Mechanochemical Polarization of Contiguous Cell Walls Shapes Plant Pavement Cells

Abstract

The epidermis of aerial plant organs is thought to be limiting for growth, because it acts as a continuous load-bearing layer, resisting tension. Leaf epidermis contains jigsaw puzzle piece-shaped pavement cells whose shape has been proposed to be a result of subcellular variations in expansion rate that induce local buckling events. Paradoxically, such local compressive buckling should not occur given the tensile stresses across the epidermis. Using computational modeling, we show that the simplest scenario to explain pavement cell shapes within an epidermis under tension must involve mechanical wall heterogeneities across and along the anticlinal pavement cell walls between adjacent cells. Combining genetics, atomic force microscopy, and immunolabeling, we demonstrate that contiguous cell walls indeed exhibit hybrid mechanochemical properties. Such biochemical wall heterogeneities precede wall bending. Altogether, this provides a possible mechanism for the generation of complex plant cell shapes. Pavement cells in the leaf epidermis are multi-lobed like jigsaw puzzle pieces. Majda et al. provide evidence through in vivo analyses using atomic force microscopy and computational modeling that mechanical heterogeneities across and along anticlinal cell walls allow wall bending that contributes to lobe formation and these complex cell shapes