Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp

. 2022 Jul 14 ; 13 (1) : 4092. [epub] 20220714

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35835759
Odkazy

PubMed 35835759
PubMed Central PMC9283417
DOI 10.1038/s41467-022-31515-w
PII: 10.1038/s41467-022-31515-w
Knihovny.cz E-zdroje

Understanding genome evolution of polyploids requires dissection of their often highly similar subgenomes and haplotypes. Polyploid animal genome assemblies so far restricted homologous chromosomes to a 'collapsed' representation. Here, we sequenced the genome of the asexual Prussian carp, which is a close relative of the goldfish, and present a haplotype-resolved chromosome-scale assembly of a hexaploid animal. Genome-wide comparisons of the 150 chromosomes with those of two ancestral diploid cyprinids and the allotetraploid goldfish and common carp revealed the genomic structure, phylogeny and genome duplication history of its genome. It consists of 25 syntenic, homeologous chromosome groups and evolved by a recent autoploid addition to an allotetraploid ancestor. We show that de-polyploidization of the alloploid subgenomes on the individual gene level occurred in an equilibrated fashion. Analysis of the highly conserved actinopterygian gene set uncovered a subgenome dominance in duplicate gene loss of one ancestral chromosome set.

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DeVries H. The coefficient of mutation in Oenothera biennis L. Botanical Gaz. 1915;59:169–196.

Blakeslee AF. Types of mutations and their possible significance in evolution. Am. Naturalist. 1921;55:254–267.

Van de Peer Y, Mizrachi E, Marchal K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 2017;18:411–424. PubMed

Muller HJ. Why polyploidy is rarer in animals than in plants. Am. Naturalist. 1925;59:346–353.

Orr HA. Why polyploidy is rarer in animals than in plants revisited. Am. Naturalist. 1990;136:759–770.

Mable BK. ‘Why polyploidy is rarer in animals than in plants’: myths and mechanisms. Biol. J. Linn. Soc. 2004;82:453–466.

Stöck, M. et al. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum’. Philos. T. R. Soc. B376, 10.1098/rstb.2020.0103 (2021). PubMed PMC

Stöck M, Lamatsch DK. Why comparing polyploidy research in animals and plants. Cytogenet. Genome Res. 2013;140:75–78. PubMed

Lamatsch, D. K. & Stöck, M. In Lost Sex. Lost Sex: The Evolutionary Biology of Parthenogenesis 399–432 (Springer, 2009).

Zhou L, Gui J. Natural and artificial polyploids in aquaculture. Aquac. Fish. 2017;2:103–111.

Kalous L, Bohlen J, Rylková K, Petrtýl M. Hidden diversity within the Prussian carp and designation of a neotype for Carassius gibelio (Teleostei: Cyprinidae) Ichthyol. Explor. Freshw. 2012;23:11–18.

Chen D, et al. The evolutionary origin and domestication history of goldfish (Carassius auratus) Proc. Natl. Acad. Sci. USA. 2020;117:29775–29785. PubMed PMC

Kon T, et al. The genetic basis of morphological diversity in domesticated goldfish. Curr. Biol. 2020;30:2260–2274.e2266. PubMed

Xu P, et al. Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat. Genet. 2014;46:1212–1219. PubMed

Rylková K, Kalous L, Bohlen J, Lamatsch DK, Petrtýl M. Phylogeny and biogeographic history of the cyprinid fish genus Carassius (Teleostei: Cyprinidae) with focus on natural and anthropogenic arrivals in Europe. Aquaculture. 2013;380-383:13–20.

van der Veer G, Nentwig W. Environmental and economic impact assessment of alien and invasive fish species in Europe using the generic impact scoring system. Ecol. Freshw. Fish. 2015;24:646–656.

Penáz, M., Rab, P. & Prokes, M. Cytological Analysis, Gynogenesis and Early Development of Carassius auratus gibelio (Academia, 1979).

Mishina T, et al. Interploidy gene flow involving the sexual-asexual cycle facilitates the diversification of gynogenetic triploid Carassius fish. Sci. Rep. 2021;11:1–12. PubMed PMC

Ding M, et al. Genomic anatomy of male-specific microchromosomes in a gynogenetic fish. PLoS Genet. 2021;17:e1009760. PubMed PMC

Knytl M, Kalous L, Symonová R, Rylková K, Ráb P. Chromosome studies of European cyprinid fishes: cross-species painting reveals natural allotetraploid origin of a Carassius female with 206 chromosomes. Cytogenet. Genome Res. 2013;139:276–283. PubMed

Yang L, Yang S-T, Wei X-H, Gui J-F. Genetic diversity among different clones of the Gynogenetic Silver Crucian Carp, Carassius auratus gibelio, revealed by Transferrin and Isozyme Markers. Biochem. Genet. 2001;39:213225. PubMed

Luo J, et al. From asymmetrical to balanced genomic diversification during rediploidization: subgenomic evolution in allotetraploid fish. Sci. Adv. 2020;6:eaaz7677. PubMed PMC

Session AM, et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature. 2016;538:336–343. PubMed PMC

Du K, et al. The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization. Nat. Ecol. Evol. 2020;4:841–852. PubMed PMC

Wen M, et al. Sex chromosome and sex locus characterization in goldfish, Carassius auratus (Linnaeus, 1758) BMC Genomics. 2020;21:552. PubMed PMC

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. PubMed

Li X-Y, et al. Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp. Mol. Phylogenet. Evol. 2014;78:96–104. PubMed

Mendiburu AO, Peloquin S. Sexual polyploidization and depolyploidization: some terminology and definitions. Theor. Appl. Genet. 1976;48:137143. PubMed

Xu P, et al. The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio. Nat. Commun. 2019;10:4625. PubMed PMC

Li J-T, et al. Parallel subgenome structure and divergent expression evolution of allo-tetraploid common carp and goldfish. Nat. Genet. 2021;53:1493–1503. PubMed PMC

Bohutínská, M. et al. Genomic novelty versus convergence in the basis of adaptation to whole genome duplication. bioRxiv, 10.1101/2020.01.31.929109 (2020).

Chen Z, et al. De novo assembly of the goldfish (Carassius auratus) genome and the evolution of genes after whole-genome duplication. Sci. Adv. 2019;5:eaav0547. PubMed PMC

Walkowiak S, et al. Multiple wheat genomes reveal global variation in modern breeding. Nature. 2020;588:277–283. PubMed PMC

Scott MF, et al. Limited haplotype diversity underlies polygenic trait architecture across 70 years of wheat breeding. Genome Biol. 2021;22:137. PubMed PMC

Hu Y, et al. Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat. Genet. 2019;51:739–748. PubMed

Zhang J, et al. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat. Genet. 2018;50:1565–1573. PubMed

Krasileva KV, et al. Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biol. 2013;14:R66. PubMed PMC

Sato, K. et al. Chromosome-scale genome assembly of the transformation-amenable common wheat cultivar ‘Fielder’. DNA Res.28, 10.1093/dnares/dsab008 (2021). PubMed PMC

Rhie A, et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature. 2021;592:737–746. PubMed PMC

Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 2017;34:1812–1819. PubMed

Martin AP, Palumbi SR. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl Acad. Sci. USA. 1993;90:4087–4091. PubMed PMC

Fasano C, et al. Transcriptome and metabolome of synthetic Solanum autotetraploids reveal key genomic stress events following polyploidization. New Phytol. 2016;210:1382–1394. PubMed

Comai L, Madlung A, Josefsson C, Tyagi A. Do the different parental ‘heteromes’ cause genomic shock in newly formed allopolyploids? Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci. 2003;358:1149–1155. PubMed PMC

Cheng F, et al. Gene retention, fractionation and subgenome differences in polyploid plants. Nat. Plants. 2018;4:258–268. PubMed

Alger EI, Edger PP. One subgenome to rule them all: underlying mechanisms of subgenome dominance. Curr. Opin. Plant Biol. 2020;54:108–113. PubMed

De Smet R, et al. Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc. Natl Acad. Sci. USA. 2013;110:2898–2903. PubMed PMC

Pikaard CS. Nucleolar dominance and silencing of transcription. Trends Plant Sci. 1999;4:478–483. PubMed

Lynch M, Conery J, Bürger R. Mutational meltdowns in sexual populations. Evolution. 1995;49:1067–1080. PubMed

Dubcovsky J, Dvorak J. Genome plasticity a key factor in the success of polyploid wheat under domestication. Science. 2007;316:1862–1866. PubMed PMC

Baniaga AE, Marx HE, Arrigo N, Barker MS. Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives. Ecol. Lett. 2020;23:68–78. PubMed

Ficetola GF, Stöck M. Do hybrid‐origin polyploid amphibians occupy transgressive or intermediate ecological niches compared to their diploid ancestors? J. Biogeogr. 2016;43:703–715.

Zhang J, et al. Meiosis completion and various sperm responses lead to unisexual and sexual reproduction modes in one clone of polyploid Carassius gibelio. Sci. Rep. 2015;5:10898. PubMed PMC

Lamatsch DK, Steinlein C, Schmid M, Schartl M. Noninvasive determination of genome size and ploidy level in fishes by flow cytometry: detection of triploid Poecilia formosa. Cytometry. 2000;39:91–95. PubMed

Alemán, J. L. F. & Oufaska, Y. In Proceedings of the Fifteenth Annual Conference on Innovation and Technology in Computer Science Education 68–72 (Association for Computing Machinery, Bilkent, 2010).

Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013;30:923–930. PubMed

R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2013).

Villanueva, R. A. M. & Chen, Z. J. ggplot2: Elegant Graphics for Data Analysis (2nd edn), Measurement: Interdisciplinary Research and Perspectives, 17, 160–167 (Routledge, 2019).

Warnes, G. R. et al. gplots: Various R Programming Tools for Plotting Data. R Package Version, 2 (Science Open, 2009).

Cheng H, Concepcion GT, Feng X, Zhang H, Li H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat. Methods. 2021;18:170–175. PubMed PMC

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–3100. PubMed PMC

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. PubMed PMC

Durand NC, et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016;3:95–98. PubMed PMC

Dudchenko O, et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017;356:92–95. PubMed PMC

Robinson JT, et al. Juicebox. js provides a cloud-based visualization system for Hi-C data. Cell Syst. 2018;6:256–258.e251. PubMed PMC

Li H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics. 2016;32:2103–2110. PubMed PMC

Kuhl H, et al. CSA: a high-throughput chromosome-scale assembly pipeline for vertebrate genomes. GigaScience. 2020;9:giaa034. PubMed PMC

Sun L, et al. Chromosome-level genome assembly of a cyprinid fish Onychostoma macrolepis by integration of nanopore sequencing, Bionano and Hi-C technology. Mol. Ecol. Resour. 2020;20:1361–1371. PubMed

Kiełbasa SM, Wan R, Sato K, Horton P, Frith MC. Adaptive seeds tame genomic sequence comparison. Genome Res. 2011;21:487–493. PubMed PMC

Frith MC, Kawaguchi R. Split-alignment of genomes finds orthologies more accurately. Genome Biol. 2015;16:106. PubMed PMC

Blanchette M, et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 2004;14:708–715. PubMed PMC

Minh BQ, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 2020;37:1530–1534. PubMed PMC

Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D. Evolution’s cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl Acad. Sci. USA. 2003;100:1148411489. PubMed PMC

Sharma V, Hiller M. Increased alignment sensitivity improves the usage of genome alignments for comparative gene annotation. Nucleic Acids Res. 2017;45:8369–8377. PubMed PMC

Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-3.0. 1996-2010 http://www.repeatmasker.org (2015).

Smit, A. F. A. & Hubley, R. RepeatModeler Open-1.0. 2008-2015 http://www.repeatmasker.org (2008).

Iwata H, Gotoh O. Benchmarking spliced alignment programs including Spaln2, an extended version of Spaln that incorporates additional species-specific features. Nucleic Acids Res. 2012;40:e161–e161. PubMed PMC

Birney E, Clamp M, Durbin R. GeneWise and genomewise. Genome Res. 2004;14:988–995. PubMed PMC

She R, Chu JS-C, Wang K, Pei J, Chen N. GenBlastA: enabling BLAST to identify homologous gene sequences. Genome Res. 2009;19:143–149. PubMed PMC

Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–i890. PubMed PMC

Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods. 2015;12:357–360. PubMed PMC

Pertea M, et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 2015;33:290–295. PubMed PMC

Stanke M, et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006;34:W435–W439. PubMed PMC

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–3212. PubMed

Camacho C, et al. BLAST+: architecture and applications. BMC Bioinforma. 2009;10:1–9. PubMed PMC

Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat. Methods. 2015;12:59–60. PubMed

Chan, P. P. & Lowe, T. M. In Gene Prediction, Methods and Protocols. Methods in Molecular Biology 1962 1–14 (Springer, 2019). PubMed

Lagesen K, et al. RNammer: consistent annotation of rRNA genes in genomic sequences. Nucleic Acids Res. 2007;35:3100–3108. PubMed PMC

Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29:2933–2935. PubMed PMC

Kalvari I, et al. Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res. 2018;46:D335–D342. PubMed PMC

Kuhn RM, Haussler D, Kent WJ. The UCSC genome browser and associated tools. Brief. Bioinforma. 2013;14:144–161. PubMed PMC

Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002;12:656664. PubMed PMC

Katoh K, Toh H. Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics. 2010;26:1899–1900. PubMed PMC

Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34:W609–W612. PubMed PMC

Yang, Z. User guide PAML: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol.3, 10.1093/molbev/msm088 (2009). PubMed

Wang Y, et al. The draft genome of the grass carp (Ctenopharyngodon idellus) provides insights into its evolution and vegetarian adaptation. Nat. Genet. 2015;47:625–631. PubMed

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