Tourdot, E. | bioRxiv Science

bioRxiv2025

ALFIN-LIKE Proteins Orchestrate H3K4me3-H3K27me3 Crosstalk to Regulate Plant Embryogenesis

In multicellular organisms such as animals and plants, development requires the precise regulation of gene expression, mediated not only by transcription factors but also by chromatin-based mechanisms. Among these, histone modifications like H3K4me3 and H3K27me3 play opposing roles in gene activation and repression, respectively. In Arabidopsis thaliana, H3K27me3 is deposited by the Polycomb Repressive Complex 2 (PRC2), while Trithorax group (TrxG) proteins mediate H3K4me3 deposition. While the functions of these writer complexes have been extensively studied, far less is known about the histone mark readers that interpret these modifications during development. Here, we investigate the antagonistic interplay between H3K27me3 and H3K4me3 during Arabidopsis embryogenesis. We identify a developmentally specific interaction between the FIS-PRC2 complex and ALFIN-LIKE (AL) proteins--a family of plant-specific PHD domain proteins that read H3K4me3. Our findings reveal a dynamic competition between these two marks during early embryogenesis that helps shape the epigenomic landscape of the developing seed. Disruption of AL function leads to severe developmental defects and loss of cell identity in early embryos. Moreover, loss of ALs impairs H3K4me3 deposition, resulting in aberrant spreading of H3K27me3, misregulation of developmental genes, and defects that persist into adult plant traits. Together, our results show that proper embryonic development relies on a finely tuned antagonism between activating and repressive chromatin states--an interplay orchestrated not only by their writers but also by specific readers that translate these epigenetic cues into developmental outcomes.

plant biology↗

bioRxiv2023

Ploidy-specific transcriptomes shed light on the heterogeneous identity and metabolism of developing pericarp cells

Endoreduplication, during which cells increase their DNA content through successive rounds of full genome replication without cell division, is the major source of endopolyploidy in higher plants. Endoreduplication plays pivotal roles in plant growth and development and is associated with the activation of specific transcriptional programs that are characteristic to each cell type, thereby defining their identity. In plants, endoreduplication is found in numerous organs and cell types and especially in agronomically valuable ones, such as the fleshy fruit (pericarp) of tomato presenting high ploidy levels. We used the tomato pericarp tissue as a model system to explore the transcriptomes associated with endoreduplication progression during fruit growth. We confirmed that expression globally scales with ploidy level and identified sets of genes differentially expressed when comparing ploidy levels at a specific developmental stage. We found that non-endoreduplicated cells are defined by cell division state and cuticle synthesis while endoreduplicated cells are mainly defined by their metabolic activity changing rapidly over time. By combining this dataset with publicly available spatiotemporal pericarp expression data, we proposed a map describing the distribution of ploidy levels within the pericarp. These transcriptome-based predictions were validated by quantifying ploidy levels within the pericarp tissue. This in situ ploidy quantification revealed the dynamic progression of endoreduplication and its cell layer specificity during early fruit development. In summary, the study sheds light on the complex relationship between endoreduplication, cell differentiation, and gene expression patterns in the tomato pericarp. Significance statementThe progression of endoreduplication is very dynamic during early fruit development and displays cell layer specific patterns. The integration of ploidy distribution maps with ploidy-specific transcriptome data revealed that gene expression in the pericarp is controlled in a ploidy-specific manner during the early stages of tomato fruit development, resulting in the spatialization of transcriptional programs.

plant biology↗