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      Promoter Motifs in NCLDVs: An Evolutionary Perspective

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          Abstract

          For many years, gene expression in the three cellular domains has been studied in an attempt to discover sequences associated with the regulation of the transcription process. Some specific transcriptional features were described in viruses, although few studies have been devoted to understanding the evolutionary aspects related to the spread of promoter motifs through related viral families. The discovery of giant viruses and the proposition of the new viral order Megavirales that comprise a monophyletic group, named nucleo-cytoplasmic large DNA viruses (NCLDV), raised new questions in the field. Some putative promoter sequences have already been described for some NCLDV members, bringing new insights into the evolutionary history of these complex microorganisms. In this review, we summarize the main aspects of the transcription regulation process in the three domains of life, followed by a systematic description of what is currently known about promoter regions in several NCLDVs. We also discuss how the analysis of the promoter sequences could bring new ideas about the giant viruses’ evolution. Finally, considering a possible common ancestor for the NCLDV group, we discussed possible promoters’ evolutionary scenarios and propose the term “MEGA-box” to designate an ancestor promoter motif (‘TATATAAAATTGA’) that could be evolved gradually by nucleotides’ gain and loss and point mutations.

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          Genome-wide analysis of mammalian promoter architecture and evolution.

          Mammalian promoters can be separated into two classes, conserved TATA box-enriched promoters, which initiate at a well-defined site, and more plastic, broad and evolvable CpG-rich promoters. We have sequenced tags corresponding to several hundred thousand transcription start sites (TSSs) in the mouse and human genomes, allowing precise analysis of the sequence architecture and evolution of distinct promoter classes. Different tissues and families of genes differentially use distinct types of promoters. Our tagging methods allow quantitative analysis of promoter usage in different tissues and show that differentially regulated alternative TSSs are a common feature in protein-coding genes and commonly generate alternative N termini. Among the TSSs, we identified new start sites associated with the majority of exons and with 3' UTRs. These data permit genome-scale identification of tissue-specific promoters and analysis of the cis-acting elements associated with them.
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            The 1.2-megabase genome sequence of Mimivirus.

            We recently reported the discovery and preliminary characterization of Mimivirus, the largest known virus, with a 400-nanometer particle size comparable to mycoplasma. Mimivirus is a double-stranded DNA virus growing in amoebae. We now present its 1,181,404-base pair genome sequence, consisting of 1262 putative open reading frames, 10% of which exhibit a similarity to proteins of known functions. In addition to exceptional genome size, Mimivirus exhibits many features that distinguish it from other nucleocytoplasmic large DNA viruses. The most unexpected is the presence of numerous genes encoding central protein-translation components, including four amino-acyl transfer RNA synthetases, peptide release factor 1, translation elongation factor EF-TU, and translation initiation factor 1. The genome also exhibits six tRNAs. Other notable features include the presence of both type I and type II topoisomerases, components of all DNA repair pathways, many polysaccharide synthesis enzymes, and one intein-containing gene. The size and complexity of the Mimivirus genome challenge the established frontier between viruses and parasitic cellular organisms. This new sequence data might help shed a new light on the origin of DNA viruses and their role in the early evolution of eukaryotes.
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              A giant virus in amoebae.

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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                Viruses
                Viruses
                viruses
                Viruses
                MDPI
                1999-4915
                20 January 2017
                January 2017
                : 9
                : 1
                : 16
                Affiliations
                [1 ]Laboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, Minas Gerais, Brazil; graziufmg@ 123456yahoo.com.br (G.P.O.); ana.andrade2008@ 123456hotmail.com (A.C.d.S.P.A.); rodriguesral07@ 123456gmail.com (R.A.L.R.); tsarantes@ 123456gmail.com (T.S.A.); pvboratto@ 123456gmail.com (P.V.M.B.); ludmilakaren@ 123456gmail.com (L.K.d.S.S.); fabiopiod154@ 123456gmail.com (F.P.D.); gitrindade@ 123456yahoo.com.br (G.d.S.T.); betaniadrumond@ 123456gmail.com (B.P.D.); ernagkroon@ 123456gmail.com (E.G.K.)
                [2 ]Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE) UM63 CNRS 7278 IRD 198 INSERM U1095, Aix-Marseille Université., 27 Boulevard Jean Moulin, Faculté de Médecine, 13385 Marseille Cedex 05, France; bernard.la-scola@ 123456univ-amu.fr
                Author notes
                [* ]Correspondence: jonatas.abrahao@ 123456gmail.com ; Tel.: +55-031-3409-3002
                [†]

                These authors contributed equally to this work.

                Article
                viruses-09-00016
                10.3390/v9010016
                5294985
                28117683
                1a117217-48a6-4e19-a226-95cff2200604
                © 2017 by the authors; licensee MDPI, Basel, Switzerland.

                This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 14 November 2016
                : 05 January 2017
                Categories
                Review

                Microbiology & Virology
                megavirales,ncldv,giant viruses,promoter,transcription,evolution,mega-box
                Microbiology & Virology
                megavirales, ncldv, giant viruses, promoter, transcription, evolution, mega-box

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