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9 results on '"Christopher D. R. Wyatt"'

1. A developmentally programmed splicing failure contributes to DNA damage response attenuation during mammalian zygotic genome activation

Author

Christopher D. R. Wyatt, Barbara Pernaute, André Gohr, Marta Miret-Cuesta, Lucia Goyeneche, Quirze Rovira, Marion C. Salzer, Elvan Boke, Ozren Bogdanovic, Sophie Bonnal, and Manuel Irimia

Subjects
Mammals, Multidisciplinary, Genome, Embriologia, Zygote, Embryonic Development, Gene Expression Regulation, Developmental, Embryo, Mammalian, Genòmica, Mice, Animals, Cattle, Female, Genètica, DNA Damage
Abstract

Transition from maternal to embryonic transcriptional control is crucial for embryogenesis. However, alternative splicing regulation during this process remains understudied. Using transcriptomic data from human, mouse, and cow preimplantation development, we show that the stage of zygotic genome activation (ZGA) exhibits the highest levels of exon skipping diversity reported for any cell or tissue type. Much of this exon skipping is temporary, leads to disruptive noncanonical isoforms, and occurs in genes enriched for DNA damage response in the three species. Two core spliceosomal components, Snrpb and Snrpd2, regulate these patterns. These genes have low maternal expression at ZGA and increase sharply thereafter. Microinjection of Snrpb/d2 messenger RNA into mouse zygotes reduces the levels of exon skipping at ZGA and leads to increased p53-mediated DNA damage response. We propose that mammalian embryos undergo an evolutionarily conserved, developmentally programmed splicing failure at ZGA that contributes to the attenuation of cellular responses to DNA damage. This work was funded by the Spanish Ministerio de Ciencia grants BFU2014-55076-P, BFU2017-89201-P and PID2020-115040GB-I00 (M.I.), Marie Skłodowska-Curie actions grant H2020-MSCA-IF-2014_ST-656843 (B.P.), La Caixa PhD fellowship (C.D.R.W.), and “Centro de Excelencia Severo Ochoa 2013-2017” SEV-2012-0208 (CRG-MI)

Published
2022

2. The molecular basis of socially mediated phenotypic plasticity in a eusocial paper wasp

Author

Max Reuter, Benjamin A. Taylor, Seirian Sumner, Alessandro Cini, and Christopher D. R. Wyatt

Subjects
0106 biological sciences, 0301 basic medicine, Bioinformatics, Science, Wasps, education, Gene regulatory network, General Physics and Astronomy, Polistes dominula, 010603 evolutionary biology, 01 natural sciences, Article, General Biochemistry, Genetics and Molecular Biology, Machine Learning, 03 medical and health sciences, Gene expression, Animals, Humans, Gene Regulatory Networks, Social Behavior, Paper wasp, Phenotypic plasticity, Multidisciplinary, biology, Gene Expression Profiling, Computational Biology, General Chemistry, Animal behaviour, biology.organism_classification, Adaptation, Physiological, Phenotype, Eusociality, Gene Ontology, 030104 developmental biology, Evolutionary biology, Female, Adaptation, Transcriptome, Entomology, Algorithms
Abstract

Phenotypic plasticity, the ability to produce multiple phenotypes from a single genotype, represents an excellent model with which to examine the relationship between gene expression and phenotypes. Analyses of the molecular foundations of phenotypic plasticity are challenging, however, especially in the case of complex social phenotypes. Here we apply a machine learning approach to tackle this challenge by analyzing individual-level gene expression profiles of Polistes dominula paper wasps following the loss of a queen. We find that caste-associated gene expression profiles respond strongly to queen loss, and that this change is partly explained by attributes such as age but occurs even in individuals that appear phenotypically unaffected. These results demonstrate that large changes in gene expression may occur in the absence of outwardly detectable phenotypic changes, resulting here in a socially mediated de-differentiation of individuals at the transcriptomic level but not at the levels of ovarian development or behavior., Connecting genotypes to complex social behaviour is challenging. Taylor et al. use machine learning to show a strong response of caste-associated gene expression to queen loss, wherein individual wasp’s expression profiles become intermediate between queen and worker states, even in the absence of behavioural changes.

Published
2021

3. Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings

Author

Ignacio Maeso, Carlos Vargas-Chávez, Ana Alcaina, Christopher D. R. Wyatt, Alex de Mendoza, Julio Rozas, Marta Gut, Jèssica Gómez-Garrido, Isabel Almudi, Bernhard Misof, Tyler Alioto, Panos N. Firbas, Stein Aerts, Ferdinand Marlétaz, Alejandro Sánchez-Gracia, Manuel Irimia, Patricia Medina, Roberto Feuda, Josefa González, Joel Vizueta, Ryan Lister, Giulio Masiero, Kristofer Davie, Fernando Cruz, Jordi Paps, Fernando Casares, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Ministerio de Ciencia, Innovación y Universidades (España), European Commission, and European Research Council

Subjects
Gills, Male, 0106 biological sciences, 0301 basic medicine, Insecta, Genome, Insect, General Physics and Astronomy, Genes, Insect, Insect, 01 natural sciences, Genome, FAMILIES, Mayfly, Wings, Animal, lcsh:Science, Phylogeny, GENE-EXPRESSION, media_common, Multidisciplinary, Gene Expression Regulation, Developmental, Functional genomics, Genomics, EVOLUTIONARY ORIGIN, Adaptation, Physiological, 3. Good health, Multidisciplinary Sciences, Fauna marina, INSIGHTS, DROSOPHILA, Sister group, Science & Technology - Other Topics, Female, Evolutionary developmental biology, animal structures, PROTEINS, Science, media_common.quotation_subject, ODORANT-BINDING, CONSERVATION, Biology, 010603 evolutionary biology, Adaptació animal, Article, General Biochemistry, Genetics and Molecular Biology, Evolution, Molecular, 03 medical and health sciences, Phylogenetics, REVEALS, Animals, TRANSCRIPTOME, Nymph, Animal adaptation, Ephemeroptera, Life Cycle Stages, Science & Technology, Genètica animal, fungi, Cloeon dipterum, General Chemistry, biology.organism_classification, Insectes, Genòmica, 030104 developmental biology, Evolutionary biology, Molecular evolution, lcsh:Q, Gene expression, Adaptation, Animal genetics
Abstract

The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects., This project was mainly funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie Grant Agreement 657732 to I.A., Grant BFU2015-66040-P to F.Ca., institutional Grant MDM-2016-0687 (MINECO, Spain). Additional funding was provided by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (ERC-StG-LS2-637591 to M.I.), the Spanish Ministerio de Ciencia (BFU2017-89201-P to M.I., RYC-2016-20089 and PGC2018-099392-A-I00 to I.M.).

Published
2020

4. Deconstructing Superorganisms and Societies to Address Big Questions in Biology

Author

Edmund R Hunt, Christopher D. Pull, Fabio Manfredini, Christopher D. R. Wyatt, Takao Sasaki, Seirian Sumner, Solenn Patalano, Bitao Qiu, Gemma L. Baron, Patrick Kennedy, Daisy Taylor, Heikki Helanterä, Thomas A. O’Shea-Wheller, and Dalial Freitak

Subjects
0301 basic medicine, Behavior, Animal, Ecology, superorganism, Superorganism, eusociality, Environmental ethics, Isoptera, Social behaviour, Biology, Biological Evolution, Hymenoptera, model organisms, Group decision-making, social behaviour, 03 medical and health sciences, Multicellular organism, 030104 developmental biology, genomics, Animals, automated monitoring, Social Behavior, Ecology, Evolution, Behavior and Systematics, Sociality
Abstract

Social insect societies are long-standing models for understanding social behaviour and evolution. Unlike other advanced biological societies (such as the multicellular body), the component parts of social insect societies can be easily deconstructed and manipulated. Recent methodological and theoretical innovations have exploited this trait to address an expanded range of biological questions. We illustrate the broadening range of biological insight coming from social insect biology with four examples. These new frontiers promote open-minded, interdisciplinary exploration of one of the richest and most complex of biological phenomena: sociality.

Published
2017

5. High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp polistes canadensis

Author

Robin J. Southon, Emily Bell, Seirian Sumner, Andrew N. Radford, Peter Graystock, and Christopher D. R. Wyatt

Subjects
Male, 0106 biological sciences, 0301 basic medicine, GENOMIC DNA, Wasps, HYMENOPTERA, 01 natural sciences, Nesting Behavior, single nucleotide polymorphisms, Nest, KIN RECOGNITION, reproductive skew, biology, Ecology, Reproduction, inclusive fitness, Inclusive fitness, Eusociality, PAIRWISE RELATEDNESS, Female, Polistes, Social evolution, Life Sciences & Biomedicine, Genetic Markers, relatedness, Biochemistry & Molecular Biology, Genotype, Kin recognition, Panama, Environmental Sciences & Ecology, Polymorphism, Single Nucleotide, 010603 evolutionary biology, Polistes canadensis, single-nucleotide polymorphisms (SNPs), 03 medical and health sciences, Genetics, Animals, SOCIAL-BEHAVIOR, Ecology, Evolution, Behavior and Systematics, Sociality, Evolutionary Biology, Science & Technology, R-PACKAGE, GENETIC RELATEDNESS, COLONY, 06 Biological Sciences, Helping Behavior, biology.organism_classification, 030104 developmental biology, PRIMITIVELY EUSOCIAL WASP, Genetic Fitness, Microsatellite Repeats, REPRODUCTIVE-SKEW
Abstract

Explaining the evolution of helping behaviour in the eusocial insects where non-reproductive ('worker') individuals help raise the offspring of other individuals ('queens'), remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on non-tropical species, where seasonality causes family groups to disperse; cofoundresses forming new colonies the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes - Polistes canadensis. Using both microsatellites and newly-developed single-nucleotide polymorphism (SNP) markers we show that adult cofoundresses are highly related, and that brood production is monopolised by a single female across the nesting cycle. Non-reproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life-history and ecologies when considering the evolution of reproductive strategies.

Published
2019

6. Amphioxus functional genomics and the origins of vertebrate gene regulation

Author

Patrick Wincker, Pierre Pontarotti, Elisa de la Calle-Mustienes, Zbynek Kozmik, Malcolm Perry, José Luis Gómez-Skarmeta, Cristian Cañestro, Stéphanie Bertrand, Yamile Marquez, Èlia Benito-Gutiérrez, Juan J. Tena, Hector Escriva, Alexandra Louis, Anthony Leon, Matthew T. Weirauch, Juan Ramón Martínez-Morales, Panos N. Firbas, Peter W. H. Holland, Iryna Kozmikova, Daniel Aldea, Sandra Jiménez-Gancedo, Jordi Garcia-Fernàndez, Jean-Marc Aury, Michael Schubert, Paul Edward Duckett, Beatriz Albuixech-Crespo, Simon J. van Heeringen, Boris Lenhard, Piero Carninci, Carlos Herrera-Úbeda, Olivier Mirabeau, Demian Burguera, Lorena Buono, Tokiharu Takahashi, Rafael D. Acemel, Silvia Naranjo, Ryan Lister, Sophie Mangenot, Lucie Subirana, Ksenia Skvortsova, Jr-Kai Yu, Hugues Roest Crollius, Ildiko M. L. Somorjai, Vincent Laudet, Piotr J. Balwierz, Gabriel A. B. Marais, Ignacio Maeso, Anlong Xu, Christopher D. R. Wyatt, Shengfeng Huang, Ozren Bogdanovic, David E. K. Ferrier, Ferdinand Marlétaz, Salvatore D'Aniello, Jon Permanyer, Filipe Castro, Manuel Irimia, Ricard Albalat, Yann Le Petillon, Ensieh Farahani, Hervé Seitz, Okinawa Institute of Science and Technology Graduate University (OIST), Department of Zoology [Oxford], University of Oxford, Centro Andaluz de Biología del Desarrollo, Universidad Pablo Olavide, University of New South Wales [Sydney] (UNSW), The University of Western Australia (UWA), Imperial College London, Universitat Pompeu Fabra [Barcelona] (UPF), Biologie intégrative des organismes marins (BIOM), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Banyuls (OOB), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Barcelona Institute of Science and Technology (BIST), Universidad Pablo de Olavide [Sevilla] (UPO), Radboud University [Nijmegen], University of Barcelona, Garvan Institute of medical research, Institute of Molecular Genetics of the Czech Academy of Sciences (IMG / CAS), Czech Academy of Sciences [Prague] (CAS), Institut de biologie de l'ENS Paris (IBENS), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Department of Genetics and IrBio, University of Cambridge [UK] (CAM), Universidade do Porto = University of Porto, Stazione Zoologica Anton Dohrn (SZN), University of St Andrews [Scotland], Sun Yat-Sen University [Guangzhou] (SYSU), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Microbes évolution phylogénie et infections (MEPHI), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Biologie du Développement de Villefranche sur mer (LBDV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Institut de génétique humaine (IGH), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), University of Manchester [Manchester], Université Paris sciences et lettres (PSL), Academia Sinica, RIKEN Center for Life Science Technologies (RIKEN CLST), RIKEN - Institute of Physical and Chemical Research [Japon] (RIKEN), University of Cincinnati (UC), University of Bergen (UiB), ANR-16-CE12-0008,CHORELAND,Détermination de la conservation du landscape génomique de régulation au cours de l'embryogenèse des chordés(2016), European Project: 637591,H2020,ERC-2014-STG,NEURAL AS(2015), European Project: 658521,H2020,H2020-MSCA-IF-2014,EVOREL(2016), European Project: 268513,EC:FP7:ERC,ERC-2010-AdG_20100317,GENEVA(2011), European Commission, The Leverhulme Trust, University of St Andrews. School of Biology, University of St Andrews. Marine Alliance for Science & Technology Scotland, University of St Andrews. Scottish Oceans Institute, University of St Andrews. Biomedical Sciences Research Complex, University of Oxford [Oxford], Radboud university [Nijmegen], Garvan Institute of Medical Research, Institut de biologie de l'ENS Paris (UMR 8197/1024) (IBENS), École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Universidade do Porto, Commission of the European Communities, Biotechnology and Biological Sciences Research Council (BBSRC), Wellcome Trust, Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Département de Biologie - ENS Paris, Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU), Departament de Genetica, Facultat de Biologia, Universitat de Barcelona (UB), Centro Andaluz de Biología del Desarrollo, Consejo Superior de Investigaciones Científicas, Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Banyuls (OOB), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Max F. Perutz Laboratories, University of Vienna [Vienna], DYnamique et Organisation des GENomes - Equipe de l'IBENS (DYOGEN), École normale supérieure - Paris (ENS Paris)-École normale supérieure - Paris (ENS Paris)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris)-École normale supérieure - Paris (ENS Paris)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut de Génétique et Développement de Rennes (IGDR), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-IFR140-Centre National de la Recherche Scientifique (CNRS), Stress, Immunité, Pathogènes (SIMPA), Université de Lorraine (UL), Unité de Biométrie et Intelligence Artificielle (UBIA), Institut National de la Recherche Agronomique (INRA), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut de Génomique d'Evry (IG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Departament de Genètica, Universitat Autònoma de Barcelona [Barcelona] (UAB), Texas A&M University [College Station], Sun Yat-Sen University (SYSU), Institut de Génomique Fonctionnelle de Lyon (IGFL), École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), Sexe et évolution, Département PEGASE [LBBE] (PEGASE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup (VAS)-Centre National de la Recherche Scientifique (CNRS), Laboratoire d'Analyse, Topologie, Probabilités (LATP), Université Paul Cézanne - Aix-Marseille 3-Université de Provence - Aix-Marseille 1-Centre National de la Recherche Scientifique (CNRS), Unité de génétique et biologie des cancers (U830), Université Paris Descartes - Paris 5 (UPD5)-Institut Curie-Institut National de la Santé et de la Recherche Médicale (INSERM), University of Medical Sciences / Beijing, Institute of Cellular and Organismic Biology, Ctr Life Sci Technol, Div Gen Technol, Tsurumi Ku, RIKEN, Centre of Excellence in Plant Energy Biology (ARC), Australian National University (ANU)-School of Biochemistry and Molecular Biology, SARS International Centre for Marine Molecular Biology, Modèles en biologie cellulaire et évolutive (MBCE), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Banyuls (OOB), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), European Research Council, Ministerio de Economía y Competitividad (España), Australian Research Council, Maeso, Ignacio [0000-0002-6440-8457], Tena, Juan J [0000-0001-8165-7984], Perry, Malcolm [0000-0001-5228-3434], Wyatt, Christopher DR [0000-0001-8033-2213], de la Calle-Mustienes, Elisa [0000-0002-8975-6503], Bertrand, Stephanie [0000-0002-0689-0126], Naranjo, Silvia [0000-0002-4529-3332], Jimenez-Gancedo, Sandra [0000-0002-2247-1319], Aldea, Daniel [0000-0001-5101-0194], Buono, Lorena [0000-0002-5457-4515], Louis, Alexandra [0000-0001-7032-5650], Balwierz, Piotr J [0000-0002-1548-4605], Aury, Jean-Marc [0000-0003-1718-3010], Albalat, Ricard [0000-0003-0282-9595], Benito-Gutiérrez, Èlia [0000-0003-2435-0948], Cañestro, Cristian [0000-0003-4623-8105], Castro, Filipe [0000-0001-7697-386X], Ferrier, David EK [0000-0003-3247-6233], Schubert, Michael [0000-0002-2341-712X], Seitz, Hervé [0000-0001-8172-5393], Somorjai, Ildiko [0000-0001-5243-6664], Takahashi, Tokiharu [0000-0002-5785-8660], Yu, Jr-Kai [0000-0001-8591-0529], Carninci, Piero [0000-0001-7202-7243], Martinez-Morales, Juan Ramon [0000-0002-4650-4293], Garcia-Fernàndez, Jordi [0000-0001-5677-5970], Lister, Ryan [0000-0001-6637-7239], Escriva, Hector [0000-0001-7577-5028], Irimia, Manuel [0000-0002-2179-2567], Apollo - University of Cambridge Repository, CIIMAR - Centro Interdisciplinar de Investigação Marinha e Ambiental, COMBE, Isabelle, Détermination de la conservation du landscape génomique de régulation au cours de l'embryogenèse des chordés - - CHORELAND2016 - ANR-16-CE12-0008 - AAPG2016 - VALID, Functions and evolutionary impact of transcriptomic novelties in the vertebrate brain - NEURAL AS - - H20202015-04-01 - 2020-03-31 - 637591 - VALID, Evolution of Regulatory Landscapes in Chordates - EVOREL - - H20202016-01-01 - 2017-12-31 - 658521 - VALID, Genome Evolution in the Animal Kingdom - GENEVA - - EC:FP7:ERC2011-06-01 - 2016-05-31 - 268513 - VALID, Institute of Molecular Genetics of the Czech Academy of Sciences, Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'Énergie Atomique et aux Énergies Alternatives (CEA) - Grenoble, Laboratoire de Biologie Moléculaire de la Cellule (LBMC), École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut de Mathématiques de Marseille (I2M), Centre National de la Recherche Scientifique (CNRS)-Ecole Centrale de Marseille (ECM)-Aix Marseille Université (AMU), Riken Omics Science Center, Riken Yokohama Institute, Cincinnati Children's Hospital Medical Center, and Computational Regulatory Genomics

Subjects
Epigenomics, Branchiostoma, genetic analysis, animal cell, transcriptomics, 0302 clinical medicine, [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases, vertebrate, zebra fish, histone modification, Branchiostoma lanceolatum, ComputingMilieux_MISCELLANEOUS, comparative study, Lancelets, Regulation of gene expression, DDC model, DNA methylation, adult, Vertebrate, Genomics, priority journal, Science & Technology - Other Topics, Molecular Developmental Biology, LANDSCAPES, whole genome duplication, Functional genomics, chordate evolution, CONSERVATION, embryo, gene sequence, PLURIPOTENCY, Article, animal tissue, 03 medical and health sciences, regulatory genomics, biology.animal, genomics, Humans, genome, mouse, Science & Technology, Molecular Sequence Annotation, TRANSGENESIS, DNA Methylation, Ancestral expression, developmental stage, 030104 developmental biology, hourglass model, Amfiox, Evolutionary biology, molecular genetics, chromatin, Subfunctionalization, transcriptome, 030217 neurology & neurosurgery, CHROMATIN, 0301 basic medicine, Branchiostoma Lanceolatum, Genome, specialization, Gene duplication, Vertebrats, Promoter Regions, Genetic, Whole-genome Duplication (WGD), Multidisciplinary, gene control, BRANCHIOSTOMA-LANCEOLATUM, innovation, Multidisciplinary Sciences, female, SEQ, Vertebrates, [SDV.MHEP.MI] Life Sciences [q-bio]/Human health and pathology/Infectious diseases, Phylotypic Period, General Science & Technology, invertebrate, QH426 Genetics, Biology, DNA DEMETHYLATION, male, evolution, Animals, controlled study, gene, QH426, multigene family, Body Patterning, Vertebrata, nonhuman, Amphioxus, ZEBRAFISH, gene duplication, embryo development, DAS, biology.organism_classification, EVOLUTION, [SDV.BDD.EO]Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis, Gene Expression Regulation, gene expression, Molecular evolution, Transcriptome
Abstract

Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that—in vertebrates—over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations., This research was funded primarily by the European Research Council (ERC) under the European Union’s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Economía y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208), the ‘Unidad de Excelencia María de Maetzu 2017-2021’(MDM-2016-0687), the People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program FP7 under REA grant agreement number 607142 (DevCom) to J.L.G.-S., and the CNRS and the ANR (ANR16-CE12-0008-01) to H.E. O.B. was supported by an Australian Research Council Discovery Early Career Researcher Award (DECRA; DE140101962).

Published
2018

7. Evolutionary origin and functional divergence of totipotent cell homeobox genes in eutherian mammals

Author

Juan A. Bernal, Manuel Irimia, Ignacio Maeso, Ferdinand Marlétaz, Shan Quah, Christopher D. R. Wyatt, Thomas L. Dunwell, Borbála Vető, Peter W. H. Holland, European Research Council, Ministerio de Economía y Competitividad (España), and Fundación La Caixa

Subjects
0301 basic medicine, Transcription, Genetic, Physiology, Plant Science, MOUSE, Genome, MULTIPLE SEQUENCE ALIGNMENT, Structural Biology, Gene Duplication, Gene duplication, Tandem duplication, PHYLOTYPIC STAGE, Genetics, Mammals, Agricultural and Biological Sciences(all), Genes, Homeobox, Gene Expression Regulation, Developmental, Placental, Asymmetric evolution, FAMILY, Embryo, Chromosomal region, General Agricultural and Biological Sciences, STEM-CELLS, Biotechnology, Research Article, Embryonic Development, Homeodomain, Cell fate determination, Biology, ANTERIOR, General Biochemistry, Genetics and Molecular Biology, Evolution, Molecular, 03 medical and health sciences, EMBRYOS, Protein Domains, XENOPUS-LAEVIS, Animals, CRX GENES, Gene, Ecology, Evolution, Behavior and Systematics, Cell Nucleus, Base Sequence, Biochemistry, Genetics and Molecular Biology(all), Cell Biology, Embryo, Mammalian, 030104 developmental biology, Homeobox, Ectopic expression, VERTEBRATE, Totipotent Stem Cells, PRD, Functional divergence, Developmental Biology
Abstract

Background: A central goal of evolutionary biology is to link genomic change to phenotypic evolution. The origin of new transcription factors is a special case of genomic evolution since it brings opportunities for novel regulatory interactions and potentially the emergence of new biological properties. Results: We demonstrate that a group of four homeobox gene families (Argfx, Leutx, Dprx, Tprx), plus a gene newly described here (Pargfx), arose by tandem gene duplication from the retinal-expressed Crx gene, followed by asymmetric sequence evolution. We show these genes arose as part of repeated gene gain and loss events on a dynamic chromosomal region in the stem lineage of placental mammals, on the forerunner of human chromosome 19. The human orthologues of these genes are expressed specifically in early embryo totipotent cells, peaking from 8-cell to morula, prior to cell fate restrictions; cow orthologues have similar expression. To examine biological roles, we used ectopic gene expression in cultured human cells followed by high-throughput RNA-seq and uncovered extensive transcriptional remodelling driven by three of the genes. Comparison to transcriptional profiles of early human embryos suggest roles in activating and repressing a set of developmentally-important genes that spike at 8-cell to morula, rather than a general role in genome activation. Conclusions: We conclude that a dynamic chromosome region spawned a set of evolutionarily new homeobox genes, the ETCHbox genes, specifically in eutherian mammals. After these genes diverged from the parental Crx gene, we argue they were recruited for roles in the preimplantation embryo including activation of genes at the 8-cell stage and repression after morula. We propose these new homeobox gene roles permitted fine-tuning of cell fate decisions necessary for specification and function of embryonic and extra-embryonic tissues utilised in mammalian development and pregnancy. This work was supported primarily by the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013 ERC grant 268513) to PWHH. In addition, support was provided by the Spanish Ministry of Economy and Competitiveness (BFU2014-55076-P) to MI and a fellowship from `la Caixa'-Severo Ochoa to CDRW. Sí

Published
2016

8. The alternative splicing factor Nova2 regulates vascular development and lumen formation

Author

Claudia Ghigna, Stefania Gallo, Carla Taveggia, Federica Pisati, Elisabetta Ferrero, Elisa Belloni, Gianluca Deflorian, Valeria Quaranta, Fabrizio Orsenigo, Benjamin J. Blencowe, Serena Bonomi, Christopher D. R. Wyatt, Daniel Nyqvist, Pier Paolo Di Fiore, Costanza Giampietro, Stefano Confalonieri, Anna Di Matteo, Elisabetta Dejana, Giuseppe Biamonti, Manuel Irimia, Davide Pradella, Giovanni Bertalot, and Evelien Fredrickx

Subjects
Endothelium, Angiogenesis, Regulator, General Physics and Astronomy, Lumen (anatomy), Neovascularization, Physiologic, RNA-binding protein, Biology, Neurones -- Fisiologia, General Biochemistry, Genetics and Molecular Biology, Article, Neovascularization, Exon, Mice, Antigens, Neoplasm, Neuro-Oncological Ventral Antigen, medicine, Animals, Cardiac and Cardiovascular Systems, Cells, Cultured, Multidisciplinary, Kardiologi, Alternative splicing, Endothelial Cells, RNA-Binding Proteins, General Chemistry, Anatomy, Cell biology, Angiogènesi, Alternative Splicing, medicine.anatomical_structure, Endothelium, Vascular, medicine.symptom
Abstract

Vascular lumen formation is a fundamental step during angiogenesis; yet, the molecular mechanisms underlying this process are poorly understood. Recent studies have shown that neural and vascular systems share common anatomical, functional and molecular similarities. Here we show that the organization of endothelial lumen is controlled at the post-transcriptional level by the alternative splicing (AS) regulator Nova2, which was previously considered to be neural cell-specific. Nova2 is expressed during angiogenesis and its depletion disrupts vascular lumen formation in vivo. Similarly, Nova2 depletion in cultured endothelial cells (ECs) impairs the apical distribution and the downstream signalling of the Par polarity complex, resulting in altered EC polarity, a process required for vascular lumen formation. These defects are linked to AS changes of Nova2 target exons affecting the Par complex and its regulators. Collectively, our results reveal that Nova2 functions as an AS regulator in angiogenesis and is a novel member of the ‘angioneurins' family., The alternative splicing factor Nova2 is best known for its pivotal function in the brain. Giampietro et al. reveal an important role for Nova2 in the regulation of alternative splicing of transcripts in the vascular endothelium that are crucial for the maintenance of endothelial cell polarity and vessel lumen formation in zebrafish.

Published
2015

9. Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Author

James E. Tarver, Claire Asher, Martin Bachman, Pedro G. Ferreira, Irene González-Navarrete, Ana Vlasova, Fabio S. Nascimento, Marina Marcet-Houben, Ernesto Lowy, Solenn Patalano, William O. H. Hughes, Roderic Guigó, Wolf Reik, Philip Ewels, Heinz Himmelbauer, Christopher D. R. Wyatt, Jose Luis Rodriguez-Ales, Francisco Camara, Anne Segonds-Pichon, André E. Minoche, Tomasz P. Jurkowski, Seirian Sumner, Felix Krueger, Shankar Balasubramanian, Toni Gabaldón, Simon Andrews, Bachman, Martin [0000-0003-3903-6492], and Apollo - University of Cambridge Repository

Subjects
Genome, Insect, Molecular Sequence Data, Wasps, Hierarchy, Social, Phenotypic plasticity, Biology, Genome sequencing, Polistes canadensis, Genome, Transcriptomes, Animals, Social Behavior, Gene, health care economics and organizations, Seqüència de nucleòtids, EVOLUÇÃO SOCIAL, Genetics, Social evolution, DNA methylation, Multidisciplinary, Base Sequence, Models, Genetic, Ants, Mechanism (biology), Insectes -- Genètica, fungi, Brain, High-Throughput Nucleotide Sequencing, Biological Sciences, Eusociality, Phenotype, MicroRNAs, Gene Expression Regulation, Adaptation, Transcriptome
Abstract

Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity. This work was funded by Natural Environment Research Council Grants NE/G000638/1, NBAF581, and NE/K011316/1 (to S.S.) and Grant NE/G012121/1 (to W.O.H.H. and S.S.); the Research Councils UK (S.S); the Cancer Research UK Grant C14303/A17197 (to S.B); the Leverhulme Trust (W.O.H.H.); German Federal Ministry of Education and Research Grant FKZ 0315962 B; CRG core funding (to H.H.); Spanish Ministry of Economy and Competitiveness (MINECO) Grant BIO2012-37161 (to T.G.); MINECO Grant BIO2011-26205 (to R.G.); Instituto de Salud Carlos III Grant PT13/0001/0021 (to R.G.); the Instituto Nacional de Bioinformatica and Agència de Gestió d’Ajuts Universitaris i de Recerca (R.G.); Wellcome Trust Grants 095645/Z/11/Z (to W.R.) and WT099232 (to S.B); Biotechnology and Biological Sciences Research Council Grant BB/K010867/1 (to W.R.); the Stuttgart Universität (T.P.J.); and Fundaçao de Amparo à Pesquisa do Estado de Sao Paulo Grant 2010/10027-5 (to F.S.N.).

Published
2015

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