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Adaptation dynamics between copynumber and point mutations. eLife. 11, e82240."},"publication":"eLife","article_type":"original","has_accepted_license":"1","article_processing_charge":"No","day":"22","scopus_import":"1","oa_version":"Published Version","file":[{"relation":"main_file","file_id":"12338","date_updated":"2023-01-23T08:56:21Z","date_created":"2023-01-23T08:56:21Z","checksum":"9321fd5f06ff59d5e2d33daee84b3da1","success":1,"file_name":"2022_eLife_Tomanek.pdf","access_level":"open_access","content_type":"application/pdf","file_size":8835954,"creator":"dernst"}],"_id":"12333","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","intvolume":" 11","ddc":["570"],"title":"Adaptation dynamics between copynumber and point mutations","status":"public","abstract":[{"lang":"eng","text":"Together, copy-number and point mutations form the basis for most evolutionary novelty, through the process of gene duplication and divergence. While a plethora of genomic data reveals the long-term fate of diverging coding sequences and their cis-regulatory elements, little is known about the early dynamics around the duplication event itself. In microorganisms, selection for increased gene expression often drives the expansion of gene copy-number mutations, which serves as a crude adaptation, prior to divergence through refining point mutations. Using a simple synthetic genetic reporter system that can distinguish between copy-number and point mutations, we study their early and transient adaptive dynamics in real time in Escherichia coli. We find two qualitatively different routes of adaptation, depending on the level of functional improvement needed. In conditions of high gene expression demand, the two mutation types occur as a combination. However, under low gene expression demand, copy-number and point mutations are mutually exclusive; here, owing to their higher frequency, adaptation is dominated by copy-number mutations, in a process we term amplification hindrance. Ultimately, due to high reversal rates and pleiotropic cost, copy-number mutations may not only serve as a crude and transient adaptation, but also constrain sequence divergence over evolutionary time scales."}],"type":"journal_article","doi":"10.7554/ELIFE.82240","language":[{"iso":"eng"}],"external_id":{"isi":["000912674700001"]},"tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)","image":"/images/cc_by.png"},"oa":1,"quality_controlled":"1","isi":1,"publication_identifier":{"eissn":["2050-084X"]},"month":"12","related_material":{"record":[{"id":"12339","status":"public","relation":"research_data"}],"link":[{"relation":"software","url":"https://doi.org/10.5281/zenodo.6974122"}]},"author":[{"orcid":"0000-0001-6197-363X","id":"3981F020-F248-11E8-B48F-1D18A9856A87","last_name":"Tomanek","first_name":"Isabella","full_name":"Tomanek, Isabella"},{"first_name":"Calin C","last_name":"Guet","id":"47F8433E-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-6220-2052","full_name":"Guet, Calin C"}],"volume":11,"date_updated":"2023-08-03T14:23:07Z","date_created":"2023-01-22T23:00:55Z","year":"2022","acknowledgement":"We are grateful to N Barton, F Kondrashov, M Lagator, M Pleska, R Roemhild, D Siekhaus, and G\r\nTkacik for input on the manuscript and to K Tomasek for help with flow cytometry.","publisher":"eLife Sciences Publications","department":[{"_id":"CaGu"}],"publication_status":"published","file_date_updated":"2023-01-23T08:56:21Z","article_number":"e82240"},{"ddc":["570"],"status":"public","title":"Flow cytometry YFP and CFP data and deep sequencing data of populations evolving in galactose","publisher":"Dryad","department":[{"_id":"CaGu"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","_id":"12339","year":"2022","date_created":"2023-01-23T09:00:37Z","date_updated":"2023-08-03T14:23:06Z","oa_version":"Published Version","author":[{"full_name":"Tomanek, Isabella","first_name":"Isabella","last_name":"Tomanek","id":"3981F020-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-6197-363X"},{"orcid":"0000-0001-6220-2052","id":"47F8433E-F248-11E8-B48F-1D18A9856A87","last_name":"Guet","first_name":"Calin C","full_name":"Guet, Calin C"}],"related_material":{"record":[{"id":"12333","relation":"used_in_publication","status":"public"}]},"type":"research_data_reference","abstract":[{"text":"Copy-number and point mutations form the basis for most evolutionary novelty through the process of gene duplication and divergence. While a plethora of genomic sequence data reveals the long-term fate of diverging coding sequences and their cis-regulatory elements, little is known about the early dynamics around the duplication event itself. In microorganisms, selection for increased gene expression often drives the expansion of gene copy-number mutations, which serves as a crude adaptation, prior to divergence through refining point mutations. Using a simple synthetic genetic system that allows us to distinguish copy-number and point mutations, we study their early and transient adaptive dynamics in real-time in Escherichia coli. We find two qualitatively different routes of adaptation depending on the level of functional improvement selected for: In conditions of high gene expression demand, the two types of mutations occur as a combination. Under low gene expression demand, negative epistasis between the two types of mutations renders them mutually exclusive. Thus, owing to their higher frequency, adaptation is dominated by copy-number mutations. Ultimately, due to high rates of reversal and pleiotropic cost, copy-number mutations may not only serve as a crude and transient adaptation but also constrain sequence divergence over evolutionary time scales.","lang":"eng"}],"main_file_link":[{"open_access":"1","url":"https://doi.org/10.5061/dryad.rfj6q57ds"}],"oa":1,"citation":{"chicago":"Tomanek, Isabella, and Calin C Guet. “Flow Cytometry YFP and CFP Data and Deep Sequencing Data of Populations Evolving in Galactose.” Dryad, 2022. https://doi.org/10.5061/dryad.rfj6q57ds.","mla":"Tomanek, Isabella, and Calin C. Guet. Flow Cytometry YFP and CFP Data and Deep Sequencing Data of Populations Evolving in Galactose. Dryad, 2022, doi:10.5061/dryad.rfj6q57ds.","short":"I. Tomanek, C.C. Guet, (2022).","ista":"Tomanek I, Guet CC. 2022. 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Over the course of the first semester, students participated in seminars, where they shared their results with the colleagues from other fields and took part in discussions on relevant subjects. The main focus during this sessions was on delivering the information in a simplified and comprehensible way, going into the very basics of a subject if necessary. At the end, the students were asked to present their research in the written form to exercise their writing skills. The reports were gathered in this document. All of them were reviewed by the teaching assistants and write-ups illustrating unique stylistic features and, in general, an outstanding level of writing skills, were honorably mentioned in the section \"Selected Reports\"."}],"extern":"1"},{"type":"journal_article","abstract":[{"text":"Organisms cope with change by taking advantage of transcriptional regulators. However, when faced with rare environments, the evolution of transcriptional regulators and their promoters may be too slow. Here, we investigate whether the intrinsic instability of gene duplication and amplification provides a generic alternative to canonical gene regulation. Using real-time monitoring of gene-copy-number mutations in Escherichia coli, we show that gene duplications and amplifications enable adaptation to fluctuating environments by rapidly generating copy-number and, therefore, expression-level polymorphisms. This amplification-mediated gene expression tuning (AMGET) occurs on timescales that are similar to canonical gene regulation and can respond to rapid environmental changes. Mathematical modelling shows that amplifications also tune gene expression in stochastic environments in which transcription-factor-based schemes are hard to evolve or maintain. The fleeting nature of gene amplifications gives rise to a generic population-level mechanism that relies on genetic heterogeneity to rapidly tune the expression of any gene, without leaving any genomic signature.","lang":"eng"}],"issue":"4","title":"Gene amplification as a form of population-level gene expression regulation","ddc":["570"],"status":"public","intvolume":" 4","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","_id":"7652","file":[{"file_id":"8640","relation":"main_file","date_created":"2020-10-09T09:56:01Z","date_updated":"2020-10-09T09:56:01Z","success":1,"checksum":"ef3bbf42023e30b2c24a6278025d2040","file_name":"2020_NatureEcolEvo_Tomanek.pdf","access_level":"open_access","creator":"dernst","content_type":"application/pdf","file_size":745242}],"oa_version":"Submitted Version","scopus_import":"1","day":"01","article_processing_charge":"No","has_accepted_license":"1","article_type":"original","page":"612-625","publication":"Nature Ecology & Evolution","citation":{"chicago":"Tomanek, Isabella, Rok Grah, M. Lagator, A. M. C. Andersson, Jonathan P Bollback, Gašper Tkačik, and Calin C Guet. “Gene Amplification as a Form of Population-Level Gene Expression Regulation.” Nature Ecology & Evolution. Springer Nature, 2020. https://doi.org/10.1038/s41559-020-1132-7.","short":"I. Tomanek, R. Grah, M. Lagator, A.M.C. Andersson, J.P. Bollback, G. Tkačik, C.C. Guet, Nature Ecology & Evolution 4 (2020) 612–625.","mla":"Tomanek, Isabella, et al. “Gene Amplification as a Form of Population-Level Gene Expression Regulation.” Nature Ecology & Evolution, vol. 4, no. 4, Springer Nature, 2020, pp. 612–25, doi:10.1038/s41559-020-1132-7.","ieee":"I. Tomanek et al., “Gene amplification as a form of population-level gene expression regulation,” Nature Ecology & Evolution, vol. 4, no. 4. Springer Nature, pp. 612–625, 2020.","apa":"Tomanek, I., Grah, R., Lagator, M., Andersson, A. M. C., Bollback, J. P., Tkačik, G., & Guet, C. C. (2020). Gene amplification as a form of population-level gene expression regulation. 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R.G. is a recipient of a DOC (Doctoral Fellowship Programme of the Austrian Academy of Sciences) Fellowship of the Austrian Academy of Sciences.","year":"2020","date_created":"2020-04-08T15:20:53Z","date_updated":"2024-03-28T23:30:37Z","volume":4,"author":[{"last_name":"Tomanek","first_name":"Isabella","orcid":"0000-0001-6197-363X","id":"3981F020-F248-11E8-B48F-1D18A9856A87","full_name":"Tomanek, Isabella"},{"full_name":"Grah, Rok","orcid":"0000-0003-2539-3560","id":"483E70DE-F248-11E8-B48F-1D18A9856A87","last_name":"Grah","first_name":"Rok"},{"last_name":"Lagator","first_name":"M.","full_name":"Lagator, M."},{"full_name":"Andersson, A. M. C.","last_name":"Andersson","first_name":"A. M. 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Point mutations change a single letter in the DNA sequence, while copy number mutations like duplications or deletions add or remove many letters of the DNA sequence simultaneously. Each type of mutation exhibits specific properties like its rate of formation and reversal. \r\nGene expression is a fundamental phenotype that can be altered by both, point and copy number mutations. The following thesis is concerned with the dynamics of gene expression evolution and how it is affected by the properties exhibited by point and copy number mutations. Specifically, we are considering i) copy number mutations during adaptation to fluctuating environments and ii) the interaction of copy number and point mutations during adaptation to constant environments. "}],"alternative_title":["ISTA Thesis"],"type":"dissertation","date_published":"2020-10-13T00:00:00Z","page":"117","citation":{"short":"I. Tomanek, The Evolution of Gene Expression by Copy Number and Point Mutations, Institute of Science and Technology Austria, 2020.","mla":"Tomanek, Isabella. The Evolution of Gene Expression by Copy Number and Point Mutations. Institute of Science and Technology Austria, 2020, doi:10.15479/AT:ISTA:8653.","chicago":"Tomanek, Isabella. “The Evolution of Gene Expression by Copy Number and Point Mutations.” Institute of Science and Technology Austria, 2020. https://doi.org/10.15479/AT:ISTA:8653.","ama":"Tomanek I. The evolution of gene expression by copy number and point mutations. 2020. doi:10.15479/AT:ISTA:8653","ieee":"I. Tomanek, “The evolution of gene expression by copy number and point mutations,” Institute of Science and Technology Austria, 2020.","apa":"Tomanek, I. (2020). The evolution of gene expression by copy number and point mutations. Institute of Science and Technology Austria. https://doi.org/10.15479/AT:ISTA:8653","ista":"Tomanek I. 2020. 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(2019). Data for the paper “Gene amplification as a form of population-level gene expression regulation.” Institute of Science and Technology Austria. https://doi.org/10.15479/AT:ISTA:7016","ieee":"I. Tomanek, “Data for the paper ‘Gene amplification as a form of population-level gene expression regulation.’” Institute of Science and Technology Austria, 2019.","ista":"Tomanek I. 2019. Data for the paper ‘Gene amplification as a form of population-level gene expression regulation’, Institute of Science and Technology Austria, 10.15479/AT:ISTA:7016.","ama":"Tomanek I. Data for the paper “Gene amplification as a form of population-level gene expression regulation.” 2019. doi:10.15479/AT:ISTA:7016","chicago":"Tomanek, Isabella. “Data for the Paper ‘Gene Amplification as a Form of Population-Level Gene Expression Regulation.’” Institute of Science and Technology Austria, 2019. https://doi.org/10.15479/AT:ISTA:7016.","short":"I. Tomanek, (2019).","mla":"Tomanek, Isabella. Data for the Paper “Gene Amplification as a Form of Population-Level Gene Expression Regulation.” Institute of Science and Technology Austria, 2019, doi:10.15479/AT:ISTA:7016."},"oa":1,"file_date_updated":"2020-07-14T12:47:47Z","abstract":[{"lang":"eng","text":"Organisms cope with change by employing transcriptional regulators. However, when faced with rare environments, the evolution of transcriptional regulators and their promoters may be too slow. We ask whether the intrinsic instability of gene duplication and amplification provides a generic alternative to canonical gene regulation. By real-time monitoring of gene copy number mutations in E. coli, we show that gene duplications and amplifications enable adaptation to fluctuating environments by rapidly generating copy number, and hence expression level, polymorphism. This ‘amplification-mediated gene expression tuning’ occurs on timescales similar to canonical gene regulation and can deal with rapid environmental changes. Mathematical modeling shows that amplifications also tune gene expression in stochastic environments where transcription factor-based schemes are hard to evolve or maintain. 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