Shubo Jin
Chao Bian
Jie Ma3†
Hongtuo Fu- 1Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, China
- 2Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, BGI, Shenzhen, China
- 3Department of Fish and Wildlife Resources, University of Idaho, Moscow, ID, United States
- 4Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, China
Editorial on the Research Topic
Sex Determination and Developmental Mechanism of Crustaceans and Shellfish
Introduction
Culture of crustacean and shellfish species produce huge economic benefits (1). Sex-determination and reproduction are complex mechanisms in crustacean and shellfish species. Many crustaceans and shellfish show significant growth differences between male and female individuals, including Macrobrachium nipponense (2), Macrobrachium resenbergii (3), and Eriocheir sinensis (4). Thus, single-sex production may have dramatic economic benefits. In addition, the process of gonad maturation has a great effect on the sustainable development of aquatic animals. Slow gonad development will extend the breeding cycle, while rapid gonad development will result in the inbreeding between the new-born animals (5). Thus, the mechanisms of sex-determination and reproduction are urgently needed to be fully understood, in order to establish the technique to produce a single-sex population and regulate the gonad development in crustaceans and shellfish. The aims and objective of this Research Topic is to present an overview of the fundamental discoveries in the field of sex-determination and reproduction in crustaceans and shellfish species. The article contents of this Research Topic are shown in Figure 1.
Figure 1 The main article contents of this Research Topic.
Analysis of Reproduction-Related Genes in M. nipponense
A total of three reproduction-related genes were analysed in M. nipponense by using qPCR and RNAi analysis, including Cathepsin L (CL), Legumain-like protease (Lel) and Ftz-f1. CL and Lel were predicted to participate in the process of ovarian development in M. nipponense through the transcriptome profiling analysis of five ovarian stages (6). qPCR analysis revealed that both of Mn-Lel and Mn-CL were specifically highly expressed in the hepatopancreas and ovaries of female prawns in different mature tissues. Mn-Lel showed significantly high expressions after metamorphosis during different development stages, while Mn-CL expression reached the peak before ovarian maturation in both hepatopancreas and ovary during the different ovarian developmental stages. The expressions of Mn-Lel were significantly decreased at day 9 and day 17 after the injection of Mn-Lel dsRNA in both hepatopancreas and ovary, and changes in the gonad somatic index (GSI) confirmed the inhibitory effects of Mn-Lel dsRNA on ovary maturation (Jiang et al.). The expressions of Mn-CL were significantly decreased at day 9 and day 17 after the injection of Mn-CL dsRNA in ovary, and the expression of Mn-vitellogenin were also decreased with the decrease of Mn-CL, indicating cathepsin L has positively regulatory roles together with that of vitellogenin in M. nipponense. Changes in the GSI also confirmed the inhibitory effects of Mn-CL dsRNA on ovary maturation (Jiang et al.). These results indicated that both cathepsin L and Legumain-like protease have positively regulatory roles on ovary maturation in M. nipponense.
Mn-Ftz-f1 expression showed the highest expression level in ovary, based on the PCR analysis in different mature tissues, and Mn-Ftz-f1 expression reached the peak at the larval developmental stage 5 (L5) during the different developmental stages, followed by the post-larval developmental stage 5 (PL5). RNAi analysis revealed that the injection of Mn-Ftz-f1 dsRNA significantly decreases the expression of Mn-Ftz-f1 in M. nipponense, and the expressions of the vitellogenin, Spook, and Phantom genes were decreased with the decrease of Mn-Ftz-f1 in M. nipponense, indicating that Ftz-f1 positively regulated the expressions of these genes in M. nipponense. In addition, the molting frequency and ovulation number of M. nipponense decreased significantly after the injection of Mn-Ftz-f1 dsRNA, demonstrating that Mn-Ftz-f1 has positive effects on the process of molting and ovulation (Yuan et al.).
Identification of Sex-Determination-Related Genes From M. rosenbergii
In vivo knockdown of the expressions of Dmrt11E by RNAi at the post-larva stage in male M. rosenbergii results in a complete and functional sex reversal and production of an all-male monosex population. The sex-determination-related genes were further investigated from M. rosenbergii through performing the transcriptome profiling analysis after the injection of Dmrt11E dsRNA. Transformer, fruitless, feminization, insulin-like androgenic gland gene, and Dmrt gene family were primarily identified to be regulated by the changes of Dmrt11E, which were predicted to be involved in the mechanism of sex-determination in M. rosenbergii (Xu et al.).
Identification of the Functions of Reproduction-Related Genes in E. sinensis
The potential functions of the red pigment concentrating hormone (RPCH) and the pigment dispersing hormone (PDH) on the ovarian development were investigated in E. sinensis. qPCR analysis identified that Es-RPCH and Es-β-PDH transcripts were distributed in the brain and eyestalks. The in vivo injection of Es-RPCH and Es-β-PDH peptides into the female E. sinensis results in the significant decrease of GSI and mean oocyte diameter, as well as the expression of vitellogenin, cdc2 kinase, cyclin B, 5-HT-R and retinoid-X receptor mRNA, indicating that Es-RPCH and Es-β-PDH have the inductive effects on the oocyte meiotic maturation in E. sinensis (Wei et al.).
Identification of the Effect of Estradiol on Strongylocentrotus intermedius
A sex-associated single nucleotide polymorphism (SNP) was identified in S. intermedius, which was located within spata4. Knockdown the expressions of spata4 by RNAi results in the significant changes of the other well studied testis differentiation-related genes and germ cell marker genes, including Dmrt1, SoxE, Foxl2, Hsd17b8, Boule and Nanos1. In addition, the differentially expressed genes affected by estradiol were identified through performing the transcriptome profiling analysis after a 58-day feeding experiment, which may be involved in the process of testis differentiation, ovary differentiation, and estrogen metabolism in S. intermedius (Han et al.).
Identification of Metabolites Affecting the Ovarian Development of Scylla paramamosain
A total of 101 differentially expressed metabolites were identified after the treatment with juvenile hormone III (JH III), methyl farnesoate (MF), farnesoic acid (FA) and methoprene (Met), enriched in 47 metabolic pathways, providing a comprehensive insight to understand the process of ovarian development in S. paramamosain. MF, JH III and Met played an extensive role in lipid accumulation, while FA has opposite effects (Fu et al.).
Author Contributions
SJ wrote the editorial. CB, JM, and PW summarize the findings of the articles in this Research Topic. PX and HF supervised and revised the editorial. All authors contributed to the article and approved the submitted version.
Funding
This research was supported by grants from the National Key R&D Program of China (2018YFD0900201); Central Public-interest Scientific Institution Basal Research Fund CAFS (2021JBFM02; 2020TD36); Jiangsu Agricultural Industry Technology System; the China Agriculture Research System-48 (CARS-48); the New cultivar breeding Major Project of Jiangsu province (PZCZ201745).
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
Thank you for the Jiangsu Province Platform for the Conservation and Utilization of Agricultural Germplasm.
References
1. Zhang XL, Cui LF, Li SM, Liu XZ, Han X, Jiang KY, et al. Bureau of Fisheries, Ministry of Agriculture, P.R.C. Fisheries Economic Statistics. In: China Fishery Yearbook, vol. 24. . Beijing China: Agricultural Press (2020).
2. Fu HT, Jiang SF, Xiong YW. Current Status and Prospects of Farming the Giant River Prawn (Macrobrachium Rosenbergii) and the Oriental River Prawn (Macrobrachium Nipponense) in China. Aquac Res (2012) 43:993–8. doi: 10.1111/j.1365-2109.2011.03085.x
3. Rosen O, Manor R, Weil S, Gafni O, Linial A, Aflalo ED, et al. A Sexual Shift Induced by Silencing of a Single Insulin-Like Gene in Crayfish: Ovarian Upregulation and Testicular Degeneration. PloS One (2010) 5:e15281. doi: 10.1371/journal.pone.0015281
4. Li J, Tian YX, Li XH, Zuo JM, Zhao RH, Sun JS. Insulin-Like Signaling Promotes Limb Regeneration in the Chinese Mitten Crab (Eriocheir Sinensis). Fish Shellfish Immu (2022) 122:268–75. doi: 10.1016/j.fsi.2022.02.007
5. Jin SB, Hu YN, Fu HT, Jiang SF, Xiong YW, Qiao H, et al. Identification and Characterization of the Succinate Dehydrogenase Complex Iron Sulfur Subunit B Gene in the Oriental River Prawn. Macrobrachium nipponense Front Genet (2021) 12:698318. doi: 10.3389/fgene.2021.698318
Keywords: sex-determination, development, crustacean, shellfish, genes
Citation: Jin S, Bian C, Ma J, Wang P, Xu P and Fu H (2022) Editorial: Sex Determination and Developmental Mechanism of Crustacean and Shellfish. Front. Endocrinol. 13:940144. doi: 10.3389/fendo.2022.940144
Received: 10 May 2022; Accepted: 23 May 2022;
Published: 28 June 2022.
Edited and reviewed by:
Ralf Jockers, Université de Paris, FranceCopyright © 2022 Jin, Bian, Ma, Wang, Xu and Fu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Hongtuo Fu, fuht@ffrc.cn; Pao Xu, xupao@ffrc.cn
†These authors have contributed equally to this work