Evolution of the chromatin organization in plants

Genome activities are regulated by the chromatin, which consists largely of basic proteins histones that form the nucleosomes supporting the DNA. Genome wide studies have shown that combinations of histone modifications contribute to the chromatin landscape that correlates with gene transcription and silencing. More recently variants of histones H3 and H2A were also shown to affect gene expression and their proper function is required to prevent several types of cancers. Surprisingly, the combination of profiles of variants maps the position of major components of the genome such as protein-coding genes, non-protein-coding heterochromatic domains. During the evolution of plants, histone variants have diversified tremendously while the number of histone modifications remained constant, providing a unique opportunity to question whether genome organization has been shaped by a diversifying repertoire of histone variants. To address this question we propose to use a filamentous alga and a moss as models representing ancestors of land plants. Using these species, we will establish the ancestral plant chromatin landscape using a combination of genomics and high-resolution microscopy. This will enable to establish the origin of the relationship between histone variants and major genomic features during plant evolution. In addition we identified the new class of H2A.M variant present only in mosses and ferns. This class may represent an attempt to evolve a variant with properties similar to H2A.W variants that are present in flowering plants and responsible for higher order organization of heterochromatin. Hence we will study properties and functions of H2A.M in Marchantia to find clues that explain the origins of H2A.W and the cause of its selection in relation with genome three-dimensional organization. We thus plan to obtain an overview of the evolution of chromatin and genome organization in one major kingdom of eukaryotes. Phylogenetic analyses suggests a degree of convergence during histone diversification between flowering plants and mammals. Our findings related will likely find parallels between plant and animal evolution of chromatin structure, thereby broadening the impact of our study.

Evolutionary biologists have focused a large part of their efforts in understanding the origins of organisms in terms of their modes of development, as shown in EvoDevo studies. How limbs formed from fins? How heads became more complex with development or larger brains? How did cell aggregate to form more complex organisms? These are typical questions studied by evolutionary biologists. Much less attention has been devoted towards understanding the origin and changes of essential elements found in all organisms. Chromatin consists from the DNA and associated proteins that package, protect and regulate activities of the genome from its expression to its propagation through sexual reproduction. The most important of chromatin associated proteins are histones, five types of small proteins that self-assemble with DNA. In this project we have questioned the origins and diversification of histone H2A. We have focused our efforts on plants because they show a dramatic diversification of H2A. Our results have identified that this diversification occurred about 500 millions years ago when plants invaded land. We have shown that diversification of H2A led to acquisition of new biophysical properties and acquisition of new capacities to index specific elements of the genome according to their function. With efforts from other colleagues, these new insights into the impact of evolution of chromatin led the foundation of a new field of research EvoChromo. We anticipate that similar to the revolutionary changes bred by EvoDevo researchers, EvoChromo will shed new light on regulations of genomic activities that will profit our understanding of a large array of biological and medical phenomena.