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Evolutionary Patterns in the Sequence and Structure of Transfer RNA: A Window into Early Translation and the Genetic Code

Publication Date: July 30, 2008
Journal: PLoS ONE
Authors: Feng-Jie Sun & Gustavo Caetano-Anollés
Volume: 3
Issue: 7
Pages: e2799
DOI: https://dx.plos.org/10.1371/journal.pone.0002799
Publisher URL: http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0002799
Web of Science: 000264304300018
Scopus: 50949084622
Mendeley: http://www.mendeley.com/research/evolutionary-patterns-sequence-structure-transfer-rna-window-early-translation-genetic-code

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{"title"=>"Evolutionary patterns in the sequence and structure of transfer RNA: A window into early translation and the genetic code", "type"=>"journal", "authors"=>[{"first_name"=>"Feng Jie", "last_name"=>"Sun", "scopus_author_id"=>"15726651300"}, {"first_name"=>"Gustavo", "last_name"=>"Caetano-Anollés", "scopus_author_id"=>"56269658000"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-50949084622", "sgr"=>"50949084622", "pui"=>"352269665", "isbn"=>"1932-6203", "pmid"=>"18665254", "doi"=>"10.1371/journal.pone.0002799"}, "id"=>"e89a76d3-537c-371f-9cd6-20560c030e20", "abstract"=>"Transfer RNA (tRNA) molecules play vital roles during protein synthesis. Their acceptor arms are aminoacylated with specific amino acid residues while their anticodons delimit codon specificity. The history of these two functions has been generally linked in evolutionary studies of the genetic code. However, these functions could have been differentially recruited as evolutionary signatures were left embedded in tRNA molecules. Here we built phylogenies derived from the sequence and structure of tRNA, we forced taxa into monophyletic groups using constraint analyses, tested competing evolutionary hypotheses, and generated timelines of amino acid charging and codon discovery. Charging of Sec, Tyr, Ser and Leu appeared ancient, while specificities related to Asn, Met, and Arg were derived. The timelines also uncovered an early role of the second and then first codon bases, identified codons for Ala and Pro as the most ancient, and revealed important evolutionary take-overs related to the loss of the long variable arm in tRNA. The lack of correlation between ancestries of amino acid charging and encoding indicated that the separate discoveries of these functions reflected independent histories of recruitment. These histories were probably curbed by co-options and important take-overs during early diversification of the living world.", "link"=>"http://www.mendeley.com/research/evolutionary-patterns-sequence-structure-transfer-rna-window-early-translation-genetic-code", "reader_count"=>30, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>20, "Physics and Astronomy"=>2, "Chemistry"=>4, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>4}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "Netherlands"=>1, "United States"=>1, "Brazil"=>1, "Poland"=>1, "Switzerland"=>1, "Germany"=>1, "India"=>2}, "group_count"=>0}

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{"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/7bfcae51-7723-42a2-8942-fd9a0b1287fa", "title"=>"Related article", "body"=>"This work is available in PLoS Computational Biology at: http://www.ploscompbiol.org/doi/pcbi.1000018.", "highlightedText"=>"''This phylogenetic method (known as constraint analysis) is powerful and was recently used to gain insight into the origin of cellular superkingdoms and viruses''\nhttp://plosone.org/article/info:doi/10.1371/journal.pone.0002799#article1.body1.sec1.p3", "isRemoved"=>false, "created"=>"2009-02-17T11:36:43Z", "lastModified"=>"2009-02-17T11:36:43Z", "creator"=>{"userId"=>"40493"}, "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0002799", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2009-02-17T11:36:43Z", "replies"=>[]}

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Figshare07 Jan 06:06 UTC

Figshare

{"files"=>["https://ndownloader.figshare.com/files/456284", "https://ndownloader.figshare.com/files/456298", "https://ndownloader.figshare.com/files/456309", "https://ndownloader.figshare.com/files/456329"], "description"=>"<div>Transfer RNA (tRNA) molecules play vital roles during protein synthesis. Their acceptor arms are aminoacylated with specific amino acid residues while their anticodons delimit codon specificity. The history of these two functions has been generally linked in evolutionary studies of the genetic code. However, these functions could have been differentially recruited as evolutionary signatures were left embedded in tRNA molecules. Here we built phylogenies derived from the sequence and structure of tRNA, we forced taxa into monophyletic groups using constraint analyses, tested competing evolutionary hypotheses, and generated timelines of amino acid charging and codon discovery. Charging of Sec, Tyr, Ser and Leu appeared ancient, while specificities related to Asn, Met, and Arg were derived. The timelines also uncovered an early role of the second and then first codon bases, identified codons for Ala and Pro as the most ancient, and revealed important evolutionary take-overs related to the loss of the long variable arm in tRNA. The lack of correlation between ancestries of amino acid charging and encoding indicated that the separate discoveries of these functions reflected independent histories of recruitment. These histories were probably curbed by co-options and important take-overs during early diversification of the living world.</div>", "links"=>[], "tags"=>["evolutionary", "patterns"], "article_id"=>149876, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.s001", "https://dx.doi.org/10.1371/journal.pone.0002799.s002", "https://dx.doi.org/10.1371/journal.pone.0002799.s003", "https://dx.doi.org/10.1371/journal.pone.0002799.s004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Evolutionary_Patterns_in_the_Sequence_and_Structure_of_Transfer_RNA_A_Window_into_Early_Translation_and_the_Genetic_Code/149876", "title"=>"Evolutionary Patterns in the Sequence and Structure of Transfer RNA: A Window into Early Translation and the Genetic Code", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-07-30 02:44:36"}
{"files"=>["https://ndownloader.figshare.com/files/924539"], "description"=>"MP analyses of data from 571 tRNA molecules resulted in the preset limit of 20,000 minimal length trees, each of 10,083 steps. Consistency index = 0.069 and 0.069, with and without uninformative characters, respectively; Retention index = 0.681; Rescaled consistency index = 0.047; g1 = −0.107. Terminal leaves are not labeled since they would not be legible. tRNA molecules coding for Sec, Ser, Tyr, and Leu are labeled with colors. Note several of these tRNAs have short variable arms and these are derived in the tree. Nodes labeled with closed circles have BS values >50%. The figure has been modified from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002799#pone.0002799-Sun2\" target=\"_blank\">[27]</a> and a global tRNA tree with labeled terminal taxa can be found in Supporting Information (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002799#pone.0002799.s002\" target=\"_blank\">Figure S1</a>).", "links"=>[], "tags"=>["phylogenetic", "trna", "molecules", "reconstructed"], "article_id"=>594997, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_global_phylogenetic_tree_of_tRNA_molecules_reconstructed_from_sequence_and_structure_/594997", "title"=>"A global phylogenetic tree of tRNA molecules reconstructed from sequence and structure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-30 01:23:17"}
{"files"=>["https://ndownloader.figshare.com/files/924622"], "description"=>"A. Cumulative frequency distribution plots that describe the cumulative number of tRNAs charging for different amino acids as a function of node distance (nd), the number of nodes from an hypothetical tRNA molecules at the base of the tree. B. Average nd for each tRNA charging group plotted against number of additional steps (S) needed to satisfy constraints that force the monophyletic grouping of corresponding tRNA molecules, normalized to a 0–1 scale. Different colored circles correspond to the three groups of tRNA molecules described in the text. C. Plot describing the effect of numbers of tRNA that are constrained versus normalized S values.", "links"=>[], "tags"=>["amino", "charging"], "article_id"=>595081, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_analyses_of_the_amino_acid_charging_function_in_tRNA_/595081", "title"=>"Phylogenetic analyses of the amino acid charging function in tRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-30 01:24:41"}
{"files"=>["https://ndownloader.figshare.com/files/924775"], "description"=>"A. Degenerate genetic code table painted with colors describing the ancestry (S) of their codon identity function, in which two (A) or one (B) position in the codon is degenerate and harbors any one of the four bases (N). Ancestries were derived by constraining sets of tRNA molecules into monophyletic groups. S values are provided in the right hand corner for every codon, and corrected S values that exclude type I molecules from the constraints are given in the left hand corner for codons related to Leu, Ser, and Tyr. Amino acid that are encoded are listed below corresponding codons.", "links"=>[], "tags"=>["codon", "functions"], "article_id"=>595227, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_analysis_of_codon_identity_functions_in_tRNA_/595227", "title"=>"Phylogenetic analysis of codon identity functions in tRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-30 01:27:07"}
{"files"=>["https://ndownloader.figshare.com/files/924911"], "description"=>"Dashed lines describe the effect of excluding type I tRNA variants from the constraints (from orange to red circles), and illustrate recruitment events related to the loss of the variable arm in these molecules. Color schemes of circles follow those of <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002799#pone-0002799-g002\" target=\"_blank\">Figure 2</a>.", "links"=>[], "tags"=>["describing", "ancestries", "amino", "charging", "codon", "normalized"], "article_id"=>595359, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plot_describing_the_relationship_between_ancestries_of_amino_acid_charging_S_aac_and_codon_identity_S_cod_function_normalized_to_a_0_1_scale_/595359", "title"=>"Plot describing the relationship between ancestries of amino acid charging (Saac) and codon identity (Scod) function, normalized to a 0–1 scale.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-30 01:29:19"}
{"files"=>["https://ndownloader.figshare.com/files/925032"], "description"=>"Each constrained group is given in parentheses and amino acids are indicated by the IUPAC 3-letter nomenclature. The length of the most parsimonious trees derived from the combined data set was 10,083 steps. Superscripts associated with amino acid codes indicate tRNAs belong to Type II molecules.", "links"=>[], "tags"=>["numbers", "steps", "molecules", "monophyly", "constraints", "amino", "specificity", "trna", "classes", "ii", "mp", "571"], "article_id"=>595469, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_numbers_of_additional_steps_S_required_to_force_molecules_into_monophyly_based_on_constraints_related_to_amino_acid_specificity_spec_or_amino_acid_specificity_and_tRNA_structural_classes_type_I_and_II_tRNAs_cat_spec_during_MP_analyses_of_the_combined/595469", "title"=>"The numbers of additional steps (S) required to force molecules into monophyly based on constraints related to amino acid specificity (spec) or amino acid specificity and tRNA structural classes (type I and II tRNAs) (cat-spec) during MP analyses of the combined structure and sequence data for 571 tRNA molecules.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-07-30 01:31:09"}
{"files"=>["https://ndownloader.figshare.com/files/925065"], "description"=>"The length of the most parsimonious trees derived from the combined data set was 10,083 steps. Each constrained group is given in parentheses and groups of tRNA molecules are indicated by codons with shared the first, second, third, or the first two bases. Symbol “N” indicates A, U, G, or C.", "links"=>[], "tags"=>["numbers", "steps", "molecules", "sharing", "bases", "codons", "monophyly", "mp", "trna"], "article_id"=>595510, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_numbers_of_additional_steps_S_required_to_force_molecules_sharing_the_first_second_third_or_the_first_two_bases_in_codons_into_monophyly_during_MP_analyses_of_the_combined_tRNA_structure_and_sequence_data_/595510", "title"=>"The numbers of additional steps (S) required to force molecules sharing the first, second, third, or the first two bases in codons into monophyly during MP analyses of the combined tRNA structure and sequence data.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-07-30 01:31:50"}
{"files"=>["https://ndownloader.figshare.com/files/925097"], "description"=>"The length of the most parsimonious trees derived from the combined data set was 10,083 steps. Each constrained group is given in parentheses and groups of tRNA isoacceptors were labeled with IUPAC 3-letter amino acid nomenclature.", "links"=>[], "tags"=>["numbers", "steps", "molecules", "monophyly", "amino", "chronology", "constraints", "mp", "trna"], "article_id"=>595545, "categories"=>["Evolutionary Biology", "Biochemistry"], "users"=>["Feng-Jie Sun", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002799.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_numbers_of_additional_steps_S_required_to_force_molecules_into_monophyly_based_on_amino_acid_chronology_constraints_during_MP_analyses_of_combined_tRNA_structure_and_sequence_data_/595545", "title"=>"The numbers of additional steps (S) required to force molecules into monophyly based on amino acid chronology constraints during MP analyses of combined tRNA structure and sequence data.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-07-30 01:32:25"}

PMC Usage Stats 130317 Jan 14:42 UTC

PMC Usage Stats

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Relative Metric 97565005 Apr 21:45 UTC

Relative Metric

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F1000Prime13 Jan 12:04 UTC

F1000Prime

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