Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements

. 2018 Oct 12 ; 9 (1) : 4242. [epub] 20181012

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30315196

Grantová podpora
648143 EC | European Research Council (ERC) - International

Odkazy

PubMed 30315196
PubMed Central PMC6185902
DOI 10.1038/s41467-018-06562-x
PII: 10.1038/s41467-018-06562-x
Knihovny.cz E-zdroje

Meiotic drive is widespread in nature. The conflict it generates is expected to be an important motor for evolutionary change and innovation. In this study, we investigated the genomic consequences of two large multi-gene meiotic drive elements, Sk-2 and Sk-3, found in the filamentous ascomycete Neurospora intermedia. Using long-read sequencing, we generated the first complete and well-annotated genome assemblies of large, highly diverged, non-recombining regions associated with meiotic drive elements. Phylogenetic analysis shows that, even though Sk-2 and Sk-3 are located in the same chromosomal region, they do not form sister clades, suggesting independent origins or at least a long evolutionary separation. We conclude that they have in a convergent manner accumulated similar patterns of tandem inversions and dense repeat clusters, presumably in response to similar needs to create linkage between genes causing drive and resistance.

Zobrazit více v PubMed

Burt, A. & Trivers, R. Genes in Conflict: The Biology of Selfish Genetic Elements (Harvard University Press, Cambridge, MA, 2009).

Werren JH. Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc. Natl. Acad. Sci. USA. 2011;108:10863–10870. doi: 10.1073/pnas.1102343108. PubMed DOI PMC

Rice WR. Nothing in genetics makes sense except in light of genomic conflict. Annu. Rev. Ecol. Evol. Syst. 2013;44:217–237. doi: 10.1146/annurev-ecolsys-110411-160242. DOI

Sandler L, Novitski E. Meiotic drive as an evolutionary force. Am. Nat. 1957;91:105–110. doi: 10.1086/281969. DOI

Lindholm AK, et al. The ecology and evolutionary dynamics of meiotic drive. Trends Ecol. Evol. 2016;31:315–326. doi: 10.1016/j.tree.2016.02.001. PubMed DOI

Lyttle TW. Segregation distorters. Annu. Rev. Genet. 1991;25:511–581. doi: 10.1146/annurev.ge.25.120191.002455. PubMed DOI

Larracuente AM, Presgraves DC. The selfish segregation distorter gene complex of Drosophila melanogaster. Genetics. 2012;192:33–53. doi: 10.1534/genetics.112.141390. PubMed DOI PMC

Kelemen RK, Vicoso B. Complex history and differentiation patterns of the t-haplotype, a mouse meiotic driver. Genetics. 2018;208:365–375. doi: 10.1534/genetics.117.300513. PubMed DOI PMC

Jaenike J. Sex chromosome meiotic drive. Annu. Rev. Ecol. Syst. 2001;32:25–49. doi: 10.1146/annurev.ecolsys.32.081501.113958. DOI

Wang J, et al. A Y-like social chromosome causes alternative colony organization in fire ants. Nature. 2013;493:664–668. doi: 10.1038/nature11832. PubMed DOI

Branco S, et al. Multiple convergent supergene evolution events in mating-type chromosomes. Nat. Commun. 2018;9:2000. doi: 10.1038/s41467-018-04380-9. PubMed DOI PMC

Bachtrog D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 2013;14:113–124. doi: 10.1038/nrg3366. PubMed DOI PMC

Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993;134:1289–1303. PubMed PMC

Corcoran P, et al. Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma. Genome Res. 2016;26:486–498. doi: 10.1101/gr.197244.115. PubMed DOI PMC

Whittle CA, Sun Y, Johannesson H. Degeneration in codon usage within the region of suppressed recombination in the mating-type chromosomes of Neurospora tetrasperma. Eukaryot. Cell. 2011;10:594–603. doi: 10.1128/EC.00284-10. PubMed DOI PMC

Fontanillas E, et al. Degeneration of the nonrecombining regions in the mating-type chromosomes of the anther-smut fungi. Mol. Biol. Evol. 2015;32:928–943. doi: 10.1093/molbev/msu396. PubMed DOI PMC

Artzt K. Gene mapping within the T/t complex of the mouse. III: t-lethal genes are arranged in three clusters on chromosome 17. Cell. 1984;39:565–572. doi: 10.1016/0092-8674(84)90463-X. PubMed DOI

Didion JP, et al. A multi-megabase copy number gain causes maternal transmission ratio distortion on mouse chromosome 2. PLoS Genet. 2015;11:e1004850. doi: 10.1371/journal.pgen.1004850. PubMed DOI PMC

Brand CL, Larracuente AM, Presgraves DC. Origin, evolution, and population genetics of the selfish Segregation Distorter gene duplication in European and African populations of Drosophila melanogaster. Evolution. 2015;69:1271–1283. doi: 10.1111/evo.12658. PubMed DOI PMC

Dyer KA, Charlesworth B, Jaenike J. Chromosome-wide linkage disequilibrium as a consequence of meiotic drive. Proc. Natl. Acad. Sci. 2007;104:1587–1592. doi: 10.1073/pnas.0605578104. PubMed DOI PMC

Pieper KE, Dyer KA. Occasional recombination of a selfish X-chromosome may permit its persistence at high frequencies in the wild. J. Evol. Biol. 2016;29:2229–2241. doi: 10.1111/jeb.12948. PubMed DOI PMC

Dalstra HJP, Swart K, Debets AJM, Saupe SJ, Hoekstra RF. Sexual transmission of the [Het-s] prion leads to meiotic drive in Podospora anserina. Proc. Natl. Acad. Sci. 2003;100:6616–6621. doi: 10.1073/pnas.1030058100. PubMed DOI PMC

Grognet P, Lalucque H, Malagnac F, Silar P. Genes that bias Mendelian segregation. PLoS Genet. 2014;10:e1004387. doi: 10.1371/journal.pgen.1004387. PubMed DOI PMC

Nuckolls NL, et al. wtf genes are prolific dual poison-antidote meiotic drivers. eLife. 2017;6:e26033. doi: 10.7554/eLife.26033. PubMed DOI PMC

Hu W, et al. A large gene family in fission yeast encodes spore killers that subvert Mendel’s law. eLife. 2017;6:e26057. doi: 10.7554/eLife.26057. PubMed DOI PMC

Turner BC, Perkins DD. Spore killer, a chromosomal factor in neurospora that kills meiotic products not containing it. Genetics. 1979;93:587–606. PubMed PMC

Campbell JL, Turner BC. Recombination block in the spore killer region of Neurospora. Genome. 1987;29:129–135. doi: 10.1139/g87-022. PubMed DOI

Harvey AM, et al. A critical component of meiotic drive in Neurospora is located near a chromosome rearrangement. Genetics. 2014;197:1165–1174. doi: 10.1534/genetics.114.167007. PubMed DOI PMC

Rhoades, N. A. et al. Identification of a genetic element required for spore killing in Neurospora. Preprint at https://www.biorxiv.org/content/early/2018/08/29/404004 (2018).

Hammond TM, Rehard DG, Xiao H, Shiu PKT. Molecular dissection of Neurospora spore killer meiotic drive elements. Proc. Natl. Acad. Sci. USA. 2012;109:12093–12098. doi: 10.1073/pnas.1203267109. PubMed DOI PMC

Corcoran P, et al. A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system. Mol. Phylogenet. Evol. 2014;78:136–147. doi: 10.1016/j.ympev.2014.05.007. PubMed DOI

Sun Y, Svedberg J, Hiltunen M, Corcoran P, Johannesson H. Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma. Nat. Commun. 2017;8:1140. doi: 10.1038/s41467-017-01317-6. PubMed DOI PMC

Galagan JE, et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature. 2003;422:859–868. doi: 10.1038/nature01554. PubMed DOI

Rountree, M. R. & Selker, E. U. in Epigenomics (eds Ferguson-Smith, A. C., Greally, J. M. & Martienssen, R. A.) 321–341 (Springer, Dordrecht, 2009).

Galagan JE, Selker EU. RIP: the evolutionary cost of genome defense. Trends Genet. 2004;20:417–423. doi: 10.1016/j.tig.2004.07.007. PubMed DOI

Lewis ZA, et al. Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res. 2009;19:427–437. doi: 10.1101/gr.086231.108. PubMed DOI PMC

Selker EU, et al. The methylated component of the Neurospora crassa genome. Nature. 2003;422:893–897. doi: 10.1038/nature01564. PubMed DOI

Jamieson K, Rountree MR, Lewis ZA, Stajich JE, Selker EU. Regional control of histone H3 lysine 27 methylation in Neurospora. Proc. Natl. Acad. Sci. 2013;110:6027–6032. doi: 10.1073/pnas.1303750110. PubMed DOI PMC

Wang Y, Smith KM, Taylor JW, Freitag M, Stajich JE. Endogenous small RNA mediates meiotic silencing of a novel DNA transposon. G3 (Bethesda) 2015;5:1949–1960. doi: 10.1534/g3.115.017921. PubMed DOI PMC

Villalta CF, Jacobson DJ, Taylor JW. Three new phylogenetic and biological Neurospora species: N. hispaniola, N. metzenbergii and N. perkinsii. Mycologia. 2009;101:777–789. doi: 10.3852/08-219. PubMed DOI

Castellano, D., James, J., Eyre-Walker, A. & Hernandez, R. Nearly neutral evolution across the Drosophila melanogaster genome. Mol. Biol. Evol. 10.1093/molbev/msy164 (2018). PubMed

Lyon MF. Transmission ratio distortion in mice. Annu. Rev. Genet. 2003;37:393–408. doi: 10.1146/annurev.genet.37.110801.143030. PubMed DOI

Kirkpatrick M. How and why chromosome inversions evolve. PLoS Biol. 2010;8:e1000501. doi: 10.1371/journal.pbio.1000501. PubMed DOI PMC

Johnson LJ. The genome strikes back: the evolutionary importance of defence against mobile elements. Evol. Biol. 2007;34:121–129. doi: 10.1007/s11692-007-9012-5. DOI

Idnurm A, Hood ME, Johannesson H, Giraud T. Contrasted patterns in mating-type chromosomes in fungi: hotspots versus coldspots of recombination. Fungal Biol. Rev. 2015;29:220–229. doi: 10.1016/j.fbr.2015.06.001. PubMed DOI PMC

Lee SI, Kim NS. Transposable elements and genome size variations in plants. Genomics Inform. 2014;12:87–97. doi: 10.5808/GI.2014.12.3.87. PubMed DOI PMC

Gioti A, Mushegian AA, Strandberg R, Stajich JE, Johannesson H. Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements. Mol. Biol. Evol. 2012;29:3215–3226. doi: 10.1093/molbev/mss132. PubMed DOI

Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet. Res. 1966;8:269–294. doi: 10.1017/S0016672300010156. PubMed DOI

Wright AE, Dean R, Zimmer F, Mank JE. How to make a sex chromosome. Nat. Commun. 2016;7:12087. doi: 10.1038/ncomms12087. PubMed DOI PMC

Badouin H, et al. Chaos of rearrangements in the mating-type chromosomes of the anther-smut fungus Microbotryum lychnidis-dioicae. Genetics. 2015;200:1275–1284. doi: 10.1534/genetics.115.177709. PubMed DOI PMC

Purcell J, Brelsford A, Wurm Y, Perrin N, Chapuisat M. Convergent genetic architecture underlies social organization in ants. Curr. Biol. 2014;24:2728–2732. doi: 10.1016/j.cub.2014.09.071. PubMed DOI

McCluskey K, Wiest A, Plamann M. The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J. Biosci. 2010;35:119–126. doi: 10.1007/s12038-010-0014-6. PubMed DOI

Westergaard M, Mitchell HK. Neurospora V. A synthetic medium favoring sexual reproduction. Am. J. Bot. 1947;34:573–577. doi: 10.1002/j.1537-2197.1947.tb13032.x. DOI

Simpson JT, et al. ABySS: a parallel assembler for short read sequence data. Genome Res. 2009;19:1117–1123. doi: 10.1101/gr.089532.108. PubMed DOI PMC

Turner BC, Perkins DD. Strains for studying spore killer elements in four Neurospora species. Fungal Genet. Rep. 1993;40:30. doi: 10.4148/1941-4765.1399. DOI

Yu JH, et al. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 2004;41:973–981. doi: 10.1016/j.fgb.2004.08.001. PubMed DOI

Margolin B, Freitag M, Selker E. Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation. Fungal Genet. Rep. 1997;44:34–36. doi: 10.4148/1941-4765.1281. DOI

Kurtz S, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12. doi: 10.1186/gb-2004-5-2-r12. PubMed DOI PMC

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25:1754–1760. doi: 10.1093/bioinformatics/btp324. PubMed DOI PMC

Dobin A, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21. doi: 10.1093/bioinformatics/bts635. PubMed DOI PMC

Trapnell C, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010;28:511–515. doi: 10.1038/nbt.1621. PubMed DOI PMC

Cantarel BL, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188–196. doi: 10.1101/gr.6743907. PubMed DOI PMC

Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13:2178–2189. doi: 10.1101/gr.1224503. PubMed DOI PMC

Stajich JE, et al. FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res. 2012;40:D675–D681. doi: 10.1093/nar/gkr918. PubMed DOI PMC

She R, et al. genBlastG: using BLAST searches to build homologous gene models. Bioinformatics. 2011;27:2141–2143. doi: 10.1093/bioinformatics/btr342. PubMed DOI

McKenna A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–1303. doi: 10.1101/gr.107524.110. PubMed DOI PMC

Danecek P, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156–2158. doi: 10.1093/bioinformatics/btr330. PubMed DOI PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006;23:254–267. doi: 10.1093/molbev/msj030. PubMed DOI

Ellison CE, et al. Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics. 2011;189:55–69. doi: 10.1534/genetics.111.130690. PubMed DOI PMC

Huerta-Cepas J, Serra F, Bork P. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol. 2016;33:1635–1638. doi: 10.1093/molbev/msw046. PubMed DOI PMC

Svedberg, J. et al. Datasets deposited for Svedberg et al. (2018). ‘Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements’. Figshare https://dx.doi.org/10.6084/m9.figshare.c.4202669 (2018) PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements

. 2018 Oct 12 ; 9 (1) : 4242. [epub] 20181012

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...