H3.1 Eviction Marks Female Germline Precursors in Arabidopsis

Abstract

In flowering plants, germline precursors are differentiated from somatic cells. The female germline precursor of Arabidopsis thaliana is located in the internal (nucellar) tissue of the ovule, and is known as the Megaspore Mother Cell (MMC). MMC differentiation in Arabidopsis occurs when a cell in the subepidermal layer of the nucellar apex enters the meiotic program. Increasing evidence has demonstrated that MMC specification is a plastic process where the number and developmental outcome of MMCs are variable. During its differentiation, the MMC displays specific chromatin hallmarks that distinguish it from other cells within the primordium. To date, these signatures have been only analyzed at developmental stages where the MMC is morphologically conspicuous, and their role in reproductive fate acquisition remains to be elucidated. Here, we show that the histone 3 variant H3.1 HISTONE THREE RELATED 13 (HTR13) can be evicted in multiple subepidermal cells of the nucellus, but that H3.1 eviction persists only in the MMC. This pattern is established very early in ovule development and is reminiscent of the specific eviction of H3.1 that marks cell cycle exit in other somatic cell types, such as the root quiescent center (QC) of Arabidopsis. Our findings suggest that cell cycle progression in the subepidermal region of the ovule apex is modified very early in development and is associated with plasticity of reproductive fate acquisition.

Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium

“…Furthermore, our analyses unveiled new characteristics of the SMC establishment process. We found that SMC candidates emerge from within a mitotically quiescent L2 apical domain, consistent with the finding that the H3.1 histone variant HTR13 is evicted, marking cell cycle exit ( Hernandez-Lagana and Autran, 2020 ). In addition, SMC candidates have a markedly long S-phase compared to surrounding cells.…”

“…SMC fate emergence is characterized by mitotic quiescence and cellular growth in one or more L2 apical cells. SMC singleness resolution is associated with re-entry into a somatic cell cycle (this study), and re-incorporation of a replicative histone H3.1 ( Hernandez-Lagana and Autran, 2020 ) in candidates neighboring the SMC. How known epigenetic and signaling factors interplay to secure SMC singleness remains to be determined.…”

Competence for transcellular infection in the root cortex involves a post-replicative, cell-cycle exit decision inMedicago truncatula

“…(2); Figure 2-figure supplement 1A-E). Nuclear enlargement associated with a massive eviction of H3.1 typically identifies cells having completed a DNA replication round, but pausing in the following GAP phase for cell-cycle switches or exit decisions (Figure 2E; Otero et al, 2016;Lagana & Autran, 2020;Probst et al, 2020). Together, our data strongly suggest that cortical cells along the infection thread trajectory, different to their direct neighbours, exhibit a reduced proliferation potential and presumably exit the cell cycle (Figure 2 B-E).…”

The epigenetic origin of life history transitions in plants and algae

“…Megaspore mother cells (MMCs) are specified from nucellar cells of the ovule primordium, while pollen mother cells (PMCs) develop from sporogenous cells of the anther. Strikingly, both the MMC and PMC in Arabidopsis are characterized by several cytological changes at the level of chromatin, including a general decondensed chromatin state, the depletion of linker histone H1, the eviction of replicative histone H3.1 and a drastic reduction in the levels of H3K27me3 (She et al 2013;She and Baroux 2015;Hernandez-Lagana and Autran 2020). In the PMC, these changes in chromatin are accompanied by a modest RdDM-dependent increase in CHH methylation, which regulates the RNA splicing of genes required for normal progression through meiosis (Walker et al 2018).…”