Control of organ shape development by cellular mechanical properties

Coordination of growth between tissue layers is necessary for proper organ development in multicellular organisms. In plants, the differential growth between connected tissues generates “mechanical conflicts” which are believed to regulate 3D organ shape. However, the role of different tissue layers during this process is still unclear.

Here we use the anther – the floral male reproductive organ – as a model system to investigate this question. Combining live-microscopy, 3D image analysis, genetics, mechanical manipulations and modeling, we show that localized fast growth in internal cell layers drives the initiation of the organ complex shape. To explain this growth differential, we model the pressurization of an ideal plant tissue with finite element simulations. We propose the growth gradient is caused by a differential in ‘effective mechanical density’, a dimensionless parameter which links cell size, cell wall thickness and stiffness, as well as hydrostatic pressure. Simulations also show that forces acting at the tissue scale, so called ‘tissue tension’ emerge from such gradients, as confirmed by observing cell shapes in real tissues. Contrary to the commonly accepted assumptions, our results demonstrate that the magnitude of tissue tension does not depend on organ size, but on gradient of cell density.