Abstract
In chicken, the left and right female gonads undergo a completely different program during development. To learn more about the molecular factors underlying side-specific development and to identify potential sex- and side-specific genes in developing gonads, we separately performed next-generation sequencing-based deepSuperSAGE transcription profiling from left and right, female and male gonads of 19-day-old chicken embryos. A total of 836 transcript variants were significantly differentially expressed (p < 10-5) between combined male and female gonads. Left-right comparison revealed 1,056 and 822 differentially (p < 10-5) expressed transcript variants for male and female gonads, respectively, of which 72 are side-specific in both sexes. At least some of these may represent key players for lateral development in birds. Additionally, several genes with laterally differential expression in the ovaries seem to determine female gonads for growth or regression, whereas right-left differences in testes are mostly limited to the differentially expressed genes present in both sexes. With a few exceptions, side-specific genes are not located on the sex chromosomes. The large differences in lateral gene expression in the ovaries in almost all metabolic pathways suggest that the regressing right gonad might have undergone a change of function during evolution.
Journal Section:
Editor's choice
References
1.
Akmaev VR, Wang CJ: Correction of sequence-based artifacts in serial analysis of gene expression. Bioinformatics 20:1254-1263 (2004).
[PubMed]
2.
Alam MA, Kobayashi Y, Horiguchi R, Hirai T, Nakamura M: 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 (2008).
[PubMed]
3.
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al: Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402 (1997).
[PubMed]
4.
Ayers KL, Sinclair AH, Smith CA: The molecular genetics of ovarian differentiation in the avian model. Sex Dev 7:80-94 (2013).
[PubMed]
5.
Bassuk JA, Iruela-Arispe ML, Lane TF, Benson JM, Berg RA, Sage EH: Molecular analysis of chicken embryo SPARC (osteonectin). Eur J Biochem 218:117-127 (1993).
[PubMed]
6.
Camon E, Magrane M, Barrell D, Lee V, Dimmer E, et al: The gene ontology annotation (GOA) database: sharing knowledge in Uniprot with gene ontology. Nucleic Acids Res 32:D262-D266 (2004).
[PubMed]
7.
Carré GA, Couty I, Hennequet-Antier C, Govoroun MS: Gene expression profiling reveals new potential players of gonad differentiation in the chicken embryo. PLoS One 6:e23959 (2011).
[PubMed]
8.
Chen F, Mackey AJ, Stoeckert CJ, Roos DS: OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34:D363-D368 (2006).
[PubMed]
9.
Chiu CG, Strugnell SS, Griffith OL, Jones SJ, Gown AM, et al: Diagnostic utility of galectin-3 in thyroid cancer. Am J Pathol 176:2067-2081 (2010).
[PubMed]
10.
Chue J, Smith CA: Sex determination and sexual differentiation in the avian model. FEBS J 278:1027-1034 (2011).
[PubMed]
11.
Civetta A, Singh RS: Broad-sense sexual selection, sex gene pool evolution, and speciation. Genome 42:1033-1041 (1999).
[PubMed]
12.
Connallon T, Knowles LL: Intergenomic conflict revealed by patterns of sex-biased gene expression. Trends Genet 21:495-499 (2005).
[PubMed]
13.
Connallon T, Knowles LL: Recombination rate and protein evolution in yeast. BMC Evol Biol 7:235 (2007).
[PubMed]
14.
Delostrinos CF, Hudson AE, Feng WC, Kosman J, Bassuk JA: The c-terminal Ca2+-binding domain of SPARC confers anti-spreading activity to human urothelial cells. J Cell Physiol 206:211-220 (2006).
[PubMed]
15.
Diaz FJ, Anthony K, Halfhill AN: Early avian follicular development is characterized by changes in transcripts involved in steroidogenesis, paracrine signaling and transcription. Mol Reprod Dev 78:212-223 (2011).
[PubMed]
16.
Eads BD, Colbourne JK, Bohuski E, Andrews J: Profiling sex-biased gene expression during parthenogenetic reproduction in Daphnia pulex. BMC Genomics 8:464 (2007).
[PubMed]
17.
Ellegren H: Evolution of the avian sex chromosomes and their role in sex determination. Trends Ecol Evol 15:188-192 (2000).
[PubMed]
18.
Ellegren H, Parsch J: The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8:689-698 (2007).
[PubMed]
19.
Ellegren H, Hultin-Rosenberg L, Brunstrom B, Dencker L, Kultima K, Scholz B: Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol 5:40 (2007).
[PubMed]
20.
Florio T, Rim C, Hershberger RE, Loda M, Stork PJ: The somatostatin receptor SSTR1 is coupled to phosphotyrosine phosphatase-activity in CHO-K1 cells. Mol Endocrinol 8:1289-1297 (1994).
[PubMed]
21.
Fridolfsson AK, Ellegren H: A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116-121 (1999).
22.
Fridolfsson AK, Cheng H, Copeland NG, Jenkins NA, Liu HC, et al: Evolution of the avian sex chromosomes from an ancestral pair of autosomes. Proc Natl Acad Sci USA 95:8147-8152 (1998).
[PubMed]
23.
Germain P, Staels B, Dacquet C, Spedding M, Laudet V: Overview of nomenclature of nuclear receptors. Pharmacol Rev 58:685-704 (2006).
[PubMed]
24.
González-Morán MG: Histological and stereological changes in growing and regressing chicken ovaries during development. Anat Rec 294:893-904 (2011).
[PubMed]
25.
Hambuch TM, Parsch J: Patterns of synonymous codon usage in Drosophila melanogaster genes with sex-biased expression. Genetics 170:1691-1700 (2005).
[PubMed]
26.
Hamburger V, Hamilton HL: A series of normal stages in the development of the chick embryo. J Morphol 88:49-92 (1951).
[PubMed]
27.
Hori T, Asakawa S, Itoh Y, Shimizu N, Mizuno S: Wpkci, encoding an altered form of PKCI, is conserved widely on the avian W chromosome and expressed in early female embryos: implication of its role in female sex determination. Mol Biol Cell 11:3645-3660 (2000).
[PubMed]
28.
Hoshino A, Koide M, Ono T, Yasugi S: Sex-specific and left-right asymmetric expression pattern of Bmp7 in the gonad of normal and sex-reversed chicken embryos. Dev Growth Differ 47:65-74 (2005).
[PubMed]
29.
Hubbard TJ, Aken BL, Beal K, Ballester B, Caccamo M, et al: Ensembl 2007. Nucl Acids Res 35:D610-617 (2007).
[PubMed]
30.
Hudson QJ, Smith CA, Sinclair AH: Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Dev Dyn 233:1052-1055 (2005a).
[PubMed]
31.
Hudson QJ, Smith CA, Sinclair AH: Conserved expression of a novel gene during gonadal development. Dev Dyn 233:1083-1090 (2005b).
[PubMed]
32.
Hulsen T, Huynen MA, de Vlieg J, Groenen PM: Benchmarking ortholog identification methods using functional genomics data. Genome Biol 7:R31 (2006).
[PubMed]
33.
Ikeda K, Sato M, Tsutsumi O, Tsuchiya F, Tsuneizumi M, et al: Promoter analysis and chromosomal mapping of human EBAG9 gene. Biochem Biophys Res Commun 273:654-660 (2000).
[PubMed]
34.
Intarapat S, Stern CD: Sexually dimorphic and sex-independent left-right asymmetries in chicken embryonic gonads. PLoS One 8:e69893 (2013).
[PubMed]
35.
Itoh Y, Melamed E, Yang X, Kampf K, Wang S, et al: Dosage compensation is less effective in birds than in mammals. J Biol 6:2-2 (2007).
[PubMed]
36.
Ivakine EA, Fox CJ, Paterson AD, Mortin-Toth SM, Canty A, et al: Sex-specific effect of insulin-dependent diabetes 4 on regulation of diabetes pathogenesis in the nonobese diabetic mouse. J Immunol 174:7129-7140 (2005).
[PubMed]
37.
Jacob M, Bakst MR: Anatomy of the female reproductive tract, in Jamieson BG (ed): Reproductive Biology and Phylogeny of Aves (Birds), vol 6A, pp 553-587 (USA: Science Publishers, Enfield 2007).
38.
Koba N, Ohfuji T, Ha Y, Mizushima S, Tsukada A, et al: Profiles of mRNA expression of Foxl2, P450arom, Dmrt 1, Amh, P450(c17), Sf1, Er alpha and Ar, in relation to gonadal sex differentiation in duck embryo. J Poultry Sci 45:132-138 (2008).
39.
Lavial F, Acloque H, Bertocchini F, MacLeod DJ, Boast S, et al: The Oct4 homologue Pouv and Nanog regulate pluripotency in chicken embryonic stem cells. Development 134:3549-3563 (2007).
[PubMed]
40.
Li H, Coghlan A, Ruan J, Coin LJ, Heriche JK, et al: Treefam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res 34:D572-D580 (2006).
[PubMed]
41.
Li L, Stoeckert CJ, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178-2189 (2003).
[PubMed]
42.
Lu F, Bytautiene E, Tamayo E, Gamble P, Anderson GD, et al: Gender-specific effect of overexpression of sFlt-1 in pregnant mice on fetal programming of blood pressure in the offspring later in life. Am J Obstet Gynecol 197:418 (2007).
[PubMed]
43.
Man MZ, Wang X, Wang Y: Power_sage: comparing statistical tests for sage experiments. Bioinformatics 16:953-959 (2000).
[PubMed]
44.
Mank JE, Hultin-Rosenberg L, Axelsson E, Ellegren H: Rapid evolution of female-biased, but not male-biased, genes expressed in the avian brain. Mol Biol Evol 24:2698-2706 (2007).
[PubMed]
45.
Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JM, James AA: Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mo Biol 15:1-12 (2006).
[PubMed]
46.
Matsumura H, Reich S, Ito A, Saitoh H, Kamoun S, et al: Gene expression analysis of plant host-pathogen interactions by superSAGE. Proc Natl Acad Sci USA 100:15718-15723 (2003).
[PubMed]
47.
Matsumura H, Ito A, Saitoh H, Winter P, Kahl G, et al: SuperSAGE. Cell Microbiol 7:11-18 (2005).
[PubMed]
48.
Matsumura H, Yoshida K, Luo SJ, Kimura E, Fujibe T, et al: High-throughput superSAGE for digital gene expression analysis of multiple samples using next generation sequencing. PLoS One 5:e12010 (2010).
[PubMed]
49.
Matsumura H, Yoshida K, Luo S, Krüger DH, Kahl G, et al: High-throughput superSAGE. Methods Mol Biol 687:135-146 (2011).
[PubMed]
50.
McNagny KM, Pettersson I, Rossi F, Flamme I, Shevchenko A, et al: Thrombomucin, a novel cell surface protein that defines thrombocytes and multipotent hematopoietic progenitors. J Cell Biol 138:1395-1407 (1997).
[PubMed]
51.
Meiklejohn CD, Parsch J, Ranz JM, Hartl DL: Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci USA 100:9894-9899 (2003).
[PubMed]
52.
Merchant-Larios H, Moreno-Mendoza N: Onset of sex differentiation: dialog between genes and cells. Arch Med Res 32:553-558 (2001).
[PubMed]
53.
Nakata T, Ishiguro M, Aduma N, Izumi H, Kuroiwa A: Chicken hemogen homolog is involved in the chicken-specific sex-determining mechanism. Proc Natl Acad Sci USA 110:3417-3422 (2013).
[PubMed]
54.
Nanda I, Shan ZH, Schartl M, Burt DW, Koehler M, et al: 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21:258-259 (1999).
[PubMed]
55.
Nomura O, Nakabayashi O, Nishimori K, Yasue H, Mizuno S: Expression of five steroidogenic genes including aromatase gene at early developmental stages of chicken male and female embryos. J Steroid Biochem Mol Biol 71:103-109 (1999).
[PubMed]
56.
Nuclear Receptors Nomenclature Committee: A unified nomenclature system for the nuclear receptor superfamily. Cell 97:161-163 (1999).
[PubMed]
57.
O'Brien KP, Westerlund I, Sonnhammer EL: Orthodisease: a database of human disease orthologs. Hum Mutat 24:112-119 (2004).
[PubMed]
58.
O'Brien KP, Remm M, Sonnhammer EL: Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res33:D476-D480 (2005).
[PubMed]
59.
O'Neill M, Binder M, Smith C, Andrews J, Reed K, et al: ASW: a gene with conserved avian W-linkage and female specific expression in chick embryonic gonad. Dev Genes Evol 210:243-249 (2000).
[PubMed]
60.
Oréal E, Mazaud S, Picard JY, Magre S, Carre-Eusebe D: Different patterns of anti-mullerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads. Dev Dyn 225:221-232 (2002).
[PubMed]
61.
Patel YC: Somatostatin and its receptor family. Front Neuroendocrinol 20:157-198 (1999).
[PubMed]
62.
Pedernera E, Solis L, Peralta I, Velazquez PN: Proliferative and steroidogenic effects of follicle-stimulating hormone during chick embryo gonadal development. Gen Comp Endocrinol 116:213-220 (1999).
[PubMed]
63.
Perron JC, Bixby JL: Tetraspanins expressed in the embryonic chick nervous system. FEBS Lett 461:86-90 (1999).
[PubMed]
64.
Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45 (2001).
[PubMed]
65.
Pizette S, Niswander L: BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126:883-894 (1999).
[PubMed]
66.
Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL: Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742-1745 (2003).
[PubMed]
67.
Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D: Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215:208-220 (1999).
[PubMed]
68.
Remm M, Storm CEV, Sonnhammer ELL: Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 314:1041-1052 (2001).
[PubMed]
69.
Righi A, Jin L, Zhang S, Stilling G, Scheithauer BW, et al: Identification and consequences of galectin-3 expression in pituitary tumors. Mol Cell Endocrinol 326:8-14 (2010).
[PubMed]
70.
Rodríguez-Léon J, Esteban CR, Marti M, Santiago-Josefat B, Dubova I, et al: Pitx2 regulates gonad morphogenesis. Proc Natl Acad Sci USA 105:11242-11247 (2008).
[PubMed]
71.
Ryan AK, Blumberg B, Rodriguez-Esteban C, Yonei-Tamura S, Tamura K, et al: Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 394:545-551 (1998).
[PubMed]
72.
Sage H, Vernon RB, Funk SE, Everitt EA, Angello J: SPARC, a secreted protein associated with cellular proliferation, inhibits cell spreading in vitro and exhibits Ca2+-dependent binding to the extracellular-matrix. J Cell Biol 109:341-356 (1989).
[PubMed]
73.
Saha S, Sparks AB, Rago C, Akmaev V, Wang CJ, et al: Using the transcriptome to annotate the genome. Nat Biotechnol 20:508-512 (2002).
[PubMed]
74.
Scholz B, Kultima K, Mattsson A, Axelsson J, Brunstrom B, et al: Sex-dependent gene expression in early brain development of chicken embryos. BMC Neurosci 7:12 (2006).
[PubMed]
75.
Shimada K: Sex determination and sex differentiation. Avian Poult Biol Rev 13:1-14 (2002).
76.
Smith CA: Molecular genetics of avian, sex determination and gonadal differentiation, in Jamieson BG (ed): Reproductive Biology and Phylogeny of Birds, vol 6B, pp 479-506 (USA: Science Publishers, Enfield 2007).
77.
Smith CA, Sinclair AH: Sex determination in the chicken embryo. J Exp Zool 290:691-699 (2001).
[PubMed]
78.
Smith CA, Sinclair AH: Sex determination: insights from the chicken. Bioessays 26:120-132 (2004).
[PubMed]
79.
Smith CA, Roeszler KN, Bowles J, Koopman P, Sinclair AH: Onset of meiosis in the chicken embryo; evidence of a role for retinoic acid. BMC Dev Biol 8:85 (2008a).
[PubMed]
80.
Smith CA, Shoemaker CM, Roeszler KN, Queen J, Crews D, Sinclair AH: Cloning and expression of R-spondin1 in different vertebrates suggests a conserved role in ovarian development. BMC Dev Biol 8:72 (2008b).
[PubMed]
81.
Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, et al: The avian Z-linked gene Dmrt1 is required for male sex determination in the chicken. Nature 461:267-271 (2009).
[PubMed]
82.
Swanson WJ, Vacquier VD: The rapid evolution of reproductive proteins. Nat Rev Genet 3:137-144 (2002).
[PubMed]
83.
Termine JD, Kleinman HK, Whitson SW, Conn KM, McGarvey ML, Martin GR: Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26:99-105 (1981).
[PubMed]
84.
Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T: Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127:2741-2750 (2000).
[PubMed]
85.
Turner JM: Meiotic sex chromosome inactivation. Development 134:1823-1831 (2007).
[PubMed]
86.
Ukeshima A: Germ cell death in the degenerating right ovary of the chick embryo. Zoolog Sci 13:559-563 (1996).
[PubMed]
87.
Ukeshima A, Fujimoto T: A fine morphological study of germ cells in asymmetrically developing right and left ovaries of the chick. Anat Rec 230:378-386 (1991).
[PubMed]
88.
Velculescu V, Zhang L, Vogelstein B, Kinzler K: Serial analysis of gene expression. Science 270:484-487 (1995).
[PubMed]
89.
Villalpando I, Sanchez-Bringas G, Sanchez-Vargas I, Pedernera E, Villafan-Monroy H: The p450 aromatase (P450arom) gene is asymmetrically expressed in a critical period for gonadal sexual differentiation in the chick. Gen Comp Endocrinol 117:325-334 (2000).
[PubMed]
90.
Wan Y, Kirschner MW: Identification of multiple CDH1 homologues in vertebrates conferring different substrate specificities. Proc Natl Acad Sci USA 98:13066-13071 (2001).
[PubMed]
91.
Wicker T, Robertson JS, Schulze SR, Feltus FA, Magrini V, et al: The repetitive landscape of the chicken genome. Genome Res 15:126-136 (2005).
[PubMed]
92.
Wright MW, Eyre TA, Lush MJ, Povey S, Bruford EA: HCOP: the HGNC comparison of orthology predictions search tool. Mamm Genome 16:827-828 (2005).
[PubMed]
93.
Wu JX, Pines M, Gay CV, Hurwitz S, Leach RM: Immunolocalization of osteonectin in avian tibial dyschondroplastic cartilage. Dev Dyn 207:69-74 (1996).
[PubMed]
94.
Xu HY, Hou XW, Wang NF, Hui B, Jin JF, et al: Gender-specific effect of estrogen receptor-1 gene polymorphisms in coronary artery disease and its angiographic severity in Chinese population. Clin Chim Acta 395:130-133 (2008).
[PubMed]
95.
Yamamoto I, Tsukada A, Saito N, Shimada K: Profiles of mRNA expression of genes related to sex differentiation of the gonads in the chicken embryo. Poultry Sci 82:1462-1467 (2003).
[PubMed]
96.
Yang H, Lei C, Zhang W: Expression of galectin-3 in mouse endometrium and its effect during embryo implantation. Reprod Biomed Online 24:116-122 (2012).
[PubMed]
97.
Yang X, Schadt EE, Wang S, Wang H, Arnold AP, et al: Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16:995-1004 (2006).
[PubMed]
98.
Zawada AM, Rogacev KS, Rotter B, Winter P, Marell R-R, Fliser D, Heine GH: Supersage evidence for CD14++CD16+ monocytes as a third monocyte subset. Blood (2011).
[PubMed]
99.
Zawada AM, Rogacev KS, Hummel B, Grün OS, Friedrich A, et al: SuperTAG methylation-specific digital karyotyping reveals uremia-induced epigenetic dysregulation of atherosclerosis-related genes. Circ Cardiovas Genet 5:611-620 (2012).
[PubMed]
100.
Zhang Z, Hambuch TM, Parsch J: Molecular evolution of sex-biased genes in Drosophila. Mol Biol Evol 21:2130-2139 (2004).
[PubMed]
101.
Zhao D, McBride D, Nandi S, McQueen HA, McGrew MJ, et al: Somatic sex identity is cell autonomous in the chicken. Nature 464:237-242 (2010).
[PubMed]
© 2014 S. Karger AG, Basel
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
2014
You do not currently have access to this content.
