Evolution of linkage and genome expansion in protocells: The origin of chromosomes

English version

Autoři: András Szilágyi ^aff001; Viktor Péter Kovács ^aff001; Eörs Szathmáry ^aff001; Mauro Santos ^aff001
Působiště autorů: Institute of Evolution, Centre for Ecological Research, Tihany, Hungary ^aff001; Department of Plant Systematics, Ecology and Theoretical Biology, Eötvös Loránd University, Budapest, Hungary ^aff002; Center for the Conceptual Foundations of Science, Parmenides Foundation, Pullach/Munich, Germany ^aff003; Grup de Genòmica, Bioinformàtica i Biologia Evolutiva (GGBE), Departament de Genètica i de Microbiologia, Universitat Autonòma de Barcelona, Bellaterra, Barcelona, Spain ^aff004
Vyšlo v časopise: Evolution of linkage and genome expansion in protocells: The origin of chromosomes. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009155
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009155

Souhrn

Chromosomes are likely to have assembled from unlinked genes in early evolution. Genetic linkage reduces the assortment load and intragenomic conflict in reproducing protocell models to the extent that chromosomes can go to fixation even if chromosomes suffer from a replicative disadvantage, relative to unlinked genes, proportional to their length. Here we numerically show that chromosomes spread within protocells even if recurrent deleterious mutations affecting replicating genes (as ribozymes) are considered. Dosage effect selects for optimal genomic composition within protocells that carries over to the genic composition of emerging chromosomes. Lacking an accurate segregation mechanism, protocells continue to benefit from the stochastic corrector principle (group selection of early replicators), but now at the chromosome level. A remarkable feature of this process is the appearance of multigene families (in optimal genic proportions) on chromosomes. An added benefit of chromosome formation is an increase in the selectively maintainable genome size (number of different genes), primarily due to the marked reduction of the assortment load. The establishment of chromosomes is under strong positive selection in protocells harboring unlinked genes. The error threshold of replication is raised to higher genome size by linkage due to the fact that deleterious mutations affecting protocells metabolism (hence fitness) show antagonistic (diminishing return) epistasis. This result strengthens the established benefit conferred by chromosomes on protocells allowing for the fixation of highly specific and efficient enzymes.

Klíčová slova:

Deletion mutation – Evolutionary genetics – Fitness epistasis – Genomics – Chromosome structure and function – Natural selection – Parasite evolution – Ribozymes

Zdroje

1. Szilágyi A, Kun Á, Szathmáry E, Early evolution of efficient enzymes and genome organization. Biol. Direct. 2012;7:38. doi: 10.1186/1745-6150-7-38 23114029

2. Szostak JW, Bartel DP, Luisi PL. Synthesizing life. Nature. 2001;409:387–390. doi: 10.1038/35053176 11201752

3. Szathmáry E, Santos M, Fernando C. Evolutionary Potential and Requirements for Minimal Protocells. In: Walde P, editor. Prebiotic Chemistry. Berlin, Heidelberg: Springer Berlin Heidelberg. 2005. pp. 167–211.

4. Szilágyi A, Zachar I, Scheuring I, Kun Á, Könnyű B, Czárán T. Ecology and Evolution in the RNA World Dynamics and Stability of Prebiotic Replicator Systems. Life. 2017;7. doi: 10.3390/life7040048 29186916

5. Szathmáry E, Demeter L. Group selection of early replicators and the origin of life. J Theor Biol. 1987;128:463–486. doi: 10.1016/s0022-5193(87)80191-1 2451771

6. Bansho Y, Furubayashi T, Ichihashi N, Yomo T. Host–parasite oscillation dynamics and evolution in a compartmentalized RNA replication system. Proc Natl Acad Sci USA. 2016;113:4045. doi: 10.1073/pnas.1524404113 27035976

7. Matsumura S, Kun Á, Ryckelynck M, Coldren F, Szilágyi A, Jossinet F, et al. Transient compartmentalization of RNA replicators prevents extinction due to parasites. Science. 2016;354:1293. doi: 10.1126/science.aag1582 27940874

8. Pigliucci M. Samir Okasha: Evolution and the levels of selection. Biol Philos. 2009;24:551–560.

9. Koch AL. Evolution vs the number of gene copies per primitive cell. J Mol Evol. 1984;20:71–76. doi: 10.1007/BF02101988 6429344

10. Santos M, Zintzaras E, Szathmáry E. Recombination in Primeval Genomes: A Step Forward but Still a Long Leap from Maintaining a Sizable Genome. J Mol Evol. 2004;59:507–519. doi: 10.1007/s00239-004-2642-7 15638462

11. Hubai AG, Kun Á. Maximal gene number maintainable by stochastic correction–The second error threshold. J Theor Biol. 2016;405:29–35. doi: 10.1016/j.jtbi.2016.02.007 26876752

12. Bansho Y, Ichihashi N, Kazuta Y, Matsuura T, Suzuki H, Yomo T. Importance of Parasite RNA Species Repression for Prolonged Translation-Coupled RNA Self-Replication. Chem Biol. 2012;19:478–487. doi: 10.1016/j.chembiol.2012.01.019 22520754

13. Maynard Smith J, Szathmáry E. The Major Transitions in Evolution: Freeman Oxford;1995. doi: 10.1093/oxfordjournals.molbev.a040212 7739379

14. Maynard Smith J, Szathmáry E. The Origin of Chromosomes I. Selection for Linkage. J of Theor Biol. 1993;164:437–446.

15. Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971;58:465–523. doi: 10.1007/BF00623322 4942363

16. Kun Á, Santos M, Szathmáry E. Real ribozymes suggest a relaxed error threshold. Nat Genet. 2005;37:1008–1011. doi: 10.1038/ng1621 16127452

17. Otto SP, Feldman MW. Deleterious Mutations, Variable Epistatic Interactions, and the Evolution of Recombination. Theor Popul Biol. 1997;51:134–147. doi: 10.1006/tpbi.1997.1301 9169238

18. Feldman MW, Otto SP, Christiansen FB. Population genetic perspectives on the evolution of recombination. Annu Rev Genet. 1996;30:261–295. doi: 10.1146/annurev.genet.30.1.261 8982456

19. Szathmáry E. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics. 1993;133:127. 8417983

20. Hobbie JE, Hobbie EA. Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates. Frontiers in microbiology. 2013;4:324–324. doi: 10.3389/fmicb.2013.00324 24273534

21. Grey D, Hutson V, Szathmáry E. A re-examination of the stochastic corrector model. Proc R Soc Lond B Biol Sci. 1995;262:29–35.

22. Szathmáry E, Maynard Smith J. The Evolution of Chromosomes II. Molecular Mechanisms. J Theor Biol. 1993;164:447–454. doi: 10.1006/jtbi.1993.1166 7505372

23. Weiner AM, Maizels N. tRNA-like structures tag the 3' ends of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc Natl Acad Sci USA. 1987;84:7383. doi: 10.1073/pnas.84.21.7383 3478699

24. Zintzaras E, Santos M, Szathmáry E. Selfishness versus functional cooperation in a stochastic protocell model. J Theor Biol. 2010;267:605–613. doi: 10.1016/j.jtbi.2010.09.011 20837027

25. Zintzaras E, Santos M, Szathmáry E. “Living” Under the Challenge of Information Decay: The Stochastic Corrector Model vs. Hypercycles. J Theor Biol. 2002;217:167–181. doi: 10.1006/jtbi.2002.3026 12202111

26. Lai MM. RNA recombination in animal and plant viruses. Microbiol Rev. 1992;56:61. 1579113

27. Kacser H, Beeby R. Evolution of catalytic proteins or on the origin of enzyme species by means of natural selection. J Mol Evol. 1984;20:38–51. doi: 10.1007/BF02101984 6429341

28. Moran PAP. Random processes in genetics. Math Proc Camb Philos Soc. 1958;54:60–71.

29. Boerlijst MC, Bonhoeffer S, Nowak MA. Viral Quasi-Species and Recombination. Proc Biol Sci. 1996;263:1577–1584.

30. Wilke CO, Lenski RE, Adami C. Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol Biol. 2003;3:3. doi: 10.1186/1471-2148-3-3 12590655

31. Sanjuán R, Moya A, Elena SF. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA. 2004;101:15376. doi: 10.1073/pnas.0404125101 15492220

32. He X, Qian W, Wang Z, Li Y, Zhang J. Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks. Nat Genet. 2010;42:272. doi: 10.1038/ng.524 20101242

33. Anderson RP, Roth JR. Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol. 1977;31:473–505. doi: 10.1146/annurev.mi.31.100177.002353 334045

34. Fani R, Fondi M. Origin and evolution of metabolic pathways. Phys Life Rev. 2009;6:23–52. doi: 10.1016/j.plrev.2008.12.003 20416849

35. Leigh EG. When does the good of the group override the advantage of the individual? Proc Natl Acad Sci USA. 1983;80:2985. doi: 10.1073/pnas.80.10.2985 16593312

36. Brosius J. Gene duplication and other evolutionary strategies: from the RNA world to the future. J Struct Funct Genomics. 2003;3:1–17. doi: 10.1023/a:1022627311114 12836680

37. Bourke AFG. Principles of Social Evolution. Oxford University Press.2011.

38. Vig-Milkovics Z, Zachar I, Kun Á, Szilágyi A, Szathmáry E. Moderate sex between protocells can balance between a decrease in assortment load and an increase in parasite spread. J Theor Biol. 2019;462:304–310. doi: 10.1016/j.jtbi.2018.11.020 30471297

39. Brosius J. Disparity, adaptation, exaptation, bookkeeping, and contingency at the genome level. Paleobiology 2016;31:1–16.

Článek Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Článek A single Ho-induced double-strand break at the MAT locus is lethal in Candida glabrata

Článek A Rad51-independent pathway promotes single-strand template repair in gene editing

Článek Novel loci for childhood body mass index and shared heritability with adult cardiometabolic traits

Článek C. elegans CLASP/CLS-2 negatively regulates membrane ingression throughout the oocyte cortex and is required for polar body extrusion

Článek The O-GlcNAc transferase OGT is a conserved and essential regulator of the cellular and organismal response to hypertonic stress

Článek Drosophila phosphatidylinositol-4 kinase fwd promotes mitochondrial fission and can suppress Pink1/parkin phenotypes

Článek A new domestic cat genome assembly based on long sequence reads empowers feline genomic medicine and identifies a novel gene for dwarfism

Článek Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO

Článek How noncrossover homologs are conjoined and segregated in Drosophila male meiosis I: Stable but reversible homolog linkers require a novel Separase target protein

Článek Predominance of positive epistasis among drug resistance-associated mutations in HIV-1 protease