Abstract
Mesocentrotus nudus is an economically important mariculture species. Identification of sex-related markers and candidate genes has potential implications for sex-control breeding of Mesocentrotus nudus. The aim of this study was to identify the molecular markers and genes associated with the sex of M. nudus. Initial GWAS analysis based on 80 individuals genotyped by using GBS identified 22 sex-related SNPs located on 9 GBS tags. Further targeted sequencing in another population of 124 individuals confirmed that 7 SNPs located on 7 GBS tags displayed complete associations with sex, suggesting a ZW/ZZ sex-determination system in M. nudus. Besides, genome and transcriptome annotations presented that the heat shock protein 75 kDa, mitochondrial (trap1), and protein furry homolog-like (fryl) may be important candidate genes involved in sex determination and differentiation in M. nudus. However, further studies are needed to elucidate the functions of these genes. Overall, the current results not only provide molecular markers that may contribute to the sex-control breeding for M. nudus, but also provide new insights to understand the regulatory mechanism of sea urchin sex.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agatsuma Y (2020) Mesocentrotus nudus. Dev. Aquacult. Fish Sci 43:627–641. https://doi.org/10.1016/B978-0-12-819570-3.00034-2
Aulchenko YS, Ripke S, Isaacs A, van Duijn CM (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23:1294–1296. https://doi.org/10.1093/bioinformatics/btm108
Baqri RM, Pietron AV, Gokhale RH, Turner BA, Kaguni LS, Shingleton AW et al (2014) Mitochondrial chaperone TRAP1 activates the mitochondrial UPR and extends healthspan in Drosophila. Mech Ageing Dev 141–142:35–45. https://doi.org/10.1016/j.mad.2014.09.002
Cui Z, Hui M, Liu Y, Song C, Li X, Li Y et al (2015) High-density linkage mapping aided by transcriptomics documents ZW sex determination system in the Chinese mitten crab Eriocheir sinensis. Heredity 115:206–215. https://doi.org/10.1038/hdy.2015.26
Cui Z, Zhang J, Sun Z, Liu B, Han Y, Zhao C et al (2022) Testis-specific expression pattern of dmrt1 and its putative regulatory region in the sea urchin (Mesocentrotus nudus). Comp Biochem Physiol B-Biochem Mol Biol 257:110668. https://doi.org/10.1016/j.cbpb.2021.110668
Cui Z, Zhang J, Sun Z, Liu B, Zhao C, Chang Y (2021) Identification of sex-specific markers through 2b-RAD sequencing in the sea urchin (Mesocentrotus nudus). Front Genet 1433. https://doi.org/10.3389/fgene.2021.717538
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Emrani H, Masoudi A, Vaez Torshizi R, Ehsani A (2020) Genome-wide association study of shank length and diameter at different developmental stages in chicken F2 resource population. Anim Genet 51:722–730. https://doi.org/10.1111/age.12981
Eno CC, Bottger SA, Walker CW (2009) Methods for karyotyping and for localization of developmentally relevant genes on the chromosomes of the purple sea urchin, Strongylocentrotus purpuratus. Biol Bull 217:306–312. https://doi.org/10.1086/BBLv217n3p306
Felts SJ, Owen BA, Nguyen P, Trepel J, Donner DB, Toft DO (2000) The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 275:3305–3312. https://doi.org/10.1074/jbc.275.5.3305
Harris LG, Eddy SD (2015) Sea urchin ecology and biology. In: Aquaculture E (ed) N P Brown & S D Eddy. John Wiley & Sons, Hoboken, NJ, pp 3–24
Hayette S, Cornillet-Lefebvre P, Tigaud I, Struski S, Forissier S, Berchet A et al (2005) AF4p12, a human homologue to the furry gene of Drosophila, as a novel MLL fusion partner. Cancer Res 65:6521–6525. https://doi.org/10.1158/0008-5472
Kafkas S, Khodaeiaminjan M, Güney M, Kafkas E (2015) Identification of sex-linked SNP markers using RAD sequencing suggests ZW/ZZ sex determination in Pistacia vera L. BMC Genomics 16:1–11. https://doi.org/10.1186/s12864-015-1326-6
Koopman P (2001) The genetics and biology of vertebrate sex determination. Cell 105:843–847. https://doi.org/10.1016/S0092-8674(01)00408-1
Lin H, Zhou Z, Zhao J, Zhou T, Bai H, Ke Q et al (2021) Genome-wide association study identifies genomic loci of sex determination and gonadosomatic index traits in large yellow croaker (Larimichthys crocea). Mar Biotechnol 23:127–139. https://doi.org/10.1007/s10126-020-10007-2
Liu C, Lin Q, Yi G, Liang Y, Xing Y, Tao X (2007) Characterization and antitumor activity of a polysaccharide from Strongylocentrotus nudus eggs. Carbohydr Polym 67:313–318. https://doi.org/10.1016/j.carbpol.2006.05.024
Luo H, Xiao J, Jiang Y, Ke Y, Ke C, Cai M (2021) Mapping and marker identification for sex-determining in the Pacific abalone. Haliotis Discus Hannai Ino Aquaculture 530:735810. https://doi.org/10.1016/j.aquaculture.2020.735810
McBride SC, Price RJ, Tom PD, Lawrence JM, Lawrence AL (2004) Comparison of gonad quality factors: color, hardness and resilience, of Strongylocentrotus franciscanus between sea urchins fed prepared feed or algal diets and sea urchins harvested from the Northern California fishery. Aquaculture 233:405–422. https://doi.org/10.1016/j.aquaculture.2003.10.014
Mi X, Wei Z, Zhou Z, Liu X (2014) Identification and profiling of sex-biased microRNAs from sea urchin Strongylocentrotus nudus gonad by Solexa deep sequencing. Comp Biochem Physiol D-Genomics Proteomics 10:1–8. https://doi.org/10.1016/j.cbd.2014.01.001
Murata Y, Sata NU, Yokoyama M, Kuwahara R, Kaneniwa M, Oohara I (2001) Determination of a novel bitter amino acid, pulcherrimine, in the gonad of the green sea urchin Hemicentrotus pulcherrimus. Fish Sci 67:341–345. https://doi.org/10.1046/j.1444-2906.2001.00234.x
R Core Team (2018) R: a language and environment for statistical computing. Austria, Vienna
Sato M, Hosoya S, Yoshikawa S, Ohki S, Kobayashi Y, Itou T et al (2019) A highly flexible and repeatable genotyping method for aquaculture studies based on target amplicon sequencing using next-generation sequencing technology. Sci Rep 9:1–9. https://doi.org/10.1038/s41598-019-43336-x
Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC et al (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952. https://doi.org/10.1126/science.1133609
Sun Z, Zhang J, Zhang W, Chang Y (2019) Gonadal transcriptomic analysis and identification of candidate sex-related genes in Mesocentrotus nudus. Gene 698:72–81. https://doi.org/10.1016/j.gene.2019.02.054
Unal E, Bucklin A, Lenz PH, Towle DW (2013) Gene expression of the marine copepod Calanus finmarchicus: responses to small-scale environmental variation in the Gulf of Maine (NW Atlantic Ocean). J Exp Mar Biol Ecol 446:76–85. https://doi.org/10.1016/j.jembe.2013.04.020
Wang M, Li L, Lin H, Zhou Z, Liu B, Zhong J et al (2022) Genome-wide association study identifies genomic loci of sex determination, gonadal weight and gonadosomatic index traits in Takifugu bimaculatus. Aquaculture 546:737389. https://doi.org/10.1016/j.aquaculture.2021.737389
Wang Q, Liu Y, Yan L, Chen L, Li B (2021a) Genome-wide SNP discovery and population genetic analysis of Mesocentrotus nudus in China Seas. Front Genet 1493. https://doi.org/10.3389/fgene.2021.717764
Wang Y, Yu Y, Li S, Zhang X, Li F (2021b) Analysis of a sex-biased sequence in sex determination region and exploitation of a fast sex detection method in Litopenaeus vannamei. Aquaculture 543:736922. https://doi.org/10.1016/j.aquaculture.2021.736922
Wei J, Cong J, Sun Z, Song J, Zhao C, Chang Y (2021) A rapid and reliable method for genetic sex identification in sea cucumber Apostichopus Japonicus. Aquaculture 737021. https://doi.org/10.1016/j.aquaculture.2021.737021
Xiao J, Zou Y, Xiao S, Chen J, Wang Z, Wang Y et al (2020) Development of a PCR-based genetic sex identification method in spinyhead croaker (Collichthys lucidus). Aquaculture 522:735130. https://doi.org/10.1016/j.aquaculture.2020.735130
Yu Y, Zhang X, Yuan J, Wang Q, Li S, Huang H et al (2017) Identification of sex-determining loci in pacific white shrimp Litopeneaus vannamei using linkage and association analysis. Mar Biotechnol 19:277–286. https://doi.org/10.1007/s10126-017-9749-5
Acknowledgements
This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23050304), the International Science Partnership Program of the Chinese Academy of Sciences (133137KYSB20200002), and the Yantai Science and Technology Planning Project (2020MSGY074).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics Approval
Each of the procedures that were used to handle and treat the Mesocentrotus nudus during this study was approved by the Key Laboratory of Coastal Biology and Biological Resources Utilization, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences prior to the initiation of the study, and the Animal Management Regulations, revised on March 1, 2017, No. 676.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, Q., Liu, Y., Wang, Y. et al. GWAS Reveal Novel Sex-Related Markers and Candidate Genes in Sea Urchin Mesocentrotus nudus. Mar Biotechnol 24, 32–39 (2022). https://doi.org/10.1007/s10126-021-10084-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-021-10084-x