Abstract
Dmrt1, a putative transcription factor with a DM-binding motif (called the DM domain), is generally considered to be exclusively expressed in testicular tissue, except in some teleost species where it has also been demonstrated to be expressed at the ovary. The aim of the present manuscript was to characterize the dmrt1 cDNA and analyze its expression pattern at different spermatogenetic stages in the pejerrey fish, Odontesthes bonariensis. The pejerrey dmrt1 (pjdmrt1), encodes for a 290 amino acid protein including the conserved DM and P/S domains. The sequence comparison of the pjdmrt1 revealed a high level of identity with different dmrt1 from other vertebrates and the phylogenetic analysis showed the existence of two main clades: one represented by the mammalian dmrt1 sequences and the second by dmrt1 sequences from teleost fishes. This pattern may represent the evolution of this molecule. In pejerrey fish, the expression of this gene was exclusively restricted to the testis at all spermatogenetic stages analyzed, and pjdmrt1 expression levels varied according spermatogenetic stages suggesting a role for dmrt1 in the adult testicular function.
This is a preview of subscription content, access via your institution.
Abbreviations
- Dmrt1:
-
(Doublesex Maleabnormal-3 Related Transcription factor-1)
References
Billard R, Breton B, Fostier A, Jalabert B, Weil C (1978) Endocrine control of the teleost reproductive cycle and its relation to external factors: salmonid and cyprinid models. In: Gaillard PJ, Boer HH (eds) Comparative endocrinology. Elsevier/North-Holland, Amsterdam, pp 37–47
Brunner B, Hornung U, Shan Z, Nanda I, Kondo M, Zend-Ajusch E, Haff T, Ropers H, Shima A, Schmid M, Kalsheuer V, Shartl M (2001) Genomic organization and expression of the doublesex-related gene cluster in vertebrates and putative regulatory regions for dmrt1. Genomics 77:8–17
Chen WJ, Ortí G, Meyer A (2004) Novel evolutionary relationship among four fish model systems. Trends Genet 20:424–431
De Grandi A, Calvari V, Bertini V, Bulfone A, Peverali G, Camerino G, Borsani G, Guioli S (2000) The expression pattern of a mouse doublesex-related gene is consistent with a role in gonadal differentiation. Mech Dev 90:323–326
Ellegren H (2001) Hens, cock and avian sex determination. EMBO reports 2:192–196
Erdman S, Burtis K (1993) The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. EMBO J 12:527–535
Felsenstein J (1989) PHYLIP: phylogeny inference package. Cladistics 5:164–166
Fernandino JI, Guilgur LG, Strobl-Mazzulla PH, Somoza GM (2003) Molecular cloning of SOX9, DMRT1 and SF1 cDNA partial sequences in the pejerrey fish Odontesthes bonariensis (Atheriniformes). Fish Physiol Biochem 28:145–146
Fitch WM, Markowitz E (1970) An improved method for determining codon variability and its application to the rate of fixation of mutations in evolution. Biochem Genet 4:579–593
Gao S, Zhang T, Zhou X, Zhao Y, Li Q, Guo Y, Cheng H, Zhou R (2005) Molecular cloning, expression of Sox5 and its down-regulation of dmrt1 transcription in zebrafish. J Exp Zool (Mol Dev Evol) 304B:476–483
Guan G, Kobayashi T, Nagahama Y (2000) Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the tilapia (Oreochromis niloticus). Biochem Biophys Res Commun 272:662–666
Guo Y, Cheng H, Huang X, Gao S, Yu H, Zhou R (2005) Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem Biophys Res Commun 330:950–957
Huang X, Guo Y, Shui Y, Gao S, Yu H, Cheng H, Zhou R (2005) Multiple alternative splicing and differential expression of dmrt1 during gonad transformation in the rice field eel. Biol Reprod 73:1017–1024
Johnson G, Patterson C (1993) Percomorph phylogeny: a survey of acanthomorphs and a new proposal. Bull Mar Sci 52:554–626
Kettlewell J, Raymond C, Zarkower D (2000) Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 26:174–178
Kondo M, Froschauer A, Kitano A, Nanda I, Hornung U, Volff J, Asakawa S, Mitani H, Naruse K, Tanaka M, Schmid M, Shimizu N, Schartl M, Shima A (2002) Molecular cloning and characterization of DMRT genes from the medaka Oryzias latipes and the platyfish Xiphophorus maculatus. Gene 295:213–222
Marchand O, Govoroun M, D’Cotta H, McMeel O, Lareyre J, Bernot A, Laudet V, Guiguen Y (2000) DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta 1493:180–187
Miya M, Kawaguchi A, Nishida M (2001) Mitogenomic exploration of higher teleostean phylogenies: a case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences. Mol Biol Evol 18:1993–2009
Moniot B, Berta P, Scherer G, Sudbeck P, Poulat F (2000) Male specific expression suggests role of DMRT1 in human sex determination. Mech Dev 91:323–325
Murdock C, Wibbels T (2003) Expression of Dmrt1 in a turtle with temperature-dependent sex determination. Cytogenet Genome Res 101:302–308
Nanda I, Shan Z, Schartl M, Burt D, Koehle M, Nothwang H, Grutzner F, Paton I, Windsor D, Dunn I, Engel W, Staeheli P, Mizuno S, Haaf T, Schmid M (1999) Three-hundred million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21:258–259
Nanda I, Kondo M, Hornung U, Asakawa U, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (2002) A duplicated copy of DMRT1 in the sex-determining region of Y chromosome of medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778–11783
Nelson JS (1994) Fishes of the world. John Wiley and Sons
Osawa N, Oshima Y, Nakamura M (2005) Molecular cloning of Dmrt1 and its expression in the gonad of Xenopus. Zool Sci 22:681–687
Parenti LR, Grier HJ (2004) Evolution and phylogeny of gonad morphology in bony fishes. Integr Comp Biol 44:333–348
Raymond C, Kettlewell J, Hirsch B, Bardwell V, Zarkower D (1999b) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role␣in vertebrate sexual development. Dev Biol 215:208–220
Raymond C, Murphy M, O’Sullivan M, Bardwell V, Zarkower D (2000) Dmrt1, a gene related to worm and fly sexual regulators is required for mammalian testis differentiation. Genes Dev 14:2587–2595
Raymond C, Parker E, Kettlewell J, Brown L, Page D, Kusz K, Jaruzelska J, Reinberg Y, Flejter W, Bardwell V, Hirsch B, Zarkower D (1999a) A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 8:989–996
Raymond C, Shamu C, Shen M, Seifert K, Hirsch B, Hodgkin J, Zarkower D (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391:691–695
Shibata K, Takase M, Nakamura M (2002) The Dmrt1 expression in sex-reversed gonads of amphibians. Gen Comp Endocrinol 127:232–241
Smith C, McCliver P, Western P, Reed K, Sinclair A (1999) Conservation of a sex-determining gene. Nature 402:601–602
Sreenivasulu K, Ganesh S, Roman R (2002) Evolutionarily conserved, DMRT1, encodes alternatively spliced transcripts and shows dimorphic expression during gonadal differentiation in the lizard, Calotes versicolor. Gene Expr Patterns 119:55–64
Strüssmann CA (1989) Basic studies on seed production of pejerrey Odontesthes bonariensis. Doctoral Thesis. Tokyo University of Fisheries, Tokyo, Japan, 351 pp
Strüssmann CA, Saito T, Usui M, Yamada H, Takashima F (1997a) Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J Exp Zool 278:167–177
Strüssmann CA, Akaba T, Ijima K, Yamaguchi K, Yoshizaki G, Takashima F (1997b) Spontaneous hybridization in the laboratory and genetic markers for the identification of hybrids between two atherinid species, Odontesthes bonariensis (Valenciennes, 1835) and Patagonina hatchery (Eigenmann, 1909). Aquacult Res 28:291–300
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Veith A, Froschauer A, Körting C, Nanda I, Hanel R, Schmid M, Shartl M, Volff J (2003) Cloning of dmrt1 gene of Xiphoporus maculatus: dmY/dmrt1Y is not the master sex-determining gene in the patlyfish. Gene 317:59–66
Wiley EO, Johnson GD, Dimmick WW (2000) The relationships of acanthomorph fishes: a total evidence approach using molecular and morphological data. Biochem Syst Ecol 28:319–350
Yi W, Zarkower D (1999) Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 126:873–881
Zhu L, Wilken J, Phillips NB, Narendra U, Chan G, Stratton SM (2000) Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev 14:1750–1764
Acknowledgements
The authors would like to thank Gabriela Carina López for her technical assistance, Dr. Denisse Vizziano for the analysis of the different pejerrey spermatogenetic stages and Dr. Carlos Augusto Strüssmann for his helpful discussion and suggestions. Grant sponsor: Agencia Nacional de Promoción Científica y Tecnológica (ANPCYT, Argentina). Grant # 01-12168 to G.M.S. and from the Ministry of Education, Culture, Sports, Science and Technology of Japan Grant (#15201003).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fernandino, J.I., Guilgur, L.G. & Somoza, G.M. Dmrt1 expression analysis during spermatogenesis in pejerrey, Odontesthes bonariensis . Fish Physiol Biochem 32, 231–240 (2006). https://doi.org/10.1007/s10695-006-9005-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-006-9005-9
Keywords
- Dmrt1
- Pejerrey
- Testis
- Spermatogenesis