{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,12]],"date-time":"2026-03-12T01:14:42Z","timestamp":1773278082898,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010147","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,5,26]],"date-time":"2022-05-26T00:00:00Z","timestamp":1653523200000}}],"reference-count":86,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2022,5,16]],"date-time":"2022-05-16T00:00:00Z","timestamp":1652659200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["851173"],"award-info":[{"award-number":["851173"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Inferring protein-protein interactions from sequences is an important task in computational biology. Recent methods based on Direct Coupling Analysis (DCA) or Mutual Information (MI) allow to find interaction partners among paralogs of two protein families. Does successful inference mainly rely on correlations from structural contacts or from phylogeny, or both? Do these two types of signal combine constructively or hinder each other? To address these questions, we generate and analyze synthetic data produced using a minimal model that allows us to control the amounts of structural constraints and phylogeny. We show that correlations from these two sources combine constructively to increase the performance of partner inference by DCA or MI. Furthermore, signal from phylogeny can rescue partner inference when signal from contacts becomes less informative, including in the realistic case where inter-protein contacts are restricted to a small subset of sites. We also demonstrate that DCA-inferred couplings between non-contact pairs of sites improve partner inference in the presence of strong phylogeny, while deteriorating it otherwise. Moreover, restricting to non-contact pairs of sites preserves inference performance in the presence of strong phylogeny. In a natural data set, as well as in realistic synthetic data based on it, we find that non-contact pairs of sites contribute positively to partner inference performance, and that restricting to them preserves performance, evidencing an important role of phylogeny.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010147","type":"journal-article","created":{"date-parts":[[2022,5,16]],"date-time":"2022-05-16T13:33:55Z","timestamp":1652708035000},"page":"e1010147","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":20,"title":["Correlations from structure and phylogeny combine constructively in the inference of protein partners from sequences"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1590-0082","authenticated-orcid":true,"given":"Andonis","family":"Gerardos","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1650-5711","authenticated-orcid":true,"given":"Nicola","family":"Dietler","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1020-494X","authenticated-orcid":true,"given":"Anne-Florence","family":"Bitbol","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,5,16]]},"reference":[{"issue":"3","key":"pcbi.1010147.ref001","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1038\/nbt.2831","article-title":"The binary protein-protein interaction landscape of Escherichia coli","volume":"32","author":"SV Rajagopala","year":"2014","journal-title":"Nat Biotechnol"},{"key":"pcbi.1010147.ref002","doi-asserted-by":"crossref","unstructured":"Lapedes AS, Giraud BG, Liu L, Stormo GD. Correlated mutations in models of protein sequences: phylogenetic and structural effects. In: Statistics in molecular biology and genetics\u2014IMS Lecture Notes\u2014Monograph Series. vol. 33; 1999. p. 236\u2013256.","DOI":"10.1214\/lnms\/1215455556"},{"key":"pcbi.1010147.ref003","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/msb4100203","article-title":"Accurate prediction of protein-protein interactions from sequence alignments using a Bayesian method","volume":"4","author":"L Burger","year":"2008","journal-title":"Mol Syst Biol"},{"issue":"4","key":"pcbi.1010147.ref004","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1103\/PhysRev.106.620","article-title":"Information Theory and Statistical Mechanics","volume":"106","author":"ET Jaynes","year":"1957","journal-title":"Phys Rev"},{"issue":"1","key":"pcbi.1010147.ref005","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1073\/pnas.0805923106","article-title":"Identification of direct residue contacts in protein-protein interaction by message passing","volume":"106","author":"M 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Evol"},{"issue":"1","key":"pcbi.1010147.ref012","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msv211","article-title":"Coevolutionary Landscape Inference and the Context-Dependence of Mutations in Beta-Lactamase TEM-1","volume":"33","author":"M Figliuzzi","year":"2016","journal-title":"Mol Biol Evol"},{"issue":"11","key":"pcbi.1010147.ref013","doi-asserted-by":"crossref","first-page":"5873","DOI":"10.1073\/pnas.1913071117","article-title":"Epistatic contributions promote the unification of incompatible models of neutral molecular evolution","volume":"117","author":"JA de la Paz","year":"2020","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"51","key":"pcbi.1010147.ref014","doi-asserted-by":"crossref","first-page":"20533","DOI":"10.1073\/pnas.1315625110","article-title":"Coevolutionary signals across protein lineages help capture multiple protein conformations","volume":"110","author":"F Morcos","year":"2013","journal-title":"Proc Natl Acad Sci 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Hopf","year":"2014","journal-title":"Elife"},{"issue":"14","key":"pcbi.1010147.ref021","doi-asserted-by":"crossref","first-page":"5177","DOI":"10.1073\/pnas.1403770111","article-title":"Integrated strategy reveals the protein interface between cancer targets Bcl-2 and NAF-1","volume":"111","author":"S Tamir","year":"2014","journal-title":"Proc Natl Acad Sci USA"},{"key":"pcbi.1010147.ref022","doi-asserted-by":"crossref","first-page":"13652","DOI":"10.1038\/srep13652","article-title":"Dimeric interactions and complex formation using direct coevolutionary couplings","volume":"5","author":"RN dos Santos","year":"2015","journal-title":"Sci Rep"},{"issue":"2","key":"pcbi.1010147.ref023","doi-asserted-by":"crossref","first-page":"e0149166","DOI":"10.1371\/journal.pone.0149166","article-title":"Inter-Protein Sequence Co-Evolution Predicts Known Physical Interactions in Bacterial Ribosomes and the Trp Operon","volume":"11","author":"C Feinauer","year":"2016","journal-title":"PLoS 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Cong","year":"2019","journal-title":"Science"},{"issue":"1","key":"pcbi.1010147.ref027","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1038\/s41467-021-21636-z","article-title":"Large-scale discovery of protein interactions at residue resolution using co-evolution calculated from genomic sequences","volume":"12","author":"AG Green","year":"2021","journal-title":"Nat Commun"},{"issue":"2","key":"pcbi.1010147.ref028","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nsb0295-171","article-title":"A method to predict functional residues in proteins","volume":"2","author":"G Casari","year":"1995","journal-title":"Nat Struct Biol"},{"issue":"4","key":"pcbi.1010147.ref029","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.cell.2009.07.038","article-title":"Protein sectors: evolutionary units of three-dimensional structure","volume":"138","author":"N Halabi","year":"2009","journal-title":"Cell"},{"issue":"4","key":"pcbi.1010147.ref030","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1073\/pnas.1711913115","article-title":"Power law tails in phylogenetic systems","volume":"115","author":"C Qin","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"issue":"9","key":"pcbi.1010147.ref031","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/S0168-9525(96)80020-5","article-title":"The coevolution of gene family trees","volume":"12","author":"KJ Fryxell","year":"1996","journal-title":"Trends Genet"},{"issue":"2","key":"pcbi.1010147.ref032","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1006\/jmbi.2000.3732","article-title":"Co-evolution of proteins with their interaction partners","volume":"299","author":"CS Goh","year":"2000","journal-title":"J Mol Biol"},{"issue":"19","key":"pcbi.1010147.ref033","doi-asserted-by":"crossref","first-page":"7999","DOI":"10.1073\/pnas.0609962104","article-title":"Specificity in protein interactions and its relationship with sequence diversity and coevolution","volume":"104","author":"L Hakes","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"issue":"8","key":"pcbi.1010147.ref034","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1016\/j.febslet.2008.02.017","article-title":"Co-evolution and co-adaptation in protein networks","volume":"582","author":"D Juan","year":"2008","journal-title":"FEBS Lett"},{"issue":"1","key":"pcbi.1010147.ref035","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.jmb.2008.09.078","article-title":"Correlated evolution of interacting proteins: looking behind the mirrortree","volume":"385","author":"MG Kann","year":"2009","journal-title":"J Mol Biol"},{"issue":"11","key":"pcbi.1010147.ref036","doi-asserted-by":"crossref","first-page":"2567","DOI":"10.1093\/molbev\/msq144","article-title":"An integrated view of molecular coevolution in protein-protein interactions","volume":"27","author":"SC Lovell","year":"2010","journal-title":"Mol Biol Evol"},{"key":"pcbi.1010147.ref037","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1186\/1471-2148-12-238","article-title":"The origins of the evolutionary signal used to predict protein-protein interactions","volume":"12","author":"LS Swapna","year":"2012","journal-title":"BMC Evol Biol"},{"issue":"9","key":"pcbi.1010147.ref038","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1093\/protein\/14.9.609","article-title":"Similarity of phylogenetic trees as indicator of protein\u2013protein interaction","volume":"14","author":"F Pazos","year":"2001","journal-title":"Protein Eng Des Sel"},{"issue":"Suppl 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Ochoa","year":"2010","journal-title":"Bioinformatics"},{"issue":"13","key":"pcbi.1010147.ref042","doi-asserted-by":"crossref","first-page":"2166","DOI":"10.1093\/bioinformatics\/btv102","article-title":"Detection of significant protein coevolution","volume":"31","author":"D Ochoa","year":"2015","journal-title":"Bioinformatics"},{"issue":"8","key":"pcbi.1010147.ref043","doi-asserted-by":"crossref","first-page":"4285","DOI":"10.1073\/pnas.96.8.4285","article-title":"Assigning protein functions by comparative genome analysis: protein phylogenetic profiles","volume":"96","author":"M Pellegrini","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"10","key":"pcbi.1010147.ref044","doi-asserted-by":"crossref","first-page":"e1006891","DOI":"10.1371\/journal.pcbi.1006891","article-title":"A multi-scale coevolutionary approach to predict interactions between protein domains","volume":"15","author":"G Croce","year":"2019","journal-title":"PLoS Comput Biol"},{"issue":"7","key":"pcbi.1010147.ref045","doi-asserted-by":"crossref","first-page":"e1007553","DOI":"10.1371\/journal.pcbi.1007553","article-title":"Scalable phylogenetic profiling using MinHash uncovers likely eukaryotic sexual reproduction genes","volume":"16","author":"D Moi","year":"2020","journal-title":"PLoS Comput Biol"},{"issue":"11","key":"pcbi.1010147.ref046","doi-asserted-by":"crossref","first-page":"e1006401","DOI":"10.1371\/journal.pcbi.1006401","article-title":"Inferring interaction partners from protein sequences using mutual information","volume":"14","author":"AF Bitbol","year":"2018","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010147.ref047","doi-asserted-by":"crossref","first-page":"032413","DOI":"10.1103\/PhysRevE.101.032413","article-title":"Statistical physics of interacting proteins: Impact of dataset size and quality assessed in synthetic sequences","volume":"101","author":"CA Gandarilla-P\u00e9rez","year":"2020","journal-title":"Phys Rev E"},{"issue":"10","key":"pcbi.1010147.ref048","doi-asserted-by":"crossref","first-page":"e1007179","DOI":"10.1371\/journal.pcbi.1007179","article-title":"Phylogenetic correlations can suffice to infer protein partners from sequences","volume":"15","author":"G Marmier","year":"2019","journal-title":"PLoS Comput Biol"},{"issue":"11","key":"pcbi.1010147.ref049","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pcbi.1006526","article-title":"Synthetic protein alignments by CCMgen quantify noise in residue-residue contact prediction","volume":"14","author":"S Vorberg","year":"2018","journal-title":"PLOS Computational Biology"},{"issue":"11","key":"pcbi.1010147.ref050","doi-asserted-by":"crossref","DOI":"10.3390\/e21111090","article-title":"Toward Inferring Potts Models for Phylogenetically Correlated Sequence Data","volume":"21","author":"E Rodriguez Horta","year":"2019","journal-title":"Entropy"},{"issue":"5","key":"pcbi.1010147.ref051","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1008957","article-title":"On the effect of phylogenetic correlations in coevolution-based contact prediction in proteins","volume":"17","author":"E Rodriguez Horta","year":"2021","journal-title":"PLoS Comput Biol"},{"issue":"2","key":"pcbi.1010147.ref052","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1006\/jmbi.1996.0167","article-title":"An evolutionary trace method defines binding surfaces common to protein families","volume":"257","author":"O Lichtarge","year":"1996","journal-title":"J Mol Biol"},{"issue":"3","key":"pcbi.1010147.ref053","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1093\/bioinformatics\/btm604","article-title":"Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction","volume":"24","author":"SD Dunn","year":"2008","journal-title":"Bioinformatics"},{"issue":"1","key":"pcbi.1010147.ref054","doi-asserted-by":"crossref","first-page":"012707","DOI":"10.1103\/PhysRevE.87.012707","article-title":"Improved contact prediction in proteins: using pseudolikelihoods to infer Potts models","volume":"87","author":"M Ekeberg","year":"2013","journal-title":"Phys Rev E"},{"issue":"10","key":"pcbi.1010147.ref055","doi-asserted-by":"crossref","DOI":"10.3390\/e21101000","article-title":"Phylogenetic weighting does little to improve the accuracy of evolutionary coupling analyses","volume":"21","author":"AJ Hockenberry","year":"2019","journal-title":"Entropy"},{"issue":"11","key":"pcbi.1010147.ref056","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.3390\/e21111127","article-title":"Coevolutionary Analysis of Protein Subfamilies by Sequence Reweighting","volume":"21","author":"D Malinverni","year":"2020","journal-title":"Entropy"},{"key":"pcbi.1010147.ref057","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1038\/s41598-021-04260-1","article-title":"Extracting phylogenetic dimensions of coevolution reveals hidden functional signals","volume":"12","author":"A Colavin","year":"2022","journal-title":"Scientific Reports"},{"key":"pcbi.1010147.ref058","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","article-title":"Highly accurate protein structure prediction with AlphaFold","volume":"596","author":"J Jumper","year":"2021","journal-title":"Nature"},{"key":"pcbi.1010147.ref059","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1126\/science.abm4805","article-title":"Computed structures of core eukaryotic protein complexes","volume":"374","author":"IR Humphreys","year":"2021","journal-title":"Science"},{"key":"pcbi.1010147.ref060","unstructured":"Evans R, O\u2019Neill M, Pritzel A, Antropova N, Senior A, Green T, et al. Protein complex prediction with AlphaFold-Multimer. BioRxiv Preprint;."},{"issue":"1","key":"pcbi.1010147.ref061","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1038\/s41467-022-28865-w","article-title":"Improved prediction of protein-protein interactions using AlphaFold2","volume":"13","author":"P Bryant","year":"2022","journal-title":"Nat Commun"},{"issue":"3","key":"pcbi.1010147.ref062","doi-asserted-by":"crossref","first-page":"032601","DOI":"10.1088\/1361-6633\/aa9965","article-title":"Inverse statistical physics of protein sequences: a key issues review","volume":"81","author":"S Cocco","year":"2018","journal-title":"Rep Prog Phys"},{"issue":"28","key":"pcbi.1010147.ref063","doi-asserted-by":"crossref","first-page":"11530","DOI":"10.1073\/pnas.1105315108","article-title":"Coordinate linkage of HIV evolution reveals regions of immunological vulnerability","volume":"108","author":"V Dahirel","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"issue":"8","key":"pcbi.1010147.ref064","doi-asserted-by":"crossref","first-page":"e1003776","DOI":"10.1371\/journal.pcbi.1003776","article-title":"The fitness landscape of HIV-1 gag: advanced modeling approaches and validation of model predictions by in vitro testing","volume":"10","author":"JK Mann","year":"2014","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010147.ref065","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/j.jcp.2014.07.024","article-title":"Fast pseudolikelihood maximization for direct-coupling analysis of protein structure from many homologous amino-acid sequences","volume":"276","author":"M Ekeberg","year":"2014","journal-title":"J Comput Phys"},{"key":"pcbi.1010147.ref066","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1186\/1471-2164-10-315","article-title":"P2CS: a two-component system resource for prokaryotic signal transduction research","volume":"10","author":"M Barakat","year":"2009","journal-title":"BMC Genomics"},{"issue":"Database issue","key":"pcbi.1010147.ref067","doi-asserted-by":"crossref","first-page":"D771","DOI":"10.1093\/nar\/gkq1023","article-title":"P2CS: a database of prokaryotic two-component systems","volume":"39","author":"M Barakat","year":"2011","journal-title":"Nucleic Acids Res"},{"issue":"4","key":"pcbi.1010147.ref068","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1093\/molbev\/msy007","article-title":"How Pairwise Coevolutionary Models Capture the Collective Residue Variability in Proteins?","volume":"35","author":"M Figliuzzi","year":"2018","journal-title":"Mol Biol Evol"},{"issue":"1","key":"pcbi.1010147.ref069","doi-asserted-by":"crossref","first-page":"5800","DOI":"10.1038\/s41467-021-25756-4","article-title":"Efficient generative modeling of protein sequences using simple autoregressive models","volume":"12","author":"J Trinquier","year":"2021","journal-title":"Nat Commun"},{"issue":"3","key":"pcbi.1010147.ref070","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0009490","article-title":"FastTree 2\u2014Approximately Maximum-Likelihood Trees for Large Alignments","volume":"5","author":"MN Price","year":"2010","journal-title":"PLOS ONE"},{"issue":"3","key":"pcbi.1010147.ref071","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1080\/00018732.2017.1341604","article-title":"Inverse statistical problems: from the inverse Ising problem to data science","volume":"66","author":"HC Nguyen","year":"2017","journal-title":"Advances in Physics"},{"issue":"6","key":"pcbi.1010147.ref072","doi-asserted-by":"crossref","first-page":"1971","DOI":"10.1088\/0305-4470\/15\/6\/035","article-title":"Convergence condition of the TAP equation for the infinite-ranged Ising spin glass model","volume":"15","author":"T Plefka","year":"1982","journal-title":"J Phys A: Math Gen"},{"key":"pcbi.1010147.ref073","doi-asserted-by":"crossref","DOI":"10.1063\/1.3057290","volume-title":"Transmission of Information: A Statistical Theory of Communications","author":"R Fano","year":"1961"},{"issue":"1","key":"pcbi.1010147.ref074","first-page":"22","article-title":"Word association norms, mutual information, and lexicography","volume":"16","author":"KW Church","year":"1990","journal-title":"Comput Linguist"},{"key":"pcbi.1010147.ref075","unstructured":"Role F, Nadif M. Handling the impact of low frequency events on co-occurrence based measures of word similarity. In: Filipe J, Fred A, editors. Proceedings of the International Conference on Knowledge Discovery and Information Retrieval (KDIR-2011). Scitepress; 2011. p. 218\u2013223."},{"key":"pcbi.1010147.ref076","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1002\/nav.3800020109","article-title":"The Hungarian Method for the assignment problem","volume":"2","author":"HW Kuhn","year":"1955","journal-title":"Naval Research Logistics Quarterly"},{"issue":"1","key":"pcbi.1010147.ref077","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1137\/0105003","article-title":"Algorithms for the Assignment and Transportation Problems","volume":"5","author":"J Munkres","year":"1957","journal-title":"Journal of the Society for Industrial and Applied Mathematics"},{"key":"pcbi.1010147.ref078","unstructured":"Buehren M. Functions for the rectangular assignment problem; 2011. Available from: https:\/\/fr.mathworks.com\/matlabcentral\/fileexchange\/6543-functions-for-the-rectangular-assignment-problem."},{"key":"pcbi.1010147.ref079","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/s41592-019-0686-2","article-title":"SciPy 1.0: Fundamental Algorithms for Scientific Computing in Python","volume":"17","author":"P Virtanen","year":"2020","journal-title":"Nature Methods"},{"issue":"34","key":"pcbi.1010147.ref080","doi-asserted-by":"crossref","first-page":"12408","DOI":"10.1073\/pnas.1413575111","article-title":"Coevolutionary information, protein folding landscapes, and the thermodynamics of natural selection","volume":"111","author":"F Morcos","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1010147.ref081","unstructured":"Ngampruetikorn V, Sachdeva V, Torrence J, Humplik J, Schwab DJ, Palmer SE. Inferring couplings in networks across order-disorder phase transitions. ArXiv Preprint; p. https:\/\/arxiv.org\/abs\/2106.02349."},{"issue":"2","key":"pcbi.1010147.ref082","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1007\/s10955-011-0229-4","article-title":"Are Biological Systems Poised at Criticality?","volume":"144","author":"T Mora","year":"2011","journal-title":"J Stat Phys"},{"key":"pcbi.1010147.ref083","volume-title":"Mathematical Population Genetics","author":"WJ Ewens","year":"1979"},{"issue":"1","key":"pcbi.1010147.ref084","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1093\/nar\/28.1.235","article-title":"The Protein Data Bank","volume":"28","author":"HM Berman","year":"2000","journal-title":"Nucleic Acids Res"},{"issue":"4","key":"pcbi.1010147.ref085","doi-asserted-by":"crossref","first-page":"e1007010","DOI":"10.1371\/journal.pcbi.1007010","article-title":"Revealing evolutionary constraints on proteins through sequence analysis","volume":"15","author":"SW Wang","year":"2019","journal-title":"PLoS Comput Biol"},{"issue":"2","key":"pcbi.1010147.ref086","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/j.cell.2009.08.032","article-title":"Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction","volume":"139","author":"P Casino","year":"2009","journal-title":"Cell"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1010147","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,5,26]],"date-time":"2022-05-26T00:00:00Z","timestamp":1653523200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010147","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,26]],"date-time":"2022-05-26T14:01:07Z","timestamp":1653573667000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010147"}},"subtitle":[],"editor":[{"given":"Jeffrey","family":"Skolnick","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,5,16]]},"references-count":86,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2022,5,16]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010147","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.11.22.469574","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,16]]}}}