Is premeiotic genome elimination an exclusive mechanism for hemiclonal reproduction in hybrid males of the genus Pelophylax?

. 2016 Jul 02 ; 17 (1) : 100. [epub] 20160702

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid27368375
Odkazy

PubMed 27368375
PubMed Central PMC4930623
DOI 10.1186/s12863-016-0408-z
PII: 10.1186/s12863-016-0408-z
Knihovny.cz E-zdroje

BACKGROUND: The ability to eliminate a parental genome from a eukaryotic germ cell is a phenomenon observed mostly in hybrid organisms displaying an alternative propagation to sexual reproduction. For most taxa, the underlying cellular pathways and timing of the elimination process is only poorly understood. In the water frog hybrid Pelophylax esculentus (parental taxa are P. ridibundus and P. lessonae) the only described mechanism assumes that one parental genome is excluded from the germline during metamorphosis and prior to meiosis, while only second genome enters meiosis after endoreduplication. Our study of hybrids from a P. ridibundus-P. esculentus-male populations known for its production of more types of gametes shows that hybridogenetic mechanism of genome elimination is not uniform. RESULTS: Using comparative genomic hybridization (CGH) on mitotic and meiotic cell stages, we identified at least two pathways of meiotic mechanisms. One type of Pelophylax esculentus males provides supporting evidence of a premeiotic elimination of one parental genome. In several other males we record the presence of both parental genomes in the late phases of meiotic prophase I (diplotene) and metaphase I. CONCLUSION: Some P. esculentus males have no genome elimination from the germ line prior to meiosis. Considering previous cytological and experimental evidence for a formation of both ridibundus and lessonae sperm within a single P. esculentus individual, we propose a hypothesis that genome elimination from the germline can either be postponed to the meiotic stages or absent altogether in these hybrids.

Zobrazit více v PubMed

Alves MJ, Coelho MM, Collares-Pereira MJ. Evolution in action through hybridisation and polyploidy in an Iberian freshwater fish: a genetic review. Genetica. 2001;111:375–385. doi: 10.1023/A:1013783029921. PubMed DOI

Berger L, Günther R. Genetic composition and reproduction of water frog populations (Rana kl. esculenta Synklepton) near nature reserve Serrahn, GDR. Arch Natschutz Landschforsch Berlin. 1988;28:265–280.

Berger L, Günther R. Inheritance patterns of water frog males from the environments of nature reserve Steckby, Germany. Zool Pol. 1991–1992;37:87–100.

Bi K, Bogart JP. Identification of intergenomic recombination in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH) Cytogenet Genome Res. 2006;112:307–312. doi: 10.1159/000089885. PubMed DOI

Bucci S, Ragghianti M, Mancino G, Berger L, Hotz H, Uzzell T. Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species. J Exp Zool. 1990;255:37–56. doi: 10.1002/jez.1402550107. PubMed DOI

Choleva L, Janko K, De Gelas K, Bohlen J, Šlechtová V, Rábová M, Ráb P. Synthesis of clonality and polyploidy in vertebrate animals by hybridization between two sexual species. Evolution. 2012;66:2191–2203. doi: 10.1111/j.1558-5646.2012.01589.x. PubMed DOI

Cimino MC. Egg-production, polyploidization and evolution in a diploid all–female fish of the genus Poeciliopsis. Evolution. 1972a;26:294–306. PubMed

Cimino MC. Meiosis in triploid all–female fish (Poeciliopsis, Poeciliidae). Science. 1972b;175:1484–1486. PubMed

Dawley RM. An introduction to unisexual vertebrates. In: Dawley RM, Bogard JP, editors. Evolution and Ecology of unisexual vertebrates New York State museum. Albany: New York Bulletin; 1989. pp. 1–18.

Dedukh D, Litvinchuk SN, Rosanov JM, Shabanov DA, Krasikova AK. Crossing experiments reveal gamete contribution into appearance of di–and triploid hybrid frogs in Pelophylax esculentus population systems. Chromosome Res. 2015;23:380–381.

Graf JD, Müller WP. Experimental gynogenesis provides evidence of hybridogenetic reproduction in the Rana esculenta complex. Experientia. 1979;35:1574–1576. doi: 10.1007/BF01953200. PubMed DOI

Graf JD, Karch F, Moreillon MC. Biochemical variation in the Rana esculenta complex: A new hybrid form related to Rana perezi and Rana ridibunda. Experientia. 1977;33:1582–1584. doi: 10.1007/BF01934010. PubMed DOI

Graham DE. The isolation of high molecular weight DNA from whole organisms or large tissue masses. Anal Biochem. 1978;85:609–613. doi: 10.1016/0003-2697(78)90262-2. PubMed DOI

Grandont L, Jenczewski E, Lloyd A. Meiosis and its deviations in polyploid plants. Cytogenet Genome Res. 2013;140:171–184. doi: 10.1159/000351730. PubMed DOI

Günther R. Der Karyotyp von Rana ridibunda Pall. und das Vorkommen von Triploidie bei Rana esculenta L. (Anura, Amphibia) Biol Zentralbl. 1970;89:327–342.

Günther R. Über die verwandtschaftlichen Beziehungen zwischen den europäischen Grünfröschen und den Bastardcharakter von Rana esculenta L. (Anura) Zool Anz. 1973;190:250–285.

Günther R. Untersuchungen der Meiose bei Männchen von Rana ridibunda Pall., Rana lessonae Cam. und der Bastardform “Rana esculenta” L. (Anura) Biol Zentralbl. 1975;94:277–294.

Günther R. Zur Populationsgenetik der mitteleuropäischen Wasserfröschen des Rana esculenta–Synkleptons (Anura, Ranidae) Zool Anz. 1983;197:43–54.

Günther R, Plötner J. Zur Problematik der klonalen Vererbung bei Rana kl. esculenta (Anura). In: Beiträge zur Biologie und Bibliographie (1960–1987) der europäischen Wasserfrösche. Jb Feldherp Beiheft. 1988;1:23–46.

Heppich S, Tunner HG, Greilhuber J. Premeiotic chromosome doubling after genome elimination during spermatogenesis of the species hybrid Rana esculenta. Theor Appl Genet. 1982;61:101–104. doi: 10.1007/BF00273874. PubMed DOI

Hotz H, Uzzell T. Interspecific hybrids of Rana ridibunda without germ line exclusion of a parental genome. Experientia. 1983;39:538–540. doi: 10.1007/BF01965196. DOI

John B. Meiosis. 3. Cambridge: Cambridge University Press; 1990.

Kim IS, Lee EH. Hybridization experiment of diploid–triploid cobitid fishes, Cobitis sinensis-longicorpus complex (Pisces: Cobitidae) Folia Zool. 2000;49:17–22.

Kato A, Vega JM, Han F, Lamb JC, Birchler JA. Advances in plant chromosome identification and cytogenetic techniques. Curr Opin Plant Biol. 2005;8:148–154. doi: 10.1016/j.pbi.2005.01.014. PubMed DOI

Král J, Musilová J, Št’áhlavský F, Řezáč M, Akan Z, Edwards RL, et al. Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spiders (Araneae: Araneomorphae) Chromosome Res. 2006;14:859–880. doi: 10.1007/s10577-006-1095-9. PubMed DOI

Lamatsch DK, Stöck M. Lost sex. Netherlands: Springer; 2009.

Morishima K, Yoshikawa H, Arai K. Meiotic hybridogenesis in triploid Misgurnus loach derived from a clonal lineage. Heredity. 2008;100:581–586. doi: 10.1038/hdy.2008.17. PubMed DOI

Neaves WB, Baumann P. Unisexual reproduction among vertebrates. Trends Genet. 2011;27:81–88. doi: 10.1016/j.tig.2010.12.002. PubMed DOI

Neusser M. Karyotypevolution, Genomorganisation und Zellkernarchitektur der Neuweltaffen (Doctoral dissertation, lmu) 2004.

Ogielska M, Bartmańska J. Development of testes and differentiation of germ cells in water frogs of the Rana esculenta-complex (Amphibia, Anura) Amphibia Reptilia. 1999;20:251–263. doi: 10.1163/156853899X00286. DOI

Ogielska M. Nucleus–like bodies in gonial cells of Rana esculenta [Amphibia, Anura] tadpoles-a putative way of chromosome elimination. Zool Pol. 1994;39:461–474.

Ohtani H. Mechanism of chromosome elimination in the hybridogenetic spermatogenesis of allotriploid males between Japanese and European water frogs. Chromosoma. 1993;102:158–162. doi: 10.1007/BF00387730. PubMed DOI

Plötner J, Köhler F, Uzzell T, Beerli P, Schreiber R, Guex GD, Hotz H. Evolution of serum albumin intron-1 is shaped by a 5’ truncated non–long terminal repeat retrotransposon in western Palearctic water frogs (Neobatrachia) Mol Phylogenet Evol. 2009;53:784–791. doi: 10.1016/j.ympev.2009.07.037. PubMed DOI PMC

Plötner J. Die westpaläarktischen Wasserfrösche: von Märtyrern der Wissenschaft zur biologischen Sensation. Germany: Laurenti; 2005.

Polls Pelaz M. Modes of gametogenesis among kleptons of the hybridogenetic water frog complex: an evolutionary synthesis. Zool Pol. 1994;39:123–138.

Ragghianti M, Bucci S, Marracci S, Casola C, Mancino G, Hotz H, et al. Gametogenesis of intergroup hybrids of hemiclonal frogs. Genet Res. 2007;89:39–45. doi: 10.1017/S0016672307008610. PubMed DOI

Reyer HU, Niederer B, Hettyey A. Variation in fertilisation abilities between hemiclonal hybrid and sexual parental males of sympatric water frogs (Rana lessonae, R. esculenta, R. ridibunda) Behav Ecol Sociobiol. 2003;54:274–284. doi: 10.1007/s00265-003-0635-y. DOI

Schmidt DJ, Bond NR, Adams M, Hughes JM. Cytonuclear evidence for hybridogenetic reproduction in natural populations of the Australian carp gudgeon (Hypseleotris: Eleotridae) Mol Ecol. 2011;20:3367–3380. doi: 10.1111/j.1365-294X.2011.05206.x. PubMed DOI

Schultz RJ. Hybridization, unisexuality, polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am Nat. 1969;103(934):605–19. doi: 10.1086/282629. DOI

Schultz R. Evolution ecology of unisexual fishes. Evol Biol. 1977;10:277–331.

Schurko AM, Neiman M, Logsdon JM. Signs of sex: what we know and how we know it. Trends Ecol Evolut. 2009;24:208–217. doi: 10.1016/j.tree.2008.11.010. PubMed DOI

Stenberg P, Saura A. Lost Sex. Netherlands: Springer; 2009. Cytology of asexual animals; pp. 63–74.

Stenberg P, Saura A. Meiosis and its deviations in polyploid animals. Cytogenet Genome Res. 2013;140:185–203. doi: 10.1159/000351731. PubMed DOI

Stöck M, Ustinova J, Betto-Colliard C, Schartl M, Moritz C, Perrin N. Simultaneous Mendelian and clonal genome transmission in a sexually reproducing, all–triploid vertebrate. Proc R Soc Lond B Biol Sci. 2011;279:1293–1299. doi: 10.1098/rspb.2011.1738. PubMed DOI PMC

Symonová R, Sember A, Majtánová Z, Ráb P. Characterization of Fish Genomes by GISH and CGH. In: Fish Cytogenetic Techniques: Ray-Fin Fishes and Chondrichthyans. USA: CRC Press; 2015. p. 118.

Traut W, Winking H. Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish and guppy. Chromosome Res. 2001;9:659–672. doi: 10.1023/A:1012956324417. PubMed DOI

Tunner H. Die klonale Struktur einer Wasserfröschpopulation. Z Zool Syst Evolut forsch. 1974;12:309–314. doi: 10.1111/j.1439-0469.1974.tb00173.x. DOI

Tunner H, Heppich S. Premeiotic genome exclusion during oogenesis in the common edible frog, Rana esculenta. Naturwissenschaften. 1981;68:207–208. doi: 10.1007/BF01047207. PubMed DOI

Tunner H, Heppich-Tunner S. Genom exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog. Naturwissenschaften. 1991;78:32–34. doi: 10.1007/BF01134041. DOI

Uzzell T, Berger L. Electrophoretic phenotypes of Rana ridibunda, Rana lessonae, and their hybridogenetic associate, Rana esculenta. Proc Acad Nat Sci Phila. 1975;127:13–24.

Uzzell T, Günther R, Berger L. Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia). Proc Acad Nat Sci Phila. 1977;128:147–171.

Uzzell T, Hotz H, Berger L. Genome exclusion in gametogenesis by an interspecific Rana hybrid: evidence from electrophoresis of individual oocytes. J Exp Zool. 1980;214:251–259. doi: 10.1002/jez.1402140303. DOI

Vinogradov AE, Borkin LJ, Günther R, Rosanov JM. Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry. Genome. 1990;33:619–627. doi: 10.1139/g90-092. PubMed DOI

Vinogradov AE, Borkin LJ, Günther R, Rosanov JM. Two germ cell lineages with genomes of different species in one and the same animal. Hereditas. 1991;114:245–251. doi: 10.1111/j.1601-5223.1991.tb00331.x. PubMed DOI

Vrijenhoek RC, Angus RA, Schultz RJ. Variation heterozygosity in sexually vs. clonally reproducing populations of Poeciliopsis. Evolution. 1977;31:767–781. doi: 10.2307/2407438. PubMed DOI

Zaleśna A, Choleva L, Ogielska M, Rábová M, Marec F, Ráb P. Evidence for integrity of parental genomes in the diploid hybridogenetic water frog Pelophylax esculentus by genomic in situ hybridization. Cytogenet Genome Res. 2011;134:206–212. doi: 10.1159/000327716. PubMed DOI

Zielinski ML, Scheid OM. Polyploidy and genome evolution. Berlin Heidelberg: Springer; 2012. Meiosis in polyploid plants; pp. 33–55.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Inheritance patterns of male asexuality in hybrid males of a water frog Pelophylax esculentus

. 2024 Sep 27 ; 14 (1) : 22221. [epub] 20240927

Cytogenetics of the Hybridogenetic Frog Pelophylax grafi and Its Parental Species Pelophylax perezi

. 2023 Dec 01 ; 15 (12) : .

Karyotypes of water frogs from the Pelophylax esculentus complex: results of cross-species chromosomal painting

. 2023 Nov ; 132 (4) : 329-342. [epub] 20231125

Chromosomes of Asian Cyprinid Fishes: Genomic Differences in Conserved Karyotypes of 'Poropuntiinae' (Teleostei, Cyprinidae)

. 2023 Apr 20 ; 13 (8) : . [epub] 20230420

Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus

. 2022 ; 10 () : 1008506. [epub] 20221014

The high diversity of gametogenic pathways in amphispermic water frog hybrids from Eastern Ukraine

. 2022 ; 10 () : e13957. [epub] 20220823

Uniparental Genome Elimination in Australian Carp Gudgeons

. 2021 Jun 08 ; 13 (6) : .

Capture and return of sexual genomes by hybridogenetic frogs provide clonal genome enrichment in a sexual species

. 2021 Jan 15 ; 11 (1) : 1633. [epub] 20210115

All-male hybrids of a tetrapod Pelophylax esculentus share its origin and genetics of maintenance

. 2018 Apr 02 ; 9 (1) : 13. [epub] 20180402

Sex Chromosome Evolution and Genomic Divergence in the Fish Hoplias malabaricus (Characiformes, Erythrinidae)

. 2018 ; 9 () : 71. [epub] 20180305

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...