Functional links between nuclear architecture and epigenome reprogramming during plant adaptive responses to light – ChromaLight

Nuclear rearrangements will be analyzed using time-resolved experiments at multiple scales - from the nucleosome (by chromatin immuno-precipitation and ATAC-seq) to the genome topology level (using cytogenetics and Hi-C of cotyledon nuclei) and to transcriptional control (through RNA polymerase 2 monitoring and quantitative RNA-seq). To dissect the spatio-temporal sequence of events, computational methods will be developed to assess whether (1) 3D genome topology reshaping relies on attraction points and their local sequence and chromatin properties; (2) the transition between states correspond to abrupt or gradual rearrangements; and (3) the establishment of a new transcriptional program shows temporal and functional links with nuclear rearrangements. Extensive plant genetic resources in which chromatin changes are impaired will allow us to test for functional dependencies between the different regulatory layers. We will also pay particular attention to the importance of transposable elements silencing on nearby genes expression and on genome topology.

Analyses of the generated data are in progress.

This study is expected to contribute significantly to the intense efforts devoted to decipher how epigenetic states influence adaptive responses of multicellular organisms to environmental cues, a topic to which plants have much to offer. Photomorphogenic responses constitute a critical step of the plant life cycle, the SAR notably having a profound impact on agricultural yield and ecological success in natural contexts. In the long term, the knowledge on the regulatory mechanisms that reshape genome topology might enable the development of novel non-GMO approaches funded in epigenetics for the engineering of plant genome function.

- Rutowicz K, Lirski M, Mermaz B, Schubert J, Teano G, Mestiri I, Kroten M, Tohnyui F, Fritz S, Grob S, Ringli C, Cherkezeyan L, Barneche F, Jerzmanowski A, Baroux C (2019) Linker histones are fine-scale chromatin architects modulating developmental decisions in Arabidopsis. Genome Biology 20: 157. Doi: 10.1186/s13059-019-1767-3

-Bourbousse C., Barneche F. and C. Laloi (2020) Plant Chromatin Catches the Sun. Front. Plant Sci. 10:1728. doi: 10.3389/fpls.2019.01728

Reshuffling of nuclear architecture and of the chromatin landscape is a recurrent theme orchestrated in many, if not all, developmental transitions and adaptive responses of eukaryotic organisms. Uncovering the influence of such processes on gene expression is revolutionizing current views in developmental and evolutionary biology. The linear epigenomic information obtained for prevalent chromatin states, notably influencing DNA accessibility, has just begun to converge with spatial 3-dimensional data obtained by cytogenetic and Chromosome Conformation Capture (3C, HiC)-based methodologies. The mechanistic and functional relationships linking nuclear rearrangements with epigenome and genome expression programs largely remain to be identified, in particular in photosynthetic organisms. The aim of the ChromaLight project is to decipher the mechanisms mediating environmentally-controlled changes in nuclear organization, and to understand how functional determinants of the epigenome influence changes in genome topology and transcriptional activity. To tackle these fundamental aspects of cell specification, we propose to exploit a synchronous biological system easily amenable to manipulation. Recent work from the converging fields of plant chromatin and sensory biology uncovered that Arabidopsis seedling de-etiolation involves massive reprogramming of genome expression that coincides with the subnuclear repositioning of light-induced genes and with the condensation of large heterochromatic domains in most cells of cotyledon embryonic leaves. Work by Partner 1 and his collaborators further unveiled that triggering a Shade Avoidance Response (SAR) by exposing plants to suboptimal light conditions trigger mirroring heterochromatin dynamics in the same organ, thus representing an ideal framework for functional analyses in a model plant species. We will compare and contrast these two light-controlled developmental adaptations, in which changes in light availability/quality profoundly impact nuclear organization, epigenomic profiles and metabolism. Nuclear rearrangements will be analyzed using time-resolved experiments at multiple scales - from the nucleosome (by chromatin immuno-precipitation and ATAC-seq) to the genome topology level (using cytogenetics and Hi-C established in Partner 3 laboratory). To dissect the spatio-temporal sequence of events, computational methods will be developed by Partner 2 to assess whether (1) 3D genome topology reshaping relies on attraction points and their local sequence and chromatin properties; (2) the transition between states correspond to abrupt or gradual rearrangements; and (3) the establishment of a new transcriptional program shows temporal and functional links with nuclear rearrangements. Extensive plant genetic resources in which chromatin changes are impaired will allow us to test for functional dependencies between the different regulatory layers. Among the molecular determinants investigated, a focus will be given to a light-controlled linker histone H1 variant that was recently found by Partner 1 and collaborators to drive heterochromatin rearrangements during photomorphogenesis. We will also pay particular attention to the importance of transposable elements silencing on nearby genes expression and on genome topology. This study is expected to contribute significantly to the intense efforts devoted to decipher how epigenetic states influence adaptive responses of multicellular organisms to environmental cues, a topic to which plants have much to offer. Photomorphogenic responses constitute a critical step of the plant life cycle, the SAR notably having a profound impact on agricultural yield and ecological success in natural contexts. In the long term, the knowledge on the regulatory mechanisms that reshape genome topology might enable the development of novel non-GMO approaches funded in epigenetics for the engineering of plant genome function.