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Molecular mechanisms underlying sex change in hermaphroditic groupers

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Abstract

Groupers are widely distributed throughout the tropical and subtropical waters of the world and are regarded as a favourite marine food fish. However, their large-scale aquaculture has been hindered by the rarity of natural males. Being protogynous hermaphrodites, groupers have been considered as study model for development and reproduction, especially for sex determination or sex differentiation, owing to the advantage that grouper gonad development undergoes transition from ovary to intersexual gonad and then to testis, and primordial germ cells and different stages of gametic cells during oogenesis and spermatogenesis are synchronously observed in the transitional gonads. Recently, a series of genes related to the reproduction regulation or sex differentiation have been identified in the groupers, mainly by researchers in China. One important finding was that the grouper gene, doublesex/male abnormal 3-related transcription factor 1 (DMRT1), is not only differentially expressed in gonads at different stages, but that it is also restricted to specific stages and specific cells of spermatogenesis. Grouper DMRT1 protein exists only in spermatogonia, primary spermatocytes and secondary spermatocytes, but not in the supporting Sertoli cells. Moreover, no introns were found in the grouper DMRT1, and no duplicated DMRT1 genes were detected. The finding implies that the intronless DMRT1 that is able to undergo rapid transcriptional turnover might be a significant gene for stimulating spermatogenesis in the protogynous hermaphroditic gonad. Additionally, we have found that grouper expression of sex-determining region Y-related high-mobility group-box gene 3 (SOX3) is a significant time point for enterable gametogenesis of primordial germ cells, because SOX3 is obviously expressed and localized in primordial germ cells. As SOX3 continues to express, the SOX3-positive primordial germ cells develop toward oogonia and then oocytes, whereas, when SOX3 expression is ceased, the SOX3-positive primordial germ cells develop toward spermatogonia. Therefore, we suggest that SOX3, as a transcription factor, might have more important roles in oogenesis than in spermatogenesis. Based on the findings, a hypothetic molecular mechanism underlying sex change is proposed in the hermaphroditic groupers, and some candidate genes related to the grouper sex change are also suggested for further research.

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Abbreviations

11-KT:

11-Keto-testosterone

AMH:

Anti-mullerian hormone

CN:

Chromatin nucleolus stage

DMRT1:

dsx and mab-3 related transcription factor 1

DMY:

The DM-domain gene on the Y chromosome

E2:

Oestradiol-17β

EcDmrt1 :

Epinephelus coioides dsx and mab-3 related transcription factor 1

EcSOX3 :

Epinephelus coioides Sry-related HMG-box gene 3

EcTSHβ :

Epinephelus coioides Thyroid-stimulating hormone β subunit

FOG2:

Friend of GATA

FSHβ:

Follicle-stimulating hormone β subunit

FTZ-F1 :

Fushi Tarazu factor-1

GATA4:

The zinc finger transcription factors GATA binding proteins 4

GH:

Growth hormone

GnRH-R1:

Gonadotropin-releasing hormone receptor

GTHα:

Gonadotropin α subunit

LHβ:

Luteinizing hormone β subunit

LV:

Lipid vesicle stage

MBP:

Myelin basic protein

MT:

17α-Methyltestosterone

NLTm:

Medial part of the lateral tuberal nucleus

NPOpc:

Parvocellular part of the parvocellular preoptic nucleus

NPY :

Neuropeptide Y

O:

Oogonia

OC2:

Ovary-specific C2 domain factor

P450arom:

Aromatase cytochrome P450

PACAP:

Pituitary adenylate cyclase activating polypeptide

PGC:

Primordial germ cells

PN:

Perinucleolus stage

POF:

Post-ovulatory follicle

PRL:

Prolactin

PVO:

Previtellogenic oocytes

RT-PCR:

Reverse transcription-polymerase chain reaction

SL:

Somatolactin

SMART:

Switching mechanism At 5′end of the RNA transcript

SPC I:

Spermatocytes I

SPC II:

Spermatocytes II

SPD:

Spermatids

SPG:

Spermatogonia

SPZ:

Spermatozoa

Sox3:

Sry-related HMG-box gene 3

T:

Testosterone

TL:

Total length

TP:

Testosterone propionate

TSHβ:

Thyroid-stimulating hormone β subunit

VO:

Vitellogenic oocyte

WT1:

Wilms tumor gene 1

YI:

Yolk granules I

YII:

Yolk granules II

YIII:

Yolk granules III

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Acknowledgements

This work was supported by grants from the National Major Basic Research Program (2004CB117401), the National 863 High Technology Research Program (grants No 2006AA09Z439), the National Natural Science Foundation of China (grant no. U0631007, 30470935) and Institute of Hydrobiology (075A01).

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  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Wuhan Center for Developmental Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Wuhan, 430072, China

    Li Zhou & Jian-Fang Gui

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  1. Li Zhou
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  2. Jian-Fang Gui
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Correspondence to Jian-Fang Gui.

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Zhou, L., Gui, JF. Molecular mechanisms underlying sex change in hermaphroditic groupers. Fish Physiol Biochem 36, 181–193 (2010). https://doi.org/10.1007/s10695-008-9219-0

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  • DOI: https://doi.org/10.1007/s10695-008-9219-0

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