Comparative piRNAs Profiles Give a Clue to Transgenerational Inheritance of Sex-Biased piRNAs in Cynoglossus semilaevis

Zhao, Na; Lu, Jia; Deng, Qiuxia; Zhu, Chunhua; Zhang, Bo

doi:10.1007/s10126-022-10109-z

Cited by 5 publications

(4 citation statements)

References 48 publications

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“…The growth of females was slightly faster than that of males and pseudo-males, while no significant difference was found between males and pseudo-males ( Figure S1B ), which was consistent with the sex dimorphism of growth in P. olivaceus . Similarly, the growth rate of females was also significantly faster than that of males and pseudo-males in C. semilaevis [ 37 , 38 ]. Moreover, as the sex marker, the amh gene was significantly higher expressed in P. olivaceus testis than in ovaries ( Figure S1C ), which agreed with its male-specific function that regulates spermatogenesis and promotes male sex differentiation and the development and maintenance of gonads in teleosts [ 39 , 40 ].…”

Section: Resultsmentioning

confidence: 99%

DNA Methylation Mediates Sperm Quality via piwil1 and piwil2 Regulation in Japanese Flounder (Paralichthys olivaceus)

Zong,

Wang,

Zhang

et al. 2024

IJMS

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DNA methylation is an important way to regulate gene expression in eukaryotes. In order to reveal the role of DNA methylation in the regulation of germ cell-specific piwi gene expression during spermatogenesis of Japanese flounder (Paralichthys olivaceus), the expression profiles of piwil1 (piwi-like 1) and piwil2 (piwi-like 2) genes in the gonads of female, male, and sex-reversed pseudo-male P. olivaceus were analyzed, and the dynamic of DNA methylation was investigated. As a result, piwil1 and piwil2 genes were highly expressed in the testis of both male and pseudo-male P. olivaceus, with significant variation among male individuals. The DNA methylation levels in the promoter regions of both piwil1 and piwil2 were negatively correlated with their expression levels, which may contribute to the transcriptional regulation of piwi genes during spermatogenesis. There was also sperm quality variation among male P. olivaceus, and the sperm curvilinear velocity was positively correlated with the expression of both piwil1 and piwil2 genes. These results indicated that the DNA methylation in piwil1 and piwil2 promoter regions may affect the initiation of piwi gene transcription, thereby regulating gene expression and further affecting the spermatogenesis process and gamete quality in P. olivaceus.

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Section: Resultsmentioning

confidence: 99%

DNA Methylation Mediates Sperm Quality via piwil1 and piwil2 Regulation in Japanese Flounder (Paralichthys olivaceus)

Zong,

Wang,

Zhang

et al. 2024

IJMS

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“…Differentially expressed piRNAs were identified in the serum exosomes of greater amberjack, as in the testis or/and ovary of other teleosts, including zebrafish ( Danio rerio ) [ 38 ], common carp ( Cyprinus carpio ) [ 39 ], Nile tilapia ( Oreochromis niloticus ) [ 40 , 41 ], Atlantic salmon ( Salmon salar L.) [ 42 ], turbot ( Scophthalmus maximus ) [ 43 , 44 ], sharpsnout seabream ( Diplodus puntazzo ) [ 45 ], Japanese flounder ( Paralichthys olivaceus ) [ 46 , 47 , 48 ], and C. semilaevis [ 34 , 35 , 49 ]. In these studies, the number of known piRNAs ranged from 13 in the gonads of D. puntazzo [ 45 ] to 296,775 piRNAs in the testis of O. niloticus [ 41 ].…”

Section: Discussionmentioning

confidence: 99%

“…Sex-inclined piRNAs are involved in various physiological processes, including sex development, sex differentiation, sex determination, and sex regulation in aquatic animals [ 20 , 30 , 31 , 32 , 33 , 34 ]. We have previously shown that sex-inclined exosomal piRNAs could be employed as biomarkers to identify the male and pseudo-male fish, with the same karyotype as female fish and the same physiological characteristics as male fish [ 34 ], in half smooth tongue sole ( Cynoglossus semilaevis ) [ 34 , 35 ]. In this study, piRNA profiles in serum exosomes from greater amberjack were characterized to screen differentially expressed piRNAs between sexes.…”

Section: Introductionmentioning

confidence: 99%

Sex-Inclined Piwi-Interacting RNAs in Serum Exosomes for Sex Determination in the Greater Amberjack (Seriola dumerili)

Deng

Zhao

et al. 2023

IJMS

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The greater amberjack (Seriola dumerili) is a gonochoristic fish with no sexual dimorphism in appearance, making sex identification difficult. Piwi-interacting RNAs (piRNAs) function in transposon silencing and gametogenesis and are involved in various physiological processes, including sex development and differentiation. Exosomal piRNAs can be indicators for the determination of sex and physiological status. In this study, four piRNAs were differentially expressed in both serum exosomes and gonads between male and female greater amberjack. Three piRNAs (piR-dre-32793, piR-dre-5797, and piR-dre-73318) were significantly up-regulated and piR-dre-332 was significantly down-regulated in serum exosomes and gonads of male fish, compared to female fish, consistent with the serum exosomal results. According to the relative expression of four marker piRNAs derived from the serum exosomes of greater amberjack, the highest relative expression of piR-dre-32793, piR-dre-5797, and piR-dre-73318 in seven female fish and that of piR-dre-332 in seven male fish can be used as the standard for sex determination. The method of sex identification can ascertain the sex of greater amberjack by blood collection from the living body, without sacrificing fish. The four piRNAs did not show sex-inclined expression in the hypothalamus, pituitary, heart, liver, intestine, and muscle tissue. A piRNA–target interaction network involving 32 piRNA-mRNA pairs was generated. Sex-related target genes were enriched in sex-related pathways, including oocyte meiosis, transforming growth factor-beta signaling pathway, progesterone-mediated oocyte maturation, and gonadotropin releasing hormone signaling pathway. These results provide a basis for sex determination in greater amberjack and improve our understanding of the mechanisms underlying sex development and differentiation in the species.

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“…DNA methylomes of gonads from different sexes' C. semilaevis in a recent study have revealed that the methylation modification of pseudomales is inherited in pseudomale offspring, and sex-related genes have possessed lots of methylation inherited in the process of sex reversal of C. semilaevis (Shao et al, 2014). Furthermore, micro RNAs (miRNAs) in sperm of C. semilaevis showed obvious sex bias between male and pseudomale, and some of them were inherited in pseudomale offspring Zhao et al, 2022). However, our knowledge of the DNA methylome of gametes is limited in C. semilaevis, which is an important link between the gonad methylomic map and the sperm miRomic map.…”

Section: Introductionmentioning

confidence: 99%

Integrative sperm DNA methylation and miRomics analysis highlights interaction of two epigenetic patterns of pseudomale inheritance in teleost

Zhao

Chen

et al. 2022

Front. Mar. Sci.

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Proper DNA methylation in spermatozoa is essential for the normal development of fertilized embryos through gene expression regulation. Abnormal sperm DNA methylation is associated with male fertility impairment, offspring quality decline, and disease susceptibility. Compared with other epigenetic regulatory mechanisms (e.g., histone modification), DNA methylation is a stable regulator for the long-term transcriptional activity of genes. Sperm DNA methylation is crucial to offspring’s survival, development, and reproduction. However, it has not been well studied in teleost to a large extent, especially in some species with sex deviation or congenital sex abnormality in offspring. In the present study, DNA methylation profiles of pseudomale (ZW) and male (ZZ) tongue sole (Cynoglossus semilaevis) spermatozoa were characterized for differential methylation regions (DMRs) screening. The global methylation levels of the two sperm groups were highly methylated with no significant differences. For all kinds of genomic elements, the mean methylation level of the ZW group was higher than that of the ZZ group. The total numbers of Covered C annotated on the W chromosome of both groups were extremely small, suggesting that W-type sperm did not exist in pseudomales. A comparison of methylation levels on 20 sex-related genes between sperm and gonad showed that the heterogeneity between tissue resources was greater than that between sexes, and the methylation level of most genes in gonads was lower than that in sperm. For integrative analysis of DNA methylation and miRomic profiles, 11 sex-related DMRs associated with 15 differentials micro RNAs (miRNAs) in spermatozoa were identified to present targeting relationships and regulatory trends of the two distinct epigenetic patterns. This study provides valuable and potential targets of coordination between two epigenetic mechanisms in the process of C. semilaevis sex congenital bias.

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Comparative piRNAs Profiles Give a Clue to Transgenerational Inheritance of Sex-Biased piRNAs in Cynoglossus semilaevis

Cited by 5 publications

References 48 publications

DNA Methylation Mediates Sperm Quality via piwil1 and piwil2 Regulation in Japanese Flounder (Paralichthys olivaceus)

DNA Methylation Mediates Sperm Quality via piwil1 and piwil2 Regulation in Japanese Flounder (Paralichthys olivaceus)

Sex-Inclined Piwi-Interacting RNAs in Serum Exosomes for Sex Determination in the Greater Amberjack (Seriola dumerili)

Integrative sperm DNA methylation and miRomics analysis highlights interaction of two epigenetic patterns of pseudomale inheritance in teleost

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