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      Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution

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      PLOS Genetics
      Public Library of Science

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          Abstract

          The integration of individually replicating genes into a primitive chromosome is a key evolutionary transition in the development of life, allowing the simultaneous inheritance of genes. However, how this transition occurred is unclear because the extended size of primitive chromosomes replicate slower than unlinked genes. Theoretical studies have suggested that a primitive chromosome can evolve in the presence of cell-like compartments, as the physical linkage prevents the stochastic loss of essential genes upon division, but experimental support for this is lacking. Here, we demonstrate the evolution of a chromosome-like RNA from two cooperative RNA replicators encoding replication and metabolic enzymes. Through their long-term replication in cell-like compartments, linked RNAs emerged with the two cooperative RNAs connected end-to-end. The linked RNAs had different mutation patterns than the two unlinked RNAs, suggesting that they were maintained as partially distinct lineages in the population. Our results provide experimental evidence supporting the plausibility of the evolution of a primitive chromosome from unlinked gene fragments, an important step in the emergence of complex biological systems.

          Author summary

          The integration of genes into a chromosome is a fundamental genetic organization in all extant life. The assembly of unlinked genes during prebiotic evolution was likely a major evolutionary transition toward the development of a complex cell. Decades of theoretical studies have suggested a plausible evolutionary pathway to a primitive chromosome from replicating RNA molecules that harbor cooperative genes within a protocell structure. However, demonstrating the evolution of a primitive chromosome in an experimental setup is challenging. We previously developed a cooperative RNA replication system in which two types of RNAs co-replicate using their self-encoded replication and metabolic enzymes. Using this system, in the present study, we demonstrate the evolution of a linkage between the two cooperative RNA replicators in compartments. An evolved “linked” RNA harbored the entire region of both genes, accumulated distinct mutations, and retained the ability to replicate using the two proteins translated from itself. These experimental findings support a prebiotic evolutionary scenario, in which unlinked genes assembled into a single genomic structure.

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          Most cited references40

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          Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation

          The Interactive Tree Of Life ( https://itol.embl.de ) is an online tool for the display, manipulation and annotation of phylogenetic and other trees. It is freely available and open to everyone. iTOL version 5 introduces a completely new tree display engine, together with numerous new features. For example, a new dataset type has been added (MEME motifs), while annotation options have been expanded for several existing ones. Node metadata display options have been extended and now also support non-numerical categorical values, as well as multiple values per node. Direct manual annotation is now available, providing a set of basic drawing and labeling tools, allowing users to draw shapes, labels and other features by hand directly onto the trees. Support for tree and dataset scales has been extended, providing fine control over line and label styles. Unrooted tree displays can now use the equal-daylight algorithm, proving a much greater display clarity. The user account system has been streamlined and expanded with new navigation options and currently handles >1 million trees from >70 000 individual users. Graphical Abstract iTOL: an online tool for the tree display and annotation.
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            MEGA11: Molecular Evolutionary Genetics Analysis Version 11

            The Molecular Evolutionary Genetics Analysis (MEGA) software has matured to contain a large collection of methods and tools of computational molecular evolution. Here, we describe new additions that make MEGA a more comprehensive tool for building timetrees of species, pathogens, and gene families using rapid relaxed-clock methods. Methods for estimating divergence times and confidence intervals are implemented to use probability densities for calibration constraints for node-dating and sequence sampling dates for tip-dating analyses. They are supported by new options for tagging sequences with spatiotemporal sampling information, an expanded interactive Node Calibrations Editor , and an extended Tree Explorer to display timetrees. Also added is a Bayesian method for estimating neutral evolutionary probabilities of alleles in a species using multispecies sequence alignments and a machine learning method to test for the autocorrelation of evolutionary rates in phylogenies. The computer memory requirements for the maximum likelihood analysis are reduced significantly through reprogramming, and the graphical user interface has been made more responsive and interactive for very big data sets. These enhancements will improve the user experience, quality of results, and the pace of biological discovery. Natively compiled graphical user interface and command-line versions of MEGA11 are available for Microsoft Windows, Linux, and macOS from www.megasoftware.net .
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              Cell-free translation reconstituted with purified components.

              We have developed a protein-synthesizing system reconstituted from recombinant tagged protein factors purified to homogeneity. The system was able to produce protein at a rate of about 160 microg/ml/h in a batch mode without the need for any supplementary apparatus. The protein products were easily purified within 1 h using affinity chromatography to remove the tagged protein factors. Moreover, omission of a release factor allowed efficient incorporation of an unnatural amino acid using suppressor transfer RNA (tRNA).
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                PLOS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                4 August 2023
                August 2023
                : 19
                : 8
                : e1010471
                Affiliations
                [1 ] Department of Life Science, Graduate School of Arts and Science, the University of Tokyo, Meguro, Tokyo, Japan
                [2 ] Department of Electrical Engineering and Bioscience, Faculty of Science and Engineering, Waseda University, Shinjuku, Tokyo, Japan
                [3 ] JST, FOREST, Kawaguchi, Saitama, Japan
                [4 ] Komaba Institute for Science, the University of Tokyo, Meguro, Tokyo, Japan
                [5 ] Universal Biology Institute, the University of Tokyo, Meguro, Tokyo, Japan
                University of Münster, GERMANY
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-6712-1040
                Article
                PGENETICS-D-22-01166
                10.1371/journal.pgen.1010471
                10431678
                37540715
                8803179b-45d8-4eba-bef0-f2b24e9c3ea3
                © 2023 Ueda et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 12 October 2022
                : 18 July 2023
                Page count
                Figures: 5, Tables: 0, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 19K23763
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 21H05867
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 20H04859
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002241, Japan Science and Technology Agency;
                Award ID: PRESTO JPMJPR19KA
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002241, Japan Science and Technology Agency;
                Award ID: CREST JPMJCR20S1
                Award Recipient :
                This work was supported by Japan Society for the Promotion of Science KAKENHI (21H05867 and 23H04403 to R.M., 22H05402 to N.I.) and Japan Science and Technology Agency PRESTO (JPMJPR19KA to R.M.) and CREST (JPMJCR20S1 to N.I.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Cloning
                Research and Analysis Methods
                Molecular Biology Techniques
                Cloning
                Research and Analysis Methods
                Research Design
                Replication Studies
                Biology and Life Sciences
                Genetics
                Gene Expression
                Protein Translation
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Genetics
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Reverse Transcriptase-Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Reverse Transcriptase-Polymerase Chain Reaction
                Biology and Life Sciences
                Evolutionary Biology
                Molecular Evolution
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and life sciences
                Molecular biology
                Molecular biology techniques
                Molecular biology assays and analysis techniques
                Nucleic acid analysis
                RNA analysis
                Research and analysis methods
                Molecular biology techniques
                Molecular biology assays and analysis techniques
                Nucleic acid analysis
                RNA analysis
                Custom metadata
                vor-update-to-uncorrected-proof
                2023-08-16
                All relevant data are within the paper and its Supporting Information files.

                Genetics
                Genetics

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