Abstract
The development of a biomarker for rapid detection of intersex is desirable to researchers and fisheries managers alike. The first step is to identify a marker that has a dimorphic expression pattern. With a focus on sex-specific genes, we assessed the use of vitellogenin (vtg), forkhead box L2 (foxl2) and doublesex and mab-3-related transcription factor 1 (dmrt1) as molecular biomarkers for the identification of gender in shovelnose sturgeon (Scaphirhynchus platorynchus), a species known to have intersex individuals. A total of 61 shovelnose sturgeons were sampled from the Wabash River, Indiana, in April 2008. Results from our study indicate that least 7.5% of the non-females had testicular oocytes. Expression level of liver vtg was not higher in females than males, nor was gonad dmrt1 expression found to be higher in males. Only the expression of foxl2 was significantly greater in females and was found to be useful for identifying gender. Variation in expression levels of foxl2 in gonads of intersex fish limited its usefulness as a single biomarker for identifying this condition. Instead, the use of foxl2 to dmrt1 (foxl2 transcript abundance/dmrt1 transcript abundance) may be useful in the identification of intersex fish, as this ratio increased with increased feminization. We conclude that foxl2 can be used to identify sex, but not intersex sturgeon.
Similar content being viewed by others
References
Alam MA, Kobayashi Y, Horiguchi R, Hirai T, Nakamura M (2008) Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra. Gen Comp Endocrinol 157:75–85
An LH, Hu JY, Zhang ZB, Yang M (2006) Quantitative real-time RT-PCR for determination of vitellogenin mRNA in so-iuy mullet (Mugil soiuy). Anal Bioanal Chem 386:1995–2001
Baron D, Batista F, Chaffaux S, Cocquet J, Cotinot C, Cribiu E, De Baeree E, Guiguen Y, Jaubert F, Pailhoux E, Pannetier M, Vaiman D, Vigier B, Veitia R, Fellous M (2004a) Foxl2 gene and the development of the ovary: a story about goat, mouse, fish and woman. In: Symposium on reproduction in vetebrates and man held in honor of Charles Thibault. EDP Sciences, Paris, pp 377–382
Baron D, Cocquet J, Xia XH, Fellous M, Guiguen Y, Veitia RA (2004b) An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. J Mol Endocrinol 33:705–715
Baron D, Houlgatte R, Fostier A, Guiguen Y (2005) Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 73:959–966
Baron D, Houlgatte R, Fostier A, Guiguen Y (2008) Expression profiling of candidate genes during ovary-to-testis trans-differentiation in rainbow trout masculinized by androgens. Gen Comp Endocrinol 156:369–378
Bjorkblom C, Salste L, Katsiadaki I, Wiklund T, Kronberg L (2008) Detection of estrogenic activity in municipal wastewater effluent using primary cell cultures from three-spined stickleback and chemical analysis. Chemosphere 73:1064–1070
Blazer VS, Iwanowicz LR, Iwanowicz DD, Smith DR, Young JA, Hedrick JD, Foster SW, Reeser SJ (2007) Intersex (testicular oocytes) in smallmouth bass from the Potomac River and selected nearby drainages. J Aquat Anim Health 19:242–253
Bruch RM, Dick TA, Choudhury A (2001) A field guide for the identification of stages of gonad development in lake sturgeon (Acipenser fulvescens: Rafinesque): with note on lake sturgeon reproductive biology and management implications. Sturgeon for Tomorrow, Fond du Lac, WI, p 38
Caprioli R, Costa C, Cataldi E, Boglione C, Cataudella S (2007) First record of female germ cells in the testis of a wild Mediterranean northern bluefin tuna Thunnus thynnus L. 1758. J Fish Biol 71:620–622
Colombo RE, Garvey JE, Jackson ND, Brooks R, Herzog DP, Hrabik RA, Spier TW (2007a) Harvest of Mississippi River sturgeon drives abundance and reproductive success: a harbinger of collapse? J Appl Ichthyol 23:444–451
Colombo RE, Garvey JE, Wills PS (2007b) Gonadal development and sex-specific demographics of the shovelnose sturgeon in the Middle Mississippi River. J Appl Ichthyol 23:420–427
Craves JAM (2008) Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42:565–586
Ferguson-Smith M (2007) The evolution of sex chromosomes and sex determination in vertebrates and the key role of DMRT1. Sex Dev 1:2–11
Huang X, Guo YQ, Shui Y, Gao S, Yu HS, Cheng HH, Zhou RJ (2005) Multiple alternative splicing and differential expression of dmrt1 during gonad transformation of the rice field eel. Biol Reprod 73:1017–1024
Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y (2008) Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78:333–341
Jackson ND, Garvey JE, Colombo RE (2007) Comparing aging precision of calcified structures in shovelnose sturgeon. J Appl Ichthyol 23:525–528
Jessica D, Robert M, Frederic S, Arnaud B, Delphine L, Jean-Pierre T, Patrick K (2007) Do sewage treatment plant discharges substantially impair fish reproduction in polluted rivers? Sci Total Environ 372:497–514
Jorgensen A, Morthorst JE, Andersen O, Rasmussen LJ, Bjerregaard P (2008) Expression profiles for six zebrafish genes during gonadal sex differentiation. Reprod Biol Endocrinol 6:1–12
Kavanagh RJ, Balch GC, Kiparissis Y, Niimi AJ, Sherry J, Tinson C, Metcalfe CD (2004) Endocrine disruption and altered gonadal development in white perch (Morone americana) from the lower Great Lakes region. Environ Health Perspect 112:898–902
Korner O, Vermeirssen ELM, Burkhardt-Holm P (2005) Intersex in feral brown trout from Swiss midland rivers. J Fish Biol 67:1734–1740
Liu ZH, Wul FR, Jiao BW, Zhang XY, Hu CJ, Huang BF, Zhou LY, Huang XG, Wang ZJ, Zhang YG, Nagahama Y, Cheng CHK, Wang DS (2007) Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation. J Endocrinol 194:223–241
Ludwig A, Belfiore NM, Pitra C, Svirsky V, Jenneckens I (2001) Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics 158:1203–1215
Matsuda M, Shinomiya A, Kinoshita M, Suzuki A, Kobayashi T, Paul-Prasanth B, Lau EL, Hamaguchi S, Sakaizumi M, Nagahama Y (2007) DMY gene induces male development in genetically female (XX) medaka fish. Proc Natl Acad Sci USA 104:3865–3870
Morrow JA, Kirk JP, Killgore KJ, George SG (1998) Age, growth and mortality of shovelnose sturgeon in the lower Mississippi River. North Am J Fish Manag 18:725–730
Nolan M, Jobling S, Brighty G, Sumpter JP, Tyler CR (2001) A histological description of intersexuality in the roach. J Fish Biol 58:160–176
Penman DJ, Piferrer F (2008) Fish gonadogenesis. Part I: genetic and environmental mechanisms of sex determination. Rev Fish Sci 16:16–34
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007
Tanaka H, Baba T (2005) Gene expression in spermiogenesis. Cell Mol Life Sci 62:344–354
Tarrant H, Mousakitis G, Wylde S, Tattersall N, Lyons A, Maloney M, Llewellyn N (2008) Raised plasma vitellogenin in male wild brown trout (Salmo trutta) near a wastewater treatment plant in Ireland. Environ Toxicol Chem 27:1773–1779
Vajda AM, Barber LB, Gray JL, Lopez EM, Woodling JD, Norris DO (2008) Reproductive disruption in fish downstream from an estrogenic wastewater effluent. Environ Sci Technol 42:3407–3414
Van den Belt K, Verheyen R, Witters H (2003) Comparison of vitellogenin responses in zebrafish and rainbow trout following exposure to environmental estrogens. Ecotoxicol Environ Saf 56:271–281
Vizziano D, Randuineau G, Baron D, Cauty C, Guiguen Y (2007) Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev Dyn 236:2198–2206
Vizziano-Cantonnet D, Baron D, Mahe S, Cauty C, Fostier A, Guiguen Y (2008) Estrogen treatment up-regulates female genes but does not suppress all early testicular markers during rainbow trout male-to-female gonadal transdifferentiation. J Mol Endocrinol 41:277–288
Woodling JD, Lopez EM, Maldonado TA, Norris DO, Vajda AM (2006) Intersex and other reproductive disruption of fish in wastewater effluent dominated Colorado streams. Comp Biochem Physiol C 144:10–15
Wu GC, Tomy S, Nakamura M, Chang CF (2008) Dual roles of cyp19a1a in gonadal sex differentiation and development in the protandrous black borgy, Acanthopagrus schlegeli. Biol Reprod 79:1111–1120
Xia W, Zhou L, Yao B, Li CJ, Gui HF (2007) Differential and spermatogenic cell-specific expression of DMRT1 during sex reversal in protogynous hermaphroditic groupers. Mol Cell Endocrinol 263:156–172
Acknowledgments
The authors would like to thank everyone that participated in the collection and processing of the fish used in this study, especially the staff of the Indiana Department of Natural Resources and Animal Disease and Diagnosis Laboratory of Purdue University for donating the tissues used in this study. We are also thankful to all of the graduate and undergraduate students that helped in the collection of data and tissues.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Amberg, J.J., Goforth, R., Stefanavage, T. et al. Sexually dimorphic gene expression in the gonad and liver of shovelnose sturgeon (Scaphirhynchus platorynchus). Fish Physiol Biochem 36, 923–932 (2010). https://doi.org/10.1007/s10695-009-9369-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-009-9369-8