Artificial whole genome duplication in paleopolyploid sturgeons yields highest documented chromosome number in vertebrates
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33184410
PubMed Central
PMC7665173
DOI
10.1038/s41598-020-76680-4
PII: 10.1038/s41598-020-76680-4
Knihovny.cz E-zdroje
- MeSH
- genetická zdatnost MeSH
- genom * MeSH
- karyotypizace veterinární MeSH
- meióza MeSH
- molekulární evoluce MeSH
- ohrožené druhy MeSH
- polyploidie MeSH
- ryby klasifikace genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Critically endangered sturgeons, having undergone three whole genome duplication events, represent an exceptional example of ploidy plasticity in vertebrates. Three extant ploidy groups, combined with autopolyploidization, interspecific hybridization and the fertility of hybrids are important issues in sturgeon conservation and aquaculture. Here we demonstrate that the sturgeon genome can undergo numerous alterations of ploidy without severe physiological consequences, producing progeny with a range of ploidy levels and extremely high chromosome numbers. Artificial suppression of the first mitotic division alone, or in combination with suppression of the second meiotic division of functionally tetraploid zygotes (4n, C-value = 4.15) of Siberian sturgeon Acipenser baerii and Russian sturgeon A. gueldenstaedtii resulted in progeny of various ploidy levels-diploid/hexaploid (2n/6n) mosaics, hexaploid, octoploid juveniles (8n), and dodecaploid (12n) larvae. Counts between 477 to 520 chromosomes in octoploid juveniles of both sturgeons confirmed the modal chromosome numbers of parental species had been doubled. This exceeds the highest previously documented chromosome count among vertebrates 2n ~ 446 in the cyprinid fish Ptychobarbus dipogon.
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Panchy N, Lehti-Shiu M, Shiu SH. Evolution of gene duplication in plants. Plant. Physiol. 2016;171:2294–2316. doi: 10.1104/pp.16.00523. PubMed DOI PMC
Mable BK, Alexandrou MA, Taylor MI. Genome duplication in amphibians and fish: an extended synthesis. J. Zool. 2011;284:151–182. doi: 10.1111/j.1469-7998.2011.00829.x. DOI
Comai L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 2005;6:836–846. doi: 10.1038/nrg1711. PubMed DOI
Ohno, S. Evolution by gene duplication. (Springer, New York, 1970).
Lynch, M. Genomics. Gene Duplication and Evolution. Science (New York, N.Y.) vol. 297 https://pubmed.ncbi.nlm.nih.gov/12169715/ (2002). PubMed
McLysaght A, Hokamp K, Wolfe KH. Extensive genomic duplication during early chordate evolution. Nat. Genet. 2002;31:200–204. doi: 10.1038/ng884. PubMed DOI
Venkatesh B. Evolution and diversity of fish genomes. Curr. Opin. Genet. Dev. 2003;13:588–592. doi: 10.1016/j.gde.2003.09.001. PubMed DOI
Hoegg S, Brinkmann H, Taylor JS, Meyer A. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J. Mol. Evol. 2004;59:190–203. doi: 10.1007/s00239-004-2613-z. PubMed DOI
Nelson, J. S., Grande, T. C. & Wilson, M. V. H. Fishes of the World. (Wiley, Hoboken, 2016).
Šlechtová V, Bohlen J, Freyhof J, Ráb P. Molecular phylogeny of the Southeast Asian freshwater fish family Botiidae (Teleostei: Cobitoidea) and the origin of polyploidy in their evolution. Mol. Phylogenet. Evol. 2006;39:529–541. doi: 10.1016/j.ympev.2005.09.018. PubMed DOI
Uyeno, T. & Smith, G. Tetraploid origin of karyotype of Catostomid fishes. Science175, 644– (1972). PubMed
David L, Blum S, Feldman MW, Lavi U, Hillel J. Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol. Biol. Evol. 2003;20:1425–1434. doi: 10.1093/molbev/msg173. PubMed DOI
Yang L, et al. Phylogeny and polyploidy: resolving the classification of cyprinine fishes (Teleostei: Cypriniformes) Mol. Phylogenet. Evol. 2015;85:97–116. doi: 10.1016/j.ympev.2015.01.014. PubMed DOI
Alexandrou MA, et al. Competition and phylogeny determine community structure in Müllerian co-mimics. Nature. 2011;469:84–88. doi: 10.1038/nature09660. PubMed DOI
Macqueen DJ, Johnston IA. A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc. R. Soc. B. 2014;281:20132881. doi: 10.1098/rspb.2013.2881. PubMed DOI PMC
Mank JE, Avise JC. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica. 2006;127:321–327. doi: 10.1007/s10709-005-5248-0. PubMed DOI
Arai, R. Fish karyotypes: a check list. (Springer, New York, 2011).
Yu X, Yu X. A schizothoracine fish species diptychus dipogon with a very high number of chromosomes. Chromosome Inf. Service. 1990;48:17–18.
Froschauer A, Braasch I, Volff JN. Fish genomes, comparative genomics and vertebrate evolution. Curr. Genomics. 2006;7:43–57. doi: 10.2174/138920206776389766. DOI
Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH. Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics. 2011;188:799–808. doi: 10.1534/genetics.111.127324. PubMed DOI PMC
Sallan LC. Major issues in the origins of ray-finned fish (Actinopterygii) biodiversity. Biol. Rev. 2014;89:950–971. doi: 10.1111/brv.12086. PubMed DOI
Havelka M, Kašpar V, Hulák M, Flajšhans M. Sturgeon genetics and cytogenetics: a review related to ploidy levels and interspecific hybridization. Folia Zool. 2011 doi: 10.25225/fozo.v60.i2.a3.2011. DOI
Symonová R, et al. Genome compositional organization in gars shows more similarities to mammals than to other ray-finned fish. J. Exp. Zool. B Mol. Dev. Evol. 2017;328:607–619. doi: 10.1002/jez.b.22719. PubMed DOI
Ludwig A, Belfiore NM, Pitra C, Svirsky V, Jenneckens I. Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus) Genetics. 2001;158:1203–1215. PubMed PMC
Peng Z, et al. Age and biogeography of major clades in sturgeons and paddlefishes (Pisces : Acipenseriformes) Mol. Phylogenet. Evol. 2007;42:854–862. doi: 10.1016/j.ympev.2006.09.008. PubMed DOI
Dingerkus G, Howell WM. Karyotypic analysis and evidence of tetraploidy in the North American paddlefish, Polyodon spathula. Science. 1976;194:842–844. doi: 10.1126/science.982045. PubMed DOI
Birstein VJ, Vasiliev VP. Tetraploid-octoploid relationships and karyological evolution in the order Acipenseriformes (Pisces) karyotypes, nucleoli, and nucleolus-organizer regions in four acipenserid species. Genetica. 1987;72:3–12. doi: 10.1007/BF00126973. DOI
Du K, et al. The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization. Nat. Ecol. Evol. 2020;4:841–852. doi: 10.1038/s41559-020-1166-x. PubMed DOI PMC
Kim DS, Nam YK, Noh JK, Park CH, Chapman FA. Karyotype of North American shortnose sturgeon Acipenser brevirostrum with the highest chromosome number in the Acipenseriformes. Icht. Res. 2004 doi: 10.1007/s10228-004-0257-z. DOI
Fontana F, et al. Evidence of hexaploid karyotype in shortnose sturgeon. Genome. 2008;51:113–119. doi: 10.1139/G07-112. PubMed DOI
Birstein VJ, Hanner R, DeSalle R. Phylogeny of the Acipenseriformes: cytogenetic and molecular approaches. Environ. Biol. Fishes. 1997;48:127–155. doi: 10.1023/A:1007366100353. DOI
Vasil’ev, V. P. Mechanisms of polyploid evolution in fish: polyploidy in sturgeons. in Biology, Conservation and Sustainable Development of Sturgeons (eds. Carmona, R. et al.) 97–117 (Springer Netherlands, 2009). doi:10.1007/978-1-4020-8437-9_6.
Majtánová Z, Symonová R, Arias-Rodriguez L, Sallan L, Ráb P. ‘Holostei versus Halecostomi’ problem: Insight from cytogenetics of ancient nonteleost actinopterygian fish, bowfin Amia calva. J. Exp. Zool. B Mol. Dev. Evol. 2017;328:620–628. doi: 10.1002/jez.b.22720. PubMed DOI
Fontana, F., Zane, L., Pepe, A. & Congiu, L. Polyploidy in Acipenseriformes: cytogenetic and molecular approaches. in Fish Cytogen. (eds. Pisano, E., Ozouf-Costaz, C., Foresti, F. & Kapoor, B. G.) 385–403 (Science Publisher, 2007).
Vasil’eva, E. D., Vasil’ev, V. P., Ponomareva, E. N. & Lapukhin, Yu. A. Triple hybrids obtained by artificial hybridization of the Russian sturgeon Acipenser gueldenstaedtii with the hybrid of the starred sturgeon A stellatus and the great sturgeon A. huso (Acipenseridae): The kind of inheritance of some morphological characters and fertility of the parental hybrid form. J. Ichthyol.50, 605–617 (2010).
Omoto N, Maebayashi M, Adachi S, Arai K, Yamauchi K. The influence of oocyte maturational stage on hatching and triploidy rates in hybrid (bester) sturgeon, Huso huso×Acipneser ruthenus. Aquaculture. 2005;245:287–294. doi: 10.1016/j.aquaculture.2004.11.008. DOI
Schreier AD, Gille D, Mahardja B, May B. Neutral markers confirm the octoploid origin and reveal spontaneous autopolyploidy in white sturgeon, Acipenser transmontanus. J. Appl. Ichthyol. 2011;27:24–33. doi: 10.1111/j.1439-0426.2011.01873.x. DOI
Zhou H, Fujimoto T, Adachi S, Yamaha E, Arai K. Genome size variation estimated by flow cytometry in Acipenser mikadoi, Huso dauricus in relation to other species of Acipenseriformes. J. Appl. Ichthyol. 2011;27:484–491. doi: 10.1111/j.1439-0426.2010.01648.x. DOI
Zhou H, et al. Molecular cytogenetic study on the ploidy status in Acipenser mikadoi. J. Appl. Ichthyol. 2013;29:51–55. doi: 10.1111/jai.12109. DOI
Schreier AD, Mahardja B, May B. Patterns of population structure vary across the range of the white sturgeon. Trans. Am. Fish. Soc. 2013;142:1273–1286. doi: 10.1080/00028487.2013.788554. DOI
Havelka M, et al. Fertility of a spontaneous hexaploid male Siberian sturgeon, Acipenser baerii. BMC Genet. 2014;15:5. doi: 10.1186/1471-2156-15-5. PubMed DOI PMC
Gille DA, Famula TR, May BP, Schreier A. Evidence for a maternal origin of spontaneous autopolyploidy in cultured white sturgeon (Acipenser transmontanus). 2015 doi: 10.1016/j.aquaculture.2014.10.002. DOI
Havelka M, Hulák M, Rodina M, Flajšhans M. First evidence of autotriploidization in sterlet (Acipenser ruthenus) J. Appl. Genetics. 2013;54:201–207. doi: 10.1007/s13353-013-0143-3. PubMed DOI
Van Eenennaam JP, et al. Mechanical shock during egg de-adhesion and post-ovulatory ageing contribute to spontaneous autopolyploidy in white sturgeon culture (Acipensertransmontanus) Aquaculture. 2020;515:734530. doi: 10.1016/j.aquaculture.2019.734530. DOI
Bytyutskyy D, Srp J, Flajšhans M. Use of Feulgen image analysis densitometry to study the effect of genome size on nuclear size in polyploid sturgeons. J. Appl. Ichthyol. 2012;28:704–708. doi: 10.1111/j.1439-0426.2012.02021.x. DOI
Symonová, R. et al. Sturgeons are pretty polyploid: hybrid and ploidy diversity in sturgeons. in Book of Abstracts KN1 pp 13 (2010).
Havelka M, Bytyutskyy D, Symonová R, Ráb P, Flajšhans M. The second highest chromosome count among vertebrates is observed in cultured sturgeon and is associated with genome plasticity. Genet. Select. Evol. 2016;48:12. doi: 10.1186/s12711-016-0194-0. PubMed DOI PMC
Linhartová Z, Havelka M, Pšenička M, Flajšhans M. Interspecific hybridization of sturgeon species affects differently their gonadal development. Czech J. Anim. Sci. 2017;63(2018):1–10.
Shivaramu S, et al. Influence of interspecific hybridization on fitness-related traits in Siberian sturgeon and Russian sturgeon. Czech J. Anim. Sci. 2019;64(2019):78–88. doi: 10.17221/165/2018-CJAS. DOI
IUCN. The IUCN Red List of Threatened Species. (2020).
Pikitch EK, Doukakis P, Lauck L, Chakrabarty P, Erickson DL. Status, trends and management of sturgeon and paddlefish fisheries. Fish Fish. 2005;6:233–265. doi: 10.1111/j.1467-2979.2005.00190.x. DOI
Bronzi P, Rosenthal H. Present and future sturgeon and caviar production and marketing: a global market overview. J. Appl. Ichthyol. 2014;30:1536–1546. doi: 10.1111/jai.12628. DOI
Bronzi P, Rosenthal H, Gessner J. Global sturgeon aquaculture production: an overview. J. Appl. Ichthyol. 2011;27:169–175. doi: 10.1111/j.1439-0426.2011.01757.x. DOI
Lebeda I, Flajshans M. Technical note: production of tetraploid sturgeons. J. Anim. Sci. 2015;93:3759–3764. doi: 10.2527/jas.2015-9094. PubMed DOI
Fontana F. Chromosomal nucleolar organizer regions in four sturgeon species as markers of karyotype evolution in Acipenseriformes (Pisces) Genome. 1994;37:888–892. doi: 10.1139/g94-126. PubMed DOI
Hardie DC, Hebert PDN. The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes. Genome. 2003;46:683–706. doi: 10.1139/g03-040. PubMed DOI
Piferrer F, et al. Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture. 2009;293:125–156. doi: 10.1016/j.aquaculture.2009.04.036. DOI
Arai, K. & Fujimoto, T. Chromosome manipulation techniques and applications to aquaculture. in Sex Control in Aquaculture 137–162 (Wiley, Hoboken, 2018). doi:10.1002/9781119127291.ch6.
Havelka, M. & Arai, K. Hybridization and polyploidization in sturgeon. in Sex Control in Aquaculture 669–687 (Wiley, Hoboken, 2018). doi:10.1002/9781119127291.ch34.
Yin, F. et al. CRISPR/Cas9 Application for gene copy fate survey of polyploid vertebrates. Front. Genet.9, (2018). PubMed PMC
Heier J, Takle KA, Hasley AO, Pelegri F. Ploidy manipulation and induction of alternate cleavage patterns through inhibition of centrosome duplication in the early zebrafish embryo. Develop. Dynam. 2015;244:1300–1312. doi: 10.1002/dvdy.24315. PubMed DOI PMC
Yabe T, Ge X, Pelegri F. The zebrafish maternal-effect gene cellular atoll encodes the centriolar component sas-6 and defects in its paternal function promote whole genome duplication. Develop. Biol. 2007;312:44–60. doi: 10.1016/j.ydbio.2007.08.054. PubMed DOI PMC
Dettlaff, T. A., Ginsburg, A. S. & Schmalhausen, O. I. Embryonic development. in Sturgeon Fishes: Developmental Biology and Aquaculture (eds. Dettlaff, T. A., Ginsburg, A. S. & Schmalhausen, O. I.) 49–154 (Springer, New York, 1993). doi:10.1007/978-3-642-77057-9_3.
Blacklidge KH, Bidwell CA. Three ploidy levels indicated by genome quantification in Acipenseriformes of North America. J. Hered. 1993;84:427–430. doi: 10.1093/oxfordjournals.jhered.a111367. DOI
Wurster DH, Atkin NB. Muntjac chromosomes: a new karyotype for Muntiacus muntjak. Experientia. 1972;28:972–973. doi: 10.1007/BF01924980. DOI
Wurster DH, Benirschke K. Indian momtjac, Muntiacus muntiak: A deer with a low diploid chromosome number. Science. 1970;168:1364–1366. doi: 10.1126/science.168.3937.1364. PubMed DOI
Gallardo MH, González CA, Cebrián I. Molecular cytogenetics and allotetraploidy in the red vizcacha rat, Tympanoctomys barrerae (Rodentia, Octodontidae) Genomics. 2006;88:214–221. doi: 10.1016/j.ygeno.2006.02.010. PubMed DOI
Schmid M, Fernández-Badillo A, Feichtinger W, Steinlein C, Roman JI. On the highest chromosome number in mammals. Cytogenet. Cell Genet. 1988;49:305–308. doi: 10.1159/000132683. PubMed DOI
Nishida C, et al. Characterization of chromosome structures of Falconinae (Falconidae, Falconiformes, Aves) by chromosome painting and delineation of chromosome rearrangements during their differentiation. Chromosome Res. 2008;16:171–181. doi: 10.1007/s10577-007-1210-6. PubMed DOI
Bian, X. & Li, Q. Studies on The karyotypes of birds V. The 20 species of Climber birds.(Aves). zr10, 309–317 (1989).
Masabanda JS, et al. Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics. 2004;166:1367–1373. doi: 10.1534/genetics.166.3.1367. PubMed DOI PMC
Olmo E. Rate of chromosome changes and spe ciation in reptiles. Genetica. 2005;125:185–203. doi: 10.1007/s10709-005-8008-2. PubMed DOI
Gela, D., Rodina, M. & Linhart, O. Artificial reproduction of sturgeon (Acipenseridae). in Edice Metodik pp 24 (2008).
Lebeda I, Dzyuba B, Rodina M, Flajshans M. Optimization of sperm irradiation protocol for induced gynogenesis in Siberian sturgeon, Acipenser baerii. Aquacult. Int. 2014;22:485–495. doi: 10.1007/s10499-013-9658-1. DOI
Völker, M. & Ráb, P. Direct chromosome preparation from regenerating fin tissue. in Fish Cytogenetic Techniques (eds. Ozouf-Costaz, C., Pisano, E., Foresti, F. & Foresti de Almeida-Toledo, L.) 37–41 (CRC Press, Boca Raton, 2015).