Cynoglossus semilaevis

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Cynoglossus semilaevis, commonly known as the Chinese tongue sole, is a popular aquaculture flatfish species. [1] They are native to China's northern coast but have experienced overfishing these past three decades. [1] [2] Tongue sole farming began in 2003 and they have since become a popular, expensive seafood. [2] However, tongue soles have created issues for farmers due to their pathogen susceptibility and uneven sex ratio. [2]

Contents

Sex determination

Sex & sex reversal

Cynoglossus semilaevis have a female heterogametic sex-determination system, with females being ZW and males being ZZ. [3] Female tongue soles grow up to 2-4 times larger and faster than males. As such, female tongue soles are preferred by farmers and attempts have been made to breed all-female stocks via artificial gynogenesis. [4] In both the wild and in aquaculture, the sex ratio of Cynoglossus semilaevis is male-skewed due to a number of the females becoming pseudomales. [5] Pseudomales have female ZW chromosomes, but become physiologically male. [6] The offspring of pseudomales have a significantly lower growth rate than the offspring of males, and are more likely to become pseudomales themselves, further skewing the sex ratio. [3] [5] This change occurs due to a combination of genotypic sex determination and temperature-dependent sex determination. [7] Exposure to higher temperatures during the gonadal sex differentiation stage (~56–62 days post-hatching) makes the sex change more likely, with one study finding that the percentage of females who became pseudomales was increased to 73% when reared at a higher temperature (28°C) as opposed to a 14% sex-reversal rate when reared at an ambient temperature (22°C). [3] [8] Furthermore, the offspring of the pseudomales reared at 28°C had a sex-reversal rate of 94% despite being reared at 22°C. [3] This high rate of females becoming pseudomales in the F2 generation was attributed to the offspring inheriting their Z chromosome from their pseudomale father and retaining paternal methylation patterns. [9]

Sex-specific molecular markers

A single SNP, Cyn_Z_6676874, allows certain females to become pseudomales. [10] Females with a thymine at this site can undergo sex reversal, but females with an adenine cannot. [10] There are also three known female-specific molecular markers that can be used to distinguish between the various tongue sole sexes. [5] Two SNPs, SNP_chr_8935925_C_T and SNP_chr_8936186_C_G, and one indel were found to enable accurate differentiation between males, females, and pseudomales. [5]

Gene expression in the gonads

Gene expression in the gonads of males and females are different before sex determination, after sex determination, and after exposure to higher temperatures. [11] Prior to sex determination, males and females have differentially expressed genes (DEGs) related to muscle development. [11] Following sex determination, females have upregulated female-specific genes, figla and foxl2, and downregulation of the male-specific genes, dmrt1 and amh, under both ambient and high-temperature conditions. [11] When exposed to higher temperatures, males, females, and pseudomales have hundreds of DEGs in common that are mainly involved in biological processes and molecular functions. [11]

Pseudomale gonads have more similar gene expression patterns to males than females. [7] DEGs between males and pseudomales played a role in spermatogenesis and energy metabolism. [11] Whereas, DEGS between females and pseudomales were related to steroid hormones, helicase activity, sexual differentiation, and development. [11]

Related Research Articles

<span class="mw-page-title-main">XY sex-determination system</span> Method of determining sex

The XY sex-determination system is a sex-determination system used to classify many mammals, including humans, some insects (Drosophila), some snakes, some fish (guppies), and some plants. In this system, the sex of an individual is determined by a pair of sex chromosomes. In most cases, females have two of the same kind of sex chromosome (XX), and are called the homogametic sex. Males have two different kinds of sex chromosomes (XY), and are called the heterogametic sex.

<span class="mw-page-title-main">Sex-determination system</span> Biological system that determines the development of organism’s sex

A sex-determination system is a biological system that determines the development of sexual characteristics in an organism. Most organisms that create their offspring using sexual reproduction have two common sexes and a few less common intersex variations.

<span class="mw-page-title-main">Gonad</span> Gland that produces sex cells

A gonad,sex gland, or reproductive gland is a mixed gland that produces the gametes and sex hormones of an organism. Female reproductive cells are egg cells, and male reproductive cells are sperm. The male gonad, the testicle, produces sperm in the form of spermatozoa. The female gonad, the ovary, produces egg cells. Both of these gametes are haploid cells. Some hermaphroditic animals have a type of gonad called an ovotestis.

<span class="mw-page-title-main">Sexual differentiation</span> Embryonic development of sex differences

Sexual differentiation is the process of development of the sex differences between males and females from an undifferentiated zygote. Sex determination is often distinct from sex differentiation; sex determination is the designation for the development stage towards either male or female, while sex differentiation is the pathway towards the development of the phenotype.

<span class="mw-page-title-main">Aromatase</span> Enzyme involved in estrogen production

Aromatase, also called estrogen synthetase or estrogen synthase, is an enzyme responsible for a key step in the biosynthesis of estrogens. It is CYP19A1, a member of the cytochrome P450 superfamily, which are monooxygenases that catalyze many reactions involved in steroidogenesis. In particular, aromatase is responsible for the aromatization of androgens into estrogens. The enzyme aromatase can be found in many tissues including gonads, brain, adipose tissue, placenta, blood vessels, skin, and bone, as well as in tissue of endometriosis, uterine fibroids, breast cancer, and endometrial cancer. It is an important factor in sexual development.

<span class="mw-page-title-main">Sex-determining region Y protein</span> Protein that initiates male sex determination in therian mammals

Sex-determining region Y protein (SRY), or testis-determining factor (TDF), is a DNA-binding protein encoded by the SRY gene that is responsible for the initiation of male sex determination in therian mammals. SRY is an intronless sex-determining gene on the Y chromosome. mutations in this gene lead to a range of disorders of sex development with varying effects on an individual's phenotype and genotype.

An oogonium is a small diploid cell which, upon maturation, forms a primordial follicle in a female fetus or the female gametangium of certain thallophytes.

<span class="mw-page-title-main">XX male syndrome</span> Congenital condition where an individual with a 46,XX karyotype has male characteristics

XX male syndrome, also known as de la Chapelle syndrome, is a rare congenital intersex condition in which an individual with a 46, XX karyotype has phenotypically male characteristics that can vary among cases. Synonyms include 46,XX testicular difference of sex development, 46,XX sex reversal, nonsyndromic 46,XX testicular DSD, and XX sex reversal.

<span class="mw-page-title-main">Genital ridge</span>

The genital ridge is the precursor to the gonads. The genital ridge initially consists mainly of mesenchyme and cells of underlying mesonephric origin. Once oogonia enter this area they attempt to associate with these somatic cells. Development proceeds and the oogonia become fully surrounded by a layer of cells.

<span class="mw-page-title-main">Sexual differentiation in humans</span> Process of development of sex differences in humans

Sexual differentiation in humans is the process of development of sex differences in humans. It is defined as the development of phenotypic structures consequent to the action of hormones produced following gonadal determination. Sexual differentiation includes development of different genitalia and the internal genital tracts and body hair plays a role in sex identification.

<span class="mw-page-title-main">Temperature-dependent sex determination</span>

Temperature-dependent sex determination (TSD) is a type of environmental sex determination in which the temperatures experienced during embryonic/larval development determine the sex of the offspring. It is only observed in reptiles and teleost fish. TSD differs from the chromosomal sex-determination systems common among vertebrates. It is the most studied type of environmental sex determination (ESD). Some other conditions, e.g. density, pH, and environmental background color, are also observed to alter sex ratio, which could be classified either as temperature-dependent sex determination or temperature-dependent sex differentiation, depending on the involved mechanisms. As sex-determining mechanisms, TSD and genetic sex determination (GSD) should be considered in an equivalent manner, which can lead to reconsidering the status of fish species that are claimed to have TSD when submitted to extreme temperatures instead of the temperature experienced during development in the wild, since changes in sex ratio with temperature variation are ecologically and evolutionally relevant.

<span class="mw-page-title-main">Disorders of sex development</span> Medical conditions involving the development of the reproductive system

Disorders of sex development (DSDs), also known as differences in sex development, diverse sex development and variations in sex characteristics (VSC), are congenital conditions affecting the reproductive system, in which development of chromosomal, gonadal, or anatomical sex is atypical.

<span class="mw-page-title-main">Steroidogenic factor 1</span> Protein-coding gene in humans

The steroidogenic factor 1 (SF-1) protein is a transcription factor involved in sex determination by controlling the activity of genes related to the reproductive glands or gonads and adrenal glands. This protein is encoded by the NR5A1 gene, a member of the nuclear receptor subfamily, located on the long arm of chromosome 9 at position 33.3. It was originally identified as a regulator of genes encoding cytochrome P450 steroid hydroxylases, however, further roles in endocrine function have since been discovered.

<span class="mw-page-title-main">SOX9</span> Transcription factor gene of the SOX family

Transcription factor SOX-9 is a protein that in humans is encoded by the SOX9 gene.

<span class="mw-page-title-main">FGF9</span> Protein-coding gene in the species Homo sapiens

Glia-activating factor is a protein that in humans is encoded by the FGF9 gene.

SOAP is a suite of bioinformatics software tools from the BGI Bioinformatics department enabling the assembly, alignment, and analysis of next generation DNA sequencing data. It is particularly suited to short read sequencing data.

Odontobutis potamophila is a species of freshwater sleeper native to China and Vietnam, is a commercially important fish species used in aquaculture in China. Demonstrating a sexually dimorphic growth pattern where the male grows quicker and larger than the female, this species can reach a length of 11.5 cm (4.5 in) in standard length.

Sex reversal is a biological process whereby the pathway directed towards the already determined-sex fate is flipped towards the opposite sex, creating a discordance between the primary sex fate and the sex phenotype expressed. The process of sex reversal occurs during embryonic development or before gonad differentiation. In GSD species sex reversal means that the sexual phenotype is discordant with the genetic/chromosomal sex. In TSD species sex reversal means that the temperature/conditions that usually trigger the differentiation towards one sexual phenotype are producing the opposite sexual phenotype.

CKLF-like MARVEL transmembrane domain-containing 5 (CMTM5), previously termed chemokine-like factor superfamily 5, designates any one of the six protein isoforms encoded by six different alternative splices of its gene, CMTM5; CMTM5-v1 is the most studied of these isoforms. The CMTM5 gene is located in band 11.2 on the long arm of chromosome 14.

<span class="mw-page-title-main">Evolution of sex-determining mechanisms</span>

The evolution of sex-determining mechanisms, characterized by the evolutionary transition to genetic sex determination or temperature-dependent sex determination from the opposite mechanism, has frequently and readily occurred among multiple taxa across a transitionary continuum.

References

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  4. ↑ Chen, Song-Lin; Tian, Yong-Sheng; Yang, Jing-Feng; Shao, Chang-Wei; Ji, Xiang-Shan; Zhai, Jie-Ming; Liao, Xiao-Lin; Zhuang, Zhi-Meng; Su, Peng-Zhi; Xu, Jian-Yong; Sha, Zhen-Xia; Wu, Peng-Fei; Wang, Na (April 2009). "Artificial Gynogenesis and Sex Determination in Half-Smooth Tongue Sole (Cynoglossus semilaevis)". Marine Biotechnology. 11 (2): 243–251. doi:10.1007/s10126-008-9139-0. ISSN   1436-2228. PMID   18779997. S2CID   24780167.
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  6. ↑ Dong, Zhongdian; Zhang, Ning; Liu, Yang; Xu, Wenteng; Cui, Zhongkai; Shao, Changwei; Chen, Songlin (January 2019). "Expression analysis and characterization of zglp1 in the Chinese tongue sole (Cynoglossus semilaevis)". Gene. 683: 72–79. doi:10.1016/j.gene.2018.10.003. PMID   30312653. S2CID   52975569.
  7. 1 2 Liu, Jinxiang; Liu, Xiaobing; Jin, Chaofan; Du, Xinxin; He, Yan; Zhang, Quanqi (29 May 2019). "Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis". Frontiers in Genetics. 10: 522. doi: 10.3389/fgene.2019.00522 . ISSN   1664-8021. PMC   6548826 . PMID   31191622.
  8. ↑ Zhu, Ying; Hu, Qiaomu; Xu, Wenteng; Li, Hailong; Guo, Hua; Meng, Liang; Wei, Min; Lu, Sheng; Shao, Changwei; Wang, Na; Yang, Guanpin; Chen, Songlin (10 May 2017). Liu, Chunming (ed.). "Identification and analysis of the β-catenin1 gene in half-smooth tongue sole (Cynoglossus semilaevis)". PLOS ONE. 12 (5): e0176122. Bibcode:2017PLoSO..1276122Z. doi: 10.1371/journal.pone.0176122 . ISSN   1932-6203. PMC   5425175 . PMID   28489928.
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  10. 1 2 Jiang, Li; Li, Hengde (1 February 2017). "Single Locus Maintains Large Variation of Sex Reversal in Half-Smooth Tongue Sole ( Cynoglossus semilaevis )". G3 Genes|Genomes|Genetics. 7 (2): 583–589. doi:10.1534/g3.116.036822. ISSN   2160-1836. PMC   5295603 . PMID   28007836.
  11. 1 2 3 4 5 6 Wang, Qian; Liu, Kaiqiang; Feng, Bo; Zhang, Zhihua; Wang, Renkai; Tang, Lili; Li, Wensheng; Li, Qiye; Piferrer, Francesc; Shao, Changwei (22 November 2019). "Transcriptome of Gonads From High Temperature Induced Sex Reversal During Sex Determination and Differentiation in Chinese Tongue Sole, Cynoglossus semilaevis". Frontiers in Genetics. 10: 1128. doi: 10.3389/fgene.2019.01128 . ISSN   1664-8021. PMC   6882949 . PMID   31824559.
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