation of both morphs of sperm development, while BmPnldc1 is required for eupyrene sperm development.…”

Section: Introductionmentioning

confidence: 99%

BmHen1 plays an essential role in the regulation of eupyrene sperm development in Bombyx mori

Yang

2022

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In lepidopteran insects, sperm polymorphism is a remarkable feature, in which males exhibit two different types of sperms. Both sperm morphs are essential for fertilization as eupyrene (nucleate) sperm carries DNA and fertilizes the egg, while apyrene (anucleate) sperm is necessary for transporting eupyrene sperm into females. To date, the functional genetic study on dichotomous spermatogenesis has been limited. It is known that, in the model species including mice, worms, and flies, the components in piRNA biogenesis pathway play an important role in gonad development. In this study, we characterize BmHen1 as a new critical component involved in the regulation of eupyrene sperm development in B. mori. We generated the loss-of-function mutant of BmHen1 (△BmHen1) through CRISPR/Cas9-based gene editing, and found that it is both female- and male-sterile. △BmHen1 females lay significantly fewer eggs than wild-type, which display morphological defects. Fluorescence staining assays show that the △BmHen1 eupyrene sperms exhibit severe defects in nuclei formation, while its apyrene sperms are normal. We then constructed the loss-of-function mutants of Siwi and BmAgo3 (△Siwi and △BmAgo3) through CRISPR/Cas9-based gene editing, which encode PIWI proteins acting as the core elements in piRNA biogenesis, and explored whether they might be involved in spermatogenesis. To our surprise, △Siwi and △BmAgo3 mutants develop normal male reproduction system, indicating that they do not participate in sperm development. As the activity of BmHen1 depends on BmPnldc1 during piRNA biogenesis, and △BmHen1 and △BmPnldc1 mutants display similar defects in sperm development, we performed RNA sequencing analysis to look for the genes that might be co-regulated by BmHen1 and BmPnldc1. Our results indicate that the defects in △BmHen1 and △BmPnldc1 eupyrene sperms could be attributed to dysregulated genes involved in energy metabolism and cell differentiation. Furthermore, we found that the piRNA biogenesis is inhibited in △BmHen1 and △BmPnldc1 sperm bundles, whereas the transposon activity was induced. Taken together, our findings suggest that BmHen1 is a new crucial component regulating eupyrene sperm development in B. mori, whereas the PIWI proteins Siwi and BmAgo3 are not involved in this process. Our results may provide a potential gene target for genetic modification of sterility in B. mori.

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The Sex Determination Cascade in the Silkworm

Cited by 17 publications

References 101 publications

Cross‐species conservation of a transposase‐linked element enables genetic sexing of commercial populations of Russian sturgeon (Acipenser gueldenstaedtii)

Cross‐species conservation of a transposase‐linked element enables genetic sexing of commercial populations of Russian sturgeon (Acipenser gueldenstaedtii)

The Prmt5-Vasa module is essential for dichotomous spermatogenesis in Bombyx mori

BmHen1 plays an essential role in the regulation of eupyrene sperm development in Bombyx mori

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