Developmental constraints modulate reproductive fate and plasticity within the Arabidopsis ovule primordium

Sexual reproduction in multicellular organisms requires the separation of the germline from the soma. In flowering plants, the formation of spore mother cells (SMCs) marks the somatic-to-reproductive cell fate transition in floral organs. The female SMC differentiates at the apex of the ovule primordium, as a single, large, and elongated subepidermal cell. However, this singleness rule is not very robust: several SMC candidates develop in some Arabidopsis accessions and mutants. Yet, the basis of this plasticity is not understood. Here we investigate whether ovule primordium growth and overarching cellular architecture serve as an instructive cue to channel the formation of a single SMC. Combining quantitative analyses of 3D cell-based information, cell cycle reporters, and 2D growth simulations, we provide a comprehensive analysis of cell proliferation and growth events that shape ovule primordium development and SMC formation. This reveals that SMC characteristics emerge earlier than previously thought, and often for more than one cell. Thus, developmental constraints gradually canalize the fate of these cells, so that a single SMC enters meiosis ultimately. Among these constraints, we explore the contribution of dynamic cell division patterns and localized cell growth anisotropy. Consistent with 2D computational simulations, the reduction of anisotropy in katanin mutants leads to altered ovule shape and cell division patterns. Such disturbance of ovule morphology is sufficient to delay SMC canalization, as multiple cells express reproductive fate markers in katanin mutant ovules. In conclusion, we show that ovule growth and shape channel SMC fate for a single cell.