Sex determination in frogs (anurans) is genetic and includes both male and female heterogamety. However, the origins of the sex chromosomes and their differentiation processes are poorly known. To investigate diversity in the origins of anuran sex chromosomes, we compared the chromosomal locations of sex-linked genes in 4 species: the African clawed frog (Xenopus laevis), the Western clawed frog (Silurana/X. tropicalis), the Japanese bell-ring frog (Buergeria buergeri), and the Japanese wrinkled frog (Rana rugosa). Comparative mapping data revealed that the sex chromosomes of X. laevis, X. tropicalis and R. rugosa are different chromosome pairs; however, the sex chromosomes of X. tropicalis and B. buergeri are homologous, although this may represent distinct evolutionary origins. We also examined the status of sex chromosomal differentiation in B. buergeri, which possesses heteromorphic ZW sex chromosomes, using comparative genomic hybridization and chromosome painting with DNA probes from the microdissected W chromosome. At least 3 rearrangement events have occurred in the proto-W chromosome: deletion of the nucleolus organizer region and a paracentric inversion followed by amplification of non-W-specific repetitive sequences.

Keywords:
Anuran, Buergeria, Chromosome homology, Comparative map, FISH, Sex chromosome, Xenopus
1.
Atsumi S, Ohta S, Sumida M: Sex differences in polymorphism and expression of AAT-1 in the Hiroshima population of Buergeria buergeri (Anura, Rhacophoridae). Zoolog Sci 15:469-475 (1998).
2.
Belterman RHR, de Boer LEM: A karyological study of 55 species of birds, including karyotypes of 39 species new to cytology. Genetica 65:39-82 (1984).
3.
Bewick AJ, Anderson DW, Evans BJ: Evolution of the closely related, sex-related genes DM-W and DMRT1 in African clawed frogs (Xenopus). Evolution 65:698-712 (2011).
4.
Bewick AJ, Chain FJ, Zimmerman LB, Sesay A, Gilchrist MJ, et al: A large pseudoautosomal region on the sex chromosomes of the frog Silurana tropicalis. Genome Biol Evol 5:1087-1098 (2013).
5.
Brelsford A, Stöck M, Betto-Colliard C, Dubey S, Dufresnes C, et al: Homologous sex chromosomes in three deeply divergent anuran species. Evolution 67:2434-2440 (2013).
6.
Charlesworth D, Mank JE: The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 186:9-31 (2010).
7.
Devlin RH, Nagahama Y: Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191-364 (2002).
8.
Elinson RP: Inheritance and expression of a sex-linked enzyme in the frog, Rana clamitans. Biochem Genet 21:435-442 (1983).
9.
Evans BJ, Kelley DB, Tinsley RC, Melnick DJ, Cannatella DC: A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol Phylogenet Evol 33:197-213 (2004).
10.
Evans BJ, Pyron RA, Wiens JJ: Polyploidization and sex chromosome evolution in amphibians, in Soltis PS, Soltis DE (eds): Polyploidy and Genome Evolution, pp 385-410 (Springer Verlag, Heidelberg 2012).
11.
Hedges SB, Dudley J, Kumar S: TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971-2972 (2006).
12.
Hellsten U, Khokha MK, Grammer TC, Harland RM, Richardson P, Rokhsar DS: Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis. BMC Biol 5:31 (2007).
13.
Hillis DM, Green DM: Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians. J Evol Biol 3:49-64 (1990).
14.
Houmard B, Small C, Yang L, Naluai-Cecchini T, Cheng E, et al: Global gene expression in the human fetal testis and ovary. Biol Reprod 81:438-443 (2009).
15.
Iwade R, Maruo K, Okada G, Nakamura M: Elevated expression of P450c17(CYP17) during testicular formation in the frog. Gen Comp Endocrinol 155:79-87 (2008).
16.
Kawagoshi T, Uno Y, Matsubara K, Matsuda Y, Nishida C: The ZW micro-sex chromosomes of the Chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae, Testudines) have the same origin as chicken chromosome 15. Cytogenet Genome Res 125:125-131 (2009).
17.
Kawagoshi T, Nishida C, Matsuda Y: The origin and differentiation process of the X and Y chromosomes of the black marsh turtle (Siebenrockiella crassicollis, Geoemydidae, Testudines). Chromosome Res 20:95-110 (2012).
18.
Kawagoshi T, Uno Y, Nishida C, Matsuda Y: The Staurotypus turtles and aves share the same origin of sex chromosomes but evolved different types of heterogametic sex determination. PLoS One 9:e105315 (2014).
19.
Kawai A, Nishida-Umehara C, Ishijima J, Tsuda Y, Ota H, Matsuda Y: Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet Genome Res 117:92-102 (2007).
20.
Kawai A, Ishijima J, Nishida C, Kosaka A, Ota H, et al: The ZW sex chromosomes of Gekko hokouensis (Gekkonidae, Squamata) represent highly conserved homology with those of avian species. Chromosoma 118:43-51 (2009).
21.
Khokha MK, Krylov V, Reilly MJ, Gall JG, Bhattacharya D, et al: Rapid gynogenetic mapping of Xenopus tropicalis mutations to chromosomes. Dev Dyn 238:1398-1406 (2009).
22.
Kikuchi K, Hamaguchi S: Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn 242:339-353 (2013).
23.
Kochan KJ, Wright DA, Schroeder LJ, Shen J, Morizot DC: Genetic linkage maps of the West African clawed frog Xenopus tropicalis. Dev Dyn 226:99-102 (2003).
24.
Matsuda Y, Chapman VM: Application of fluorescence in situ hybridization in genome analysis of the mouse. Electrophoresis 16:261-272 (1995).
25.
Mawaribuchi S, Ikeda N, Fujitani K, Ito Y, Onuma Y, et al: Cell-mass structures expressing the aromatase gene Cyp19a1 lead to ovarian cavities in Xenopus laevis. Endocrinology 155:3996-4005 (2014).
26.
Nanda I, Shan Z, 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).
27.
Nanda I, Haaf T, Schartl M, Schmid M, Burt DW: Comparative mapping of Z-orthologous genes in vertebrates: implications for the evolution of avian sex chromosomes. Cytogenet Genome Res 99:178-184 (2002).
28.
Nishioka M, Hanada H, Miura I, Ryuzaki M: Four kinds of sex chromosomes in Rana rugosa. Sci Rep Lab Amphibian Biol Hiroshima Univ 13:1-134 (1994).
29.
Ohta S: Sex determining mechanism in Buergeria buergeri (Schlegel). I. Heterozygosity of chromosome pair No. 7 in the female. Sci Rep Lab Amphibian Biol Hiroshima Univ 8:29-43 (1986).
30.
Olmo E, Signorino G: Chromorep: a reptile chromosomes database. http://193.206.118.100/professori/chromorep.pdf (2005).
31.
Olmstead AW, Lindberg-Livingston A, Degitz SJ: Genotyping sex in the amphibian, Xenopus(Silurana) tropicalis, for endocrine disruptor bioassays. Aquat Toxicol 98:60-66 (2010).
32.
Sakurai N, Maruo K, Haraguchi S, Uno Y, Oshima Y, et al: Immunohistochemical detection and biological activities of CYP17 (P450c17) in the indifferent gonad of the frog Rana rugosa. J Steroid Biochem Mol Biol 112:5-12 (2008).
33.
Schmid M, Steinlein C: Sex chromosomes, sex-linked genes, and sex determination in the vertebrate class Amphibia, in Scherer G, Schmid M (eds): Genes and Mechanisms in Vertebrate Sex Determination, pp 143-176 (Birkhäuser Verlag, Basel 2001).
34.
Schmid M, Ohta S, Steinlein C, Guttenbach M: Chromosome banding in Amphibia. XIX. Primitive ZW/ZZ sex-chromosomes in Buergeria buergeri (Anura, Rhacophoridae). Cytogenet Cell Genet 62:238-246 (1993).
35.
Schmid M, Steinlein C, Bogart JP, Feichtinger W, León P, et al: The chromosomes of terraranan frogs. Insights into vertebrate cytogenetics. Cytogenet Genome Res 130/131:1-568 (2010).
36.
Schmid M, Steinlein C, Bogart JP, Feichtinger W, Haaf T, et al: The hemiphractid frogs. Phylogeny, embryology, life history, and cytogenetics. Cytogenet Genome Res 138:69-384 (2012).
37.
Shimada K: Gene expression of steroidogenic enzymes in chicken embryonic gonads. J Exp Zool 281:450-456 (1998).
38.
Suda M, Uno Y, Mori Y, Matsuda Y, Nakamura M: Molecular cytogenetic characterization of telomere-specific repetitive DNA sequences in Rana rugosa. J Exp Zool A Ecol Genet Physiol 315:222-231 (2011).
39.
Sumida M, Nishioka M: Sex-linked genes and linkage maps in amphibians. Comp Biochem Physiol B Biochem Mol Biol 126:257-270 (2000).
40.
Taguchi T, Akimaru K, Hirai H, Mwenda JM, Yuri K: A probe generated by chromosome microdissection, useful for analyzing Y chromosome evolution in Old World monkeys. Chromosome Res 11:147-152 (2003).
41.
Taguchi T, Hirai Y, LoVerde PT, Tominaga A, Hirai H: DNA probes for identifying chromosomes 5, 6, and 7 of Schistosoma mansoni. J Parasitol 93:724-726 (2007).
42.
Takagi N, Sasaki M: A phylogenetic study of bird karyotypes. Chromosoma 46:91-120 (1974).
43.
Tymowska J: Karyotype analysis of Xenopus tropicalis Gray, Pipidae. Cytogenet Cell Genet 12:297-304 (1973).
44.
Uno Y, Nishida C, Oshima Y, Yokoyama S, Miura I, et al: Comparative chromosome mapping of sex-linked genes and identification of sex chromosomal rearrangements in the Japanese wrinkled frog (Rana rugosa, Ranidae) with ZW and XY sex chromosome systems. Chromosome Res 16:637-647 (2008a).
45.
Uno Y, Nishida C, Yoshimoto S, Ito M, Oshima Y, et al: Diversity in the origins of sex chromosomes in anurans inferred from comparative mapping of sexual differentiation genes for three species of the Raninae and Xenopodinae. Chromosome Res 16:999-1011 (2008b).
46.
Uno Y, Nishida C, Tarui H, Ishishita S, Takagi C, et al: Inference of the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes from comparative gene mapping. PLoS One 7:e53027 (2012).
47.
Uno Y, Nishida C, Takagi C, Ueno N, Matsuda Y: Homoeologous chromosomes of Xenopus laevis are highly conserved after whole genome duplication. Heredity 111:430-436 (2013).
48.
Vorontsov NN, Lyapunova EA, Borissov YM, Dovgal VE: Variability of sex chromosomes in mammals. Genetica 52/53:361-372 (1980).
49.
Wright DA, Richards CM: Two sex-linked loci in the leopard frog, Rana pipiens. Genetics 103:249-261 (1983).
50.
Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, et al: A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105:2469-2474 (2008).
51.
Yoshimoto S, Ikeda K, Izutsu Y, Shiba T, Takamatsu N, Ito M: Opposite roles of DMRT1 and its W-linked paralogue, DM-W, in sexual dimorphism of Xenopus laevis: implications of a ZZ/ZW-type sex-determining system. Development 137:2519-2526 (2010).
52.
Zhou LY, Wang DS, Kobayashi T, Yano A, Paul-Prasanth B, et al: A novel type of P450c17 lacking the lyase activity is responsible for C21-steroid biosynthesis in the fish ovary and head kidney. Endocrinology 146:4282-4291 (2007).
© 2015 S. Karger AG, Basel
2015
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.
You do not currently have access to this content.