Chromatin structure changes in Daphnia populations upon exposure to environmental cues – or – The discovery of Wolterecks “Matrix”
2020
Augusto, Ronaldo de Carvalho | Minoda, Aki | Rey, Oliver | Cosseau, Céline | Chaparro, Cristian | Vidal-Dupiol, Jeremie | Allienne, Jean-François | Duval, David | Pinaud, Silvain | Tönges, Sina | Andriantsoa, Ranja | Luquet, Émilien | Aubret, Fabien | Dia Sow, Mamadou | David, Patrice | Thomson, Vicki | Federico, Déborah | Joly, Dominique | Lima, Mariana Gomes | Danchin, Etienne | Grunau, Christoph | Interactions Hôtes-Pathogènes-Environnements (IHPE) ; Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM) | RIKEN - Institute of Physical and Chemical Research [Japon] (RIKEN) | German Cancer Research Center - Deutsches Krebsforschungszentrum [Heidelberg] (DKFZ) | Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés (LEHNA) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-École Nationale des Travaux Publics de l'État (ENTPE)-Centre National de la Recherche Scientifique (CNRS) | Station d'écologie théorique et expérimentale (SETE) ; Université Toulouse III - Paul Sabatier (UT3) ; Université de Toulouse (UT)-Université de Toulouse (UT)-Observatoire Midi-Pyrénées (OMP) ; Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3) ; Université de Toulouse (UT)-Université de Toulouse (UT)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National d'Études Spatiales [Toulouse] (CNES)-Centre National de la Recherche Scientifique (CNRS)-Météo-France-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National d'Études Spatiales [Toulouse] (CNES)-Centre National de la Recherche Scientifique (CNRS)-Météo-France-Centre National de la Recherche Scientifique (CNRS) | Curtin University | Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC) ; Université d'Orléans (UO)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Centre d’Ecologie Fonctionnelle et Evolutive (CEFE) ; Université Paul-Valéry - Montpellier 3 (UPVM)-École Pratique des Hautes Études (EPHE) ; Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [Occitanie])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - Montpellier SupAgro ; Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro) | University of Adelaide | Evolution, génomes, comportement et écologie (EGCE) ; Institut de Recherche pour le Développement (IRD)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS) | Laboratório de Malacologia [Rio de Janeiro] ; Instituto Oswaldo Cruz = Oswaldo Cruz Institute [Rio de Janeiro] (IOC) ; Fundação Oswaldo Cruz / Oswaldo Cruz Foundation (FIOCRUZ) ; Pasteur Network (Réseau International des Instituts Pasteur)-Pasteur Network (Réseau International des Instituts Pasteur)-Fundação Oswaldo Cruz / Oswaldo Cruz Foundation (FIOCRUZ) ; Pasteur Network (Réseau International des Instituts Pasteur)-Pasteur Network (Réseau International des Instituts Pasteur) | Evolution et Diversité Biologique (EDB) ; Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3) ; Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS) | These experiments were done in the framework of the RTP 3E summer school “Epigenetics for field ecologists” and received support from the CNRS.
Phenotypic plasticity is an important feature of biological systems that is likely to play a major role in the future adaptation of organisms to the ongoing global changes. It may allow an organism to produce alternative phenotypes in responses to environmental cues. Modifications in the phenotype can be reversible but are sometimes enduring and can even span over generations. The notion of phenotypic plasticity was conceptualized in the early 20 th century by Richard Woltereck. He introduced the idea that the combined relations of a phenotypic character and all environmental gradients that influence on it can be defined as “norm of reaction”. Norms of reaction are specific to species and to lineages within species, and they are heritable. He postulated that reaction norms can progressively be shifted over generations depending on the environmental conditions. One of his biological models was the water-flee daphnia . Woltereck proposed that enduring phenotypic modifications and gene mutations could have similar adaptive effects, and he postulated that their molecular bases would be different. Mutations occurred in genes, while enduring modifications were based on something he called the Matrix . He suggested that this matrix (i) was associated with the chromosomes, (ii) that it was heritable, (iii) it changed during development of the organisms, and (iv) that changes of the matrix could be simple chemical substitutions of an unknown, but probably polymeric molecule. We reasoned that the chromatin has all postulated features of this matrix and revisited Woltereck’s classical experiments with daphnia . We developed a robust and rapid ATAC-seq technique that allows for analyzing chromatin of individual daphnia and show here (i) that this technique can be used with minimal expertise in molecular biology, and (ii) we used it to identify open chromatin structure in daphnia exposed to different environmental cues. Our result indicates that chromatin structure changes consistently in daphnia upon this exposure confirming Woltereck’s classical postulate.
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