Growth directions and stiffness across cell layers determine whether tissues stay smooth or buckle.

Abstract

From smooth to buckled, nature exhibits organs of various shapes and forms. How cellular growth patterns produce smooth organ shapes such as leaves and sepals remains unclear. Here we show that unidirectional growth and comparable stiffness across both epidermal layers of Arabidopsis sepals are essential for smoothness. We identified a mutant with ectopic ASYMMETRIC LEAVES 2 (AS2) expression on the outer epidermis. Our analysis reveals that ectopic AS2 expression causes outer epidermal buckling at early stages of sepal development, due to conflicting growth directions and unequal epidermal stiffnesses. Aligning growth direction and increasing stiffness of the outer epidermis restores smoothness. Furthermore, buckling influences auxin efflux transporter protein PIN-FORMED 1 polarity to generate outgrowth in the later stages, suggesting that buckling is sufficient to initiate outgrowths. Our findings suggest that in addition to molecular cues influencing tissue mechanics, tissue mechanics can also modulate molecular signals, giving rise to well-defined shapes.