Robust planar morphogenesis in leaf-like organs requires callose-dependent coordination of division and growth

Abstract

Planar organs, such as leaves, are key developmental innovations underlying the evolutionary success of plants. In vascular plants, building a planar organ requires coordinating cell division and growth both within the organ plane and across multiple, mechanically distinct cell layers. Phyllids, the leaf-like organs of bryophytes, typically consist of a single cell layer and offer a minimal system to decouple in-plane growth coordination from inter-layer mechanics. Here, we investigate how robust planar morphogenesis is achieved in phyllids, using the moss Physcomitrium patens as a bryophyte model. We show that impaired cytokinesis, caused by the loss of a callose synthase gene, disrupts growth gradients, ultimately yielding smaller, non-planar organs of variable shape. Combining quantitative live imaging with computational modeling, we show that the severity of shape defects in mutants depends on the spatial distribution and developmental timing of local growth arrests. These findings reveal how callose-dependent coordination between cell division and in-plane growth prevents mechanical conflicts and maintains planarity in a monolayered plant organ.