{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,2]],"date-time":"2025-12-02T15:21:53Z","timestamp":1764688913466},"reference-count":43,"publisher":"Oxford University Press (OUP)","issue":"9","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013,5,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Motivation: Aligning RNAs is useful to search for homologous genes, study evolutionary relationships, detect conserved regions and identify any patterns that may be of biological relevance. Poor levels of conservation among homologs, however, make it difficult to compare RNA sequences, even when considering closely evolutionary related sequences.<\/jats:p>\n               <jats:p>Results: We describe SARA-Coffee, a tertiary structure-based multiple RNA aligner, which has been validated using BRAliDARTS, a new benchmark framework designed for evaluating tertiary structure\u2013based multiple RNA aligners. We provide two methods to measure the capacity of alignments to match corresponding secondary and tertiary structure features. On this benchmark, SARA-Coffee outperforms both regular aligners and those using secondary structure information. Furthermore, we show that on sequences in which &amp;lt;60% of the nucleotides form base pairs, primary sequence methods usually perform better than secondary-structure aware aligners.<\/jats:p>\n               <jats:p>Availability and implementation: The package and the datasets are available from http:\/\/www.tcoffee.org\/Projects\/saracoffee and http:\/\/structure.biofold.org\/sara\/.<\/jats:p>\n               <jats:p>Contact: \u00a0cedric.notredame@crg.es<\/jats:p>\n               <jats:p>Supplementary information: \u00a0Supplementary data are available at Bioinformatics online<\/jats:p>","DOI":"10.1093\/bioinformatics\/btt096","type":"journal-article","created":{"date-parts":[[2013,3,2]],"date-time":"2013-03-02T05:33:21Z","timestamp":1362202401000},"page":"1112-1119","source":"Crossref","is-referenced-by-count":19,"title":["Using tertiary structure for the computation of highly accurate multiple RNA alignments with the SARA-Coffee package"],"prefix":"10.1093","volume":"29","author":[{"given":"Carsten","family":"Kemena","sequence":"first","affiliation":[{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"},{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giovanni","family":"Bussotti","sequence":"additional","affiliation":[{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"},{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emidio","family":"Capriotti","sequence":"additional","affiliation":[{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marc A.","family":"Marti-Renom","sequence":"additional","affiliation":[{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"},{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cedric","family":"Notredame","sequence":"additional","affiliation":[{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"},{"name":"1 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain, 2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain, 3Division of Informatics, Department of Pathology, University of Alabama at Birmingham, 35249 Birmingham, AL, USA, 4Structural Genomics Team, Genome Biology Group, Centre Nacional d\u2019An\u00e0lisis Gen\u00f2mic (CNAG), 08028 Barcelona, Spain and 5Gene Regulation, Stem Cells and Cancer program, Centre for Genomic Regulation (CRG), 08003 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2013,2,28]]},"reference":[{"key":"2023012810290456600_btt096-B1","doi-asserted-by":"crossref","first-page":"2274","DOI":"10.1261\/rna.853208","article-title":"Analysis and classification of RNA tertiary structures","volume":"14","author":"Abraham","year":"2008","journal-title":"RNA"},{"key":"2023012810290456600_btt096-B2","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"2023012810290456600_btt096-B3","doi-asserted-by":"crossref","first-page":"e35","DOI":"10.1093\/bioinformatics\/btl218","article-title":"The iRMSD: a local measure of sequence alignment accuracy using structural information","volume":"22","author":"Armougom","year":"2006","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B4","doi-asserted-by":"crossref","first-page":"692","DOI":"10.3390\/a2020692","article-title":"Fast structural alignment of biomolecules using a hash table, n-grams and string descriptors","volume":"2","author":"Bauer","year":"2009","journal-title":"Algorithms"},{"key":"2023012810290456600_btt096-B5","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1093\/bioinformatics\/btk014","article-title":"Local RNA base pairing probabilities in large sequences","volume":"22","author":"Bernhart","year":"2006","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B6","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/0092-8674(92)90520-M","article-title":"The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus","volume":"71","author":"Brown","year":"1992","journal-title":"Cell"},{"key":"2023012810290456600_btt096-B7","doi-asserted-by":"crossref","first-page":"6886","DOI":"10.1093\/nar\/gkr335","article-title":"BlastR\u2013fast and accurate database searches for non-coding RNAs","volume":"39","author":"Bussotti","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B8","doi-asserted-by":"crossref","first-page":"32","DOI":"10.2174\/157489308783329823","article-title":"Computational RNA structure prediction","volume":"3","author":"Capriotti","year":"2008","journal-title":"Curr. Bioinformatics"},{"key":"2023012810290456600_btt096-B9","doi-asserted-by":"crossref","first-page":"i112","DOI":"10.1093\/bioinformatics\/btn288","article-title":"RNA structure alignment by a unit-vector approach","volume":"24","author":"Capriotti","year":"2008","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B10","doi-asserted-by":"crossref","first-page":"W260","DOI":"10.1093\/nar\/gkp433","article-title":"SARA: a server for function annotation of RNA structures","volume":"37","author":"Capriotti","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B11","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1186\/1471-2105-11-322","article-title":"Quantifying the relationship between sequence and three-dimensional structure conservation in RNA","volume":"11","author":"Capriotti","year":"2010","journal-title":"BMC Bioinformatics"},{"key":"2023012810290456600_btt096-B12","doi-asserted-by":"crossref","first-page":"W19","DOI":"10.1093\/nar\/gkn327","article-title":"SARSA: a web tool for structural alignment of RNA using a structural alphabet","volume":"36","author":"Chang","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B13","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1261\/rna.894608","article-title":"Ab initio RNA folding by discrete molecular dynamics: from structure prediction to folding mechanisms","volume":"14","author":"Ding","year":"2008","journal-title":"RNA"},{"key":"2023012810290456600_btt096-B14","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1101\/gr.2821705","article-title":"ProbCons: probabilistic consistency-based multiple sequence alignment","volume":"15","author":"Do","year":"2005","journal-title":"Genome Res."},{"key":"2023012810290456600_btt096-B15","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1186\/1471-2105-5-105","article-title":"Evaluation of the suitability of free-energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction","volume":"5","author":"Doshi","year":"2004","journal-title":"BMC Bioinformatics"},{"key":"2023012810290456600_btt096-B16","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1186\/1471-2105-7-400","article-title":"Efficient pairwise RNA structure prediction and alignment using sequence alignment constraints","volume":"7","author":"Dowell","year":"2006","journal-title":"BMC Bioinformatics"},{"key":"2023012810290456600_btt096-B17","doi-asserted-by":"crossref","first-page":"ii47","DOI":"10.1093\/bioinformatics\/bti1108","article-title":"ARTS: alignment of RNA tertiary structures","volume":"21","author":"Dror","year":"2005","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B18","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1242\/dev.005629","article-title":"The growing catalog of small RNAs and their association with distinct Argonaute\/Piwi family members","volume":"135","author":"Farazi","year":"2008","journal-title":"Development"},{"key":"2023012810290456600_btt096-B19","doi-asserted-by":"crossref","first-page":"W659","DOI":"10.1093\/nar\/gkm334","article-title":"DIAL: a web server for the pairwise alignment of two RNA three-dimensional structures using nucleotide, dihedral angle and base-pairing similarities","volume":"35","author":"Ferre","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B20","doi-asserted-by":"crossref","first-page":"2433","DOI":"10.1093\/nar\/gki541","article-title":"A benchmark of multiple sequence alignment programs upon structural RNAs","volume":"33","author":"Gardner","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B22","doi-asserted-by":"crossref","first-page":"r175","DOI":"10.1093\/nar\/16.suppl.r175","article-title":"A compilation of large subunit RNA sequences presented in a structural format","volume":"16","author":"Gutell","year":"1988","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B23","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1038\/nature07672","article-title":"Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals","volume":"458","author":"Guttman","year":"2009","journal-title":"Nature"},{"key":"2023012810290456600_btt096-B24","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1073\/pnas.93.1.397","article-title":"Smoothness within ruggedness: the role of neutrality in adaptation","volume":"93","author":"Huynen","year":"1996","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023012810290456600_btt096-B25","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1093\/nar\/gki198","article-title":"MAFFT version 5: improvement in accuracy of multiple sequence alignment","volume":"33","author":"Katoh","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B26","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1038\/nature09322","article-title":"Genome-wide measurement of RNA secondary structure in yeast","volume":"467","author":"Kertesz","year":"2010","journal-title":"Nature"},{"key":"2023012810290456600_btt096-B27","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1093\/bioinformatics\/btm404","article-title":"Clustal W and Clustal X version 2.0","volume":"23","author":"Larkin","year":"2007","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B28","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1016\/0092-8674(93)90529-Y","article-title":"The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14","volume":"75","author":"Lee","year":"1993","journal-title":"Cell"},{"key":"2023012810290456600_btt096-B29","doi-asserted-by":"crossref","first-page":"5108","DOI":"10.1093\/nar\/gkg680","article-title":"3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures","volume":"31","author":"Lu","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B30","doi-asserted-by":"crossref","first-page":"4570","DOI":"10.1093\/nar\/25.22.4570","article-title":"RAGA: RNA sequence alignment by genetic algorithm","volume":"25","author":"Notredame","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"2023012810290456600_btt096-B31","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1006\/jmbi.2000.4042","article-title":"T-Coffee: A novel method for fast and accurate multiple sequence alignment","volume":"302","author":"Notredame","year":"2000","journal-title":"J. Mol.Biol."},{"key":"2023012810290456600_btt096-B32","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.cell.2010.09.001","article-title":"Long noncoding RNAs with enhancer-like function in human cells","volume":"143","author":"Orom","year":"2010","journal-title":"Cell"},{"key":"2023012810290456600_btt096-B33","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.jmb.2004.04.058","article-title":"3DCoffee: combining protein sequences and structures within multiple sequence alignments","volume":"340","author":"O\u2019Sullivan","year":"2004","journal-title":"J. Mol. Biol."},{"key":"2023012810290456600_btt096-B34","doi-asserted-by":"crossref","first-page":"2689","DOI":"10.1093\/bioinformatics\/btq506","article-title":"R3D Align: global pairwise alignment of RNA 3D structures using local superpositions","volume":"26","author":"Rahrig","year":"2010","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B35","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1016\/j.cell.2007.05.022","article-title":"Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs","volume":"129","author":"Rinn","year":"2007","journal-title":"Cell"},{"key":"2023012810290456600_btt096-B36","doi-asserted-by":"crossref","first-page":"2264","DOI":"10.2353\/ajpath.2009.080868","article-title":"Novel biomarkers for prostate cancer including noncoding transcripts","volume":"175","author":"Romanuik","year":"2009","journal-title":"Am. J. Pathol."},{"key":"2023012810290456600_btt096-B37","doi-asserted-by":"crossref","first-page":"2715","DOI":"10.1093\/bioinformatics\/btl472","article-title":"Probalign: multiple sequence alignment using partition function posterior probabilities","volume":"22","author":"Roshan","year":"2006","journal-title":"Bioinformatics"},{"key":"2023012810290456600_btt096-B38","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1137\/0145048","article-title":"Simultaneous solution of the RNA folding, alignment and protosequence problems","volume":"45","author":"Sankoff","year":"1985","journal-title":"SIAM J.Appl. Math."},{"key":"2023012810290456600_btt096-B39","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1186\/1471-2105-9-33","article-title":"A fast structural multiple alignment method for long RNA sequences","volume":"9","author":"Tabei","year":"2008","journal-title":"BMC Bioinformatics"},{"key":"2023012810290456600_btt096-B40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0022-2836(89)90084-3","article-title":"Protein structure alignment","volume":"208","author":"Taylor","year":"1989","journal-title":"J. Mol. Biol."},{"key":"2023012810290456600_btt096-B41","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.molcel.2012.08.008","article-title":"Genome-wide measurement of RNA folding energies","volume":"48","author":"Wan","year":"2012","journal-title":"Mol. Cell"},{"key":"2023012810290456600_btt096-B42","doi-asserted-by":"crossref","first-page":"e65","DOI":"10.1371\/journal.pcbi.0030065","article-title":"Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering","volume":"3","author":"Will","year":"2007","journal-title":"PLoS Comput. Biol."},{"key":"2023012810290456600_btt096-B43","doi-asserted-by":"crossref","first-page":"1570","DOI":"10.1126\/science.1115901","article-title":"A strategy for probing the function of noncoding RNAs finds a repressor of NFAT","volume":"309","author":"Willingham","year":"2005","journal-title":"Science"},{"key":"2023012810290456600_btt096-B44","doi-asserted-by":"crossref","first-page":"e52","DOI":"10.1093\/nar\/gkn174","article-title":"R-Coffee: a method for multiple alignment of non-coding RNA","volume":"36","author":"Wilm","year":"2008","journal-title":"Nucleic Acids Res."}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/29\/9\/1112\/48897733\/bioinformatics_29_9_1112.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/29\/9\/1112\/48897733\/bioinformatics_29_9_1112.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,28]],"date-time":"2023-01-28T12:09:39Z","timestamp":1674907779000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/29\/9\/1112\/217409"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,2,28]]},"references-count":43,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2013,5,1]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btt096","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2013,5,1]]},"published":{"date-parts":[[2013,2,28]]}}}