Evolution of the Drosophila melanogaster Chromatin Landscape and Its Associated Proteins

In the nucleus of eukaryotic cells, genomic DNA associates with numerous protein complexes and RNAs, forming the chromatin landscape. Through a genome-wide study of chromatin-associated proteins in Drosophila cells, five major chromatin types were identified as a refinement of the traditional binary division into hetero- and euchromatin. These five types were given color names in reference to the Greek word chroma. They are defined by distinct but overlapping combinations of proteins and differ in biological and biochemical properties, including transcriptional activity, replication timing, and histone modifications. In this work, we assess the evolutionary relationships of chromatin-associated proteins and present an integrated view of the evolution and conservation of the fruit fly Drosophila melanogaster chromatin landscape. We combine homology prediction across a wide range of species with gene age inference methods to determine the origin of each chromatin-associated protein. This provides insight into the evolution of the different chromatin types. Our results indicate that for the euchromatic types, YELLOW and RED, young associated proteins are more specialized than old ones; and for genes found in either chromatin type, intron/exon structure is lineage-specific. Next, we provide evidence that a subset of GREEN-associated proteins is involved in a centromere drive in D. melanogaster. Our results on BLUE chromatin support the hypothesis that the emergence of Polycomb Group proteins is linked to eukaryotic multicellularity. In light of these results, we discuss how the regulatory complexification of chromatin links to the origins of eukaryotic multicellularity

Réseaux de systèmes évolutifs / Network in evolutionary systems

Publication Verd B., Clark E., Wotton K.R., Janssens H., Jiménez-Guri E., Crombach A. et Jaeger J., « A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila », PLOS Biology, vol. 16, no 2, 2018, e2003174, [première version DOI : 10.1101/068072], DOI : 10.1371/journal.pbio.2003174

Modeling Complex Biological Systems: Tackling the Parameter Curse Through Evolution

As we all know, “Nothing in biology makes sense except in the light of evolution” Dobzhansky (Am Biol Teach 35(3):125–129, 1973). Among the challenges of modeling complex biological systems is to determine the relevant parameters. The common practice is to extract parameters from the literature, or to determine them from ongoing experiments, or by collectively fitting the parameters to the experimental results the model tries to explain. Doing so ignores, or at least does not exploit, Dobzhansky’s wisdom. In this perspective paper, we argue and demonstrate the importance of using evolutionary methods to derive relevant parameters. We show that by doing so, we can debug experimental and modeling artifacts

A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila.

Insects determine their body segments in two different ways. Short-germband insects, such as the flour beetle Tribolium castaneum, use a molecular clock to establish segments sequentially. In contrast, long-germband insects, such as the vinegar fly Drosophila melanogaster, determine all segments simultaneously through a hierarchical cascade of gene regulation. Gap genes constitute the first layer of the Drosophila segmentation gene hierarchy, downstream of maternal gradients such as that of Caudal (Cad). We use data-driven mathematical modelling and phase space analysis to show that shifting gap domains in the posterior half of the Drosophila embryo are an emergent property of a robust damped oscillator mechanism, suggesting that the regulatory dynamics underlying long- and short-germband segmentation are much more similar than previously thought. In Tribolium, Cad has been proposed to modulate the frequency of the segmentation oscillator. Surprisingly, our simulations and experiments show that the shift rate of posterior gap domains is independent of maternal Cad levels in Drosophila. Our results suggest a novel evolutionary scenario for the short- to long-germband transition and help explain why this transition occurred convergently multiple times during the radiation of the holometabolan insects.MINECO BFU2009-10184/BFU2012-33775/SEV-2012-0208 European Commission FP7/KBBE-2011/5/289434 La Caixa Savings Bank (PhD fellowship to BV) KLI Klosterneuburg (PhD Writing-up & Postdoctoral Fellowships to BV) Wissenschaftskolleg zu Berlin (Wiko) (Fellowships to JJ and AC

Affiliations: ∗ Theoretical Biology and Bioinformatics Group, Utrecht University Corresponding author:

Chromosome rearrangements and the evolution of genome structuring and adaptabil-ity. (Research article

Evolutionary Systems Biology: Advances, Questions, and Opportunities

International audienceIllustrates the blossoming synergy of theory and experiment in biologyHighlights the value of evolutionary systems biology for a better understanding in (systems) genetics, synthetic biology, and metabolic engineeringExpands upon progress in the field of evolutionary development using a systems approac

Life’s Attractors Continued: Progress in Understanding Developmental Systems Through Reverse Engineering and In Silico Evolution

This manuscript is a chapter in the book "Evolutionary Systems Biology: Advances, Questions, and Opportunities" to be published with Springer-Nature.International audienceWe present a progress report on our efforts to establish a new research program for evolutionary systems biology, based on reverse-engineering and in silico evolution. The aim is a mechanistic understanding of the genotype-phenotype map and its evolution. Our review focuses on the case study of the gap gene network in dipteran insects (flies and midges). This network is the top regulatory tier of the segmentation gene hierarchy, generating a pattern of overlapping expression domains that subdivide the embryo during early embryogenesis. It is one of the best-understood developmental regulatory networks today. We have studied this system in a comparative way, across three species: the vinegar fly, Drosophila melanogaster, the scuttle fly, Megaselia abdita, and the moth midge, Clogmia albipunctata. In this context, we discuss methodological challenges concerning data processing and model-fitting, consider different functional decompositions of the gap gene network, and highlight novel insights into network evolution by compensatory developmental system drift. Finally, we discuss the prospect of simulating the phylogenesis of the gap gene network using in silico evolution. We conclude by arguing that our case study is a first step towards a more systematic empirical investigation into the principles of network evolution

Evolution of the <i>Drosophila melanogaster</i> Chromatin Landscape and Its Associated Proteins

International audienceIn the nucleus of eukaryotic cells, genomic DNA associates with numerous protein complexes and RNAs, forming the chromatin landscape. Through a genome-wide study of chromatin-associated proteins in Drosophila cells, five major chromatin types were identified as a refinement of the traditional binary division into hetero- and euchromatin. These five types were given color names in reference to the Greek word chroma. They are defined by distinct but overlapping combinations of proteins and differ in biological and biochemical properties, including transcriptional activity, replication timing, and histone modifications. In this work, we assess the evolutionary relationships of chromatin-associated proteins and present an integrated view of the evolution and conservation of the fruit fly Drosophila melanogaster chromatin landscape. We combine homology prediction across a wide range of species with gene age inference methods to determine the origin of each chromatin-associated protein. This provides insight into the evolution of the different chromatin types. Our results indicate that for the euchromatic types, YELLOW and RED, young associated proteins are more specialized than old ones; and for genes found in either chromatin type, intron/exon structure is lineage-specific. Next, we provide evidence that a subset of GREEN-associated proteins is involved in a centromere drive in D. melanogaster. Our results on BLUE chromatin support the hypothesis that the emergence of Polycomb Group proteins is linked to eukaryotic multicellularity. In light of these results, we discuss how the regulatory complexification of chromatin links to the origins of eukaryotic multicellularity

Evolution of Evolvability in Gene Regulatory Networks

Evolution of Evolvability in Gene Regulatory Network