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Downloading Them Directly from the GO bioRxiv preprint doi: https://doi.org/10.1101/284828; this version posted March 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Title: Evolution of the D. melanogaster chromatin landscape and its associated proteins Authors and affiliations: Elise Parey(1, 2) and Anton Crombach*(1,3) (1) Center for Interdisciplinary Research in Biology (CIRB), Collè!e de France, C#RS, IN$ERM, P$& Uni(ersit) Paris, 75005 Paris, France (2) (c-rrent address) Institut de Biologie de l’Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, P$& Uni(ersit) Paris, 75005 Paris, France (3) (current address) Inria, Antenne Lyon La Doua, 69603 Villeurbanne, France Author for Correspondence (*): Anton Crombach, Center for Interdisciplinary Research in Biology (CIRB), Collè!e de France, CNRS, I#$ERM, P$& Uni(ersit) Paris, 75005 Paris, "rance, anton.crombach@colle!e0de-france.fr Keywords: phylogenomics, chromatin-associated proteins, chromatin types, histone modi1cations, centromere dri(e, D. melanogaster. 1 of 46 bioRxiv preprint doi: https://doi.org/10.1101/284828; this version posted March 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Abstract (221w, max 250w) In the nucleus of eukaryotic cells, !enomic 3#A associates 4ith numerous protein comple5es and RNAs, forming the chromatin landscape. 6hrough a !enome04ide study of chromatin- associated proteins in Drosophila cells, 1(e ma7or chromatin types 4ere identi1ed as a re1nement of the traditional binary division into hetero- and euchromatin. These fi(e types are de1ned by distinct but o(erlapping combinations of proteins and differ in biological and biochemical properties, including transcriptional activity, replication timing and histone modi1cations. In this 4ork, 4e assess the e(olutionary relationships of chromatin-associated proteins and present an inte!rated vie4 of the e(olution and conser(ation of the fruit 9y D. melanogaster chromatin landscape. :e combine homology prediction across a 4ide range of species 4ith !ene a!e inference methods to determine the origin of each chromatin- associated protein. 6his provides insight into the emer!ence of the different chromatin types. ;ur results indicate that the t4o euchromatic types, <E&&;: and RE3, 4ere one single acti(ating type that split early in eukaryotic history. #e5t, 4e provide evidence that =REE#0 associated proteins are in(ol(ed in a centromere dri(e and expanded in a linea!e-speci1c 4ay in D. melanogaster. ;ur results on &'E chromatin support the hypothesis that the emer!ence of Polycomb =roup proteins is linked to eukaryotic multicellularity. In light of these results, 4e discuss ho4 the regulatory comple5i1cation of chromatin links to the origins of eukaryotic multicell-larity. 2 of 46 bioRxiv preprint doi: https://doi.org/10.1101/284828; this version posted March 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Introduction 6he chromatin landscape consists of 3#A, histones and other associated proteins and RNAs, and plays a fundamental role in de(elopment, cell-lar memory, and inte!ration of e5ternal signals. As a uni>ue feature of the eukaryotic cell, it is closely tied to the e(olution of eukaryotes, both re!arding their ori!in and the ma7or transition(s) to multicell-larity (Ne4man 2005; Aravind et al. 2014; =ombar et al. 2014; Penny et al. 2014; %iyamoto et al. 2015; $eb)0Pedrós et al. 2017). At a basic le(el, chromatin is responsible for maintenance, or!aniBation, and correct use of the !enome. Cistone proteins packa!e and condense 3#A in the nucleus, and act as a docking platform for hundreds of structural and regulatory proteins. A (ariety of re(ersible post-translational modi1cations of histones, kno4n as epi!enetic marks, promote the recruitment of speci1c proteins. 6his creates a local context for nuclear processes such as transcriptional activity, replication, as 4ell as 3#A-repair. 6hese and other epi!enetic mechanisms in(ol(ed in chromatin modi1cation ha(e been extensi(ely characteriBed in (ariety of eukaryotic species, 4hich led to the obser(ation that the chromatin landscape is effecti(ely subdivided into a small set of distinct chromatin states (Filion et al. 2010; Ernst et al. 2011; Roudier et al. 2011). A lar!ely open >uestion, ho4e(er, is ho4 these chromatin states ha(e (co-)e(ol(ed. In this 4ork, 4e assess the e(olutionary relationships of chromatin-associated proteins (CAPs) and present an inte!rated vie4 of the e(olution and conser(ation of the fruit fly D. melanogaster chromatin landscape. 3 of 46 bioRxiv preprint doi: https://doi.org/10.1101/284828; this version posted March 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Classically, chromatin is divided into t4o states, namely heterochromatin and euchromatin, the former a compacted 3#A state in 4hich transcription is mostly repressed and the latter an open, transcriptionally acti(e configuration. 6his classi1cation has been re1ned into multiple types of chromatin. In partic-lar, a breakthrough result 4as presented by "ilion et al., 4ho established 1(e ma7or chromatin types in D. melanogaster, named 4ith the colors <E&&;:, RE3, =REE#, &'E, and &ACK. 6o do so, they used !enome04ide binding profiles of CAPs obtained via 3amID (Vogel et al. 2007; Filion et al. 2010; van Bemmel et al. 2013). 6his approach is complementary to more commonly used !enome04ide histone mark pro1ling techni>ues, such as ChiP-se>. #e(ertheless, both are consistent 4ith each other and ser(e as independent (alidation. Indeed, the 1(e types can be mapped to an alternati(e classi1cation into nine chromatin states, that is deri(ed from histone modi1cations (Kharchen2o et al. 2011). 6he 1(e chromatin types ha(e different biological and biochemical properties. <E&&;: and RE3 are t4o types of e-chromatin. <E&&;: mainly marks ubi>-itously expressed house2eeping !enes. In contrast, the !enes harbored in RE3 sho4 more restricted expression patterns and are lin2ed to speci1c tissues and de(elopmental processes. Both euchromatin types are replicated in early $ phase, and of the t4o, RE3 tends to be replicated 1rst (Filion et al. 2010). =REE#, &'E, and &ACK are three types of heterochromatin. =REE# is considered a type of constit-ti(e heterochromatin. It is identi1ed by CP1-related proteins and is especially pre(alent in pericentric regions as 4ell as on chromosome @. &'E is fac-ltati(e heterochromatin and concerns mostly !enes speci1cally repressed during 4 of 46 bioRxiv preprint doi: https://doi.org/10.1101/284828; this version posted March 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. de(elopment. It is notably composed of the Polycomb =roup (Pc=) proteins, 4hich 4ere ori!inally disco(ered in D. melanogaster to repress Co5 !enes, and 4ere later found to ha(e a !eneral role in de(elopment. (Le4is 1978; 3uncan 1982; Boyer et al. 2006; &ee et al. 2006; #H!re et al. 2006). "inally, &ACK is a ma7or repressi(e type, co(ering G+I of silent !enes, 4hose underlying repressi(e molec-lar mechanisms remain poorly characteriBed (Filion et al. 2010). "rom an e(ol-tionary point of vie4, although prokaryotes ha(e specialiBed proteins associated 4ith their D#A, they do not share homology with eukaryotic CAPs (Lui7sterburg et al. 2008). In !eneral, e(olution of chromatin and di(ersi1cation of epi!enetic mechanisms are s-!!ested to be tightly linked 4ith eukaryotic e(olution, from its origin to the transition to multicell-larity (Ne4man 2005; Aravind et al. 2014; =ombar et al. 2014; Penny et al. 2014; %iyamoto et al. 2015; $eb)0Pedrós et al. 2017). Indeed, the &ast Eukaryotic Common Ancestor (LECA) is considered to possess the 2ey components of eukaryotic epi!enetics, including most histone modi1cation enzymes and some histone mark readers (Aravind et al. 2014). In addition, a current hypothesis on the transition to m-lticell-larity is that complexi1cation of the regulatory !enome, via the emer!ence of repressi(e chromatin conte5ts and distal regulatory elements, permitted to !enerate the cell-type0speci1c transcriptional programs re>uired for multicellularity (Larroux et al. 2006; %endoza et al. 2013; $eb)-Pedrós et al. 2016, 2017; Arenas0%ena 2017; Cinman J Cary 2017). Recently, a system0le(el vie4 of the e(olution of the chromatin modi1cation machinery 4as provided by (On et al. 2010). 6hey demonstrated the high conser(ation of a core of chromatin proteins 5 of 46 bioRxiv preprint doi: https://doi.org/10.1101/284828; this version posted March 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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