Sex steroids and steroidogenesis-related genes in the sea cucumber, Holothuria scabra and their potential role in gonad maturation

Tipsuda Thongbuakaew; Saowaros Suwansa-ard; Arada Chaiyamoon; Scott F Cummins; Prasert Sobhon

doi:10.1038/s41598-021-81917-x

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Sex steroids and steroidogenesis-related genes in the sea cucumber, Holothuria scabra and their potential role in gonad maturation

Journal article

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Sex steroids and steroidogenesis-related genes in the sea cucumber, Holothuria scabra and their potential role in gonad maturation

Tipsuda Thongbuakaew, Saowaros Suwansa-ard, Arada Chaiyamoon, Scott F Cummins and Prasert Sobhon

Scientific Reports, Vol.11, pp.1-16

2021

DOI: https://doi.org/10.1038/s41598-021-81917-x

PMCID: PMC7838161

PMID: 33500499

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Abstract

Estrogens

Sex

Mass spectroscopy

Liquid chromatography

Steroidogenic acute regulatory protein

Ovaries

Vitellogenin

Gene expression

Estradiol

Population decline

Testosterone

Androgens

Developmental stages

Evolutionary conservation

Steroidogenesis

Progesterone

Testes

Comparative analysis

Invertebrates

Species

Steroid hormones

The sea cucumber Holothuria scabra is an economically valuable marine species which is distributed throughout the Asia–Pacific region. With the natural population declining due to over fishing, aquaculture of this species is deemed necessary. Hence, it is essential to understand the mechanisms regulating the reproduction in order to increase their populations. Sex steroids, including estrogens, androgens and progestogens, play an important role in reproduction in most vertebrates and several invertebrates. It has been proposed that sea cucumbers have the same sex steroids as vertebrates but the steroidogenic pathway in the sea cucumbers is still unclear. In this study, we demonstrated by using liquid chromatography-tandem mass spectrometry (LC–MS/MS) that sex steroids (estradiol, progesterone, and testosterone) were present in H. scabra neural and gonadal tissues. In silico searches of available sea cucumber transcriptome data identified 26 steroidogenesis-related genes. Comparative analysis of encoded proteins for the steroidogenic acute regulatory protein (HscStAR), CYP P450 10, 17 and 3A (HscCYP10, HscCYP17, HscCYP3A) and hydroxysteroid dehydrogenases (Hsc3β-HSD, Hsc17β-HSD) with other species was performed to confirm their evolutionary conservation. Gene expression analyses revealed widespread tissue expression. Real-time PCR analysis revealed that HscStAR, HscCYP10, Hsc3β-HSD, and Hsc17β-HSD gene expressions were similar to those in ovaries and testes, which increased during the gonad maturation. HscCYP17 mRNA was increased during ovarian development and its expression declined at late stages in females but continued high level in males. The expression of the HscCYP3A was high at the early stages of ovarian development, but not at other later stages in ovaries, however it remained low in testes. Moreover, a role for steroids in reproduction was confirmed following the effect of sex steroids on vitellogenin (Vtg) expression in ovary explant culture, showing upregulation of Vtg level. Collectively, this study has confirmed the existence of steroids in an echinoderm, as well as characterizing key genes associated with the steroidogenic pathway. We propose that sex steroids might also be associated with the reproduction of H. scabra, and the identification of biosynthetic genes enables future functional studies to be performed.

Details

Title: Sex steroids and steroidogenesis-related genes in the sea cucumber, Holothuria scabra and their potential role in gonad maturation
Authors: Tipsuda Thongbuakaew (Author) - Walailak University
Saowaros Suwansa-ard (Author) - University of the Sunshine Coast, Queensland, GeneCology Research Centre - Legacy
Arada Chaiyamoon (Author) - Khon Kaen University
Scott F Cummins (Author) - University of the Sunshine Coast, Queensland, GeneCology Research Centre - Legacy
Prasert Sobhon (Author) - Mahidol University
Publication details: Scientific Reports, Vol.11, pp.1-16
Publisher: Nature Publishing Group
Date published: 2021
DOI: 10.1038/s41598-021-81917-x
ISSN: 2045-2322
PMID: 33500499; PMC7838161
Copyright note: Copyright (c) 2021 The Authors. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Organisation Unit: School of Science and Engineering - Legacy; University of the Sunshine Coast, Queensland; School of Science, Technology and Engineering; Centre for Bioinnovation
Language: English
Record Identifier: 99506008002621
Output Type: Journal article

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