Chromatin structure changes in Daphnia populations upon exposure to environmental cues – or – The discovery of Wolterecks “Matrix”

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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

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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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