Multiscale mechanics of hydraulic actuation in plants

Pulvinus organs are joint-like motor organs that power active leaf folding in many plants. To understand the underlying mechanical principles, we built a soft hydraulic actuator that mimics pulvinus structure and bending mechanics. Adding circumferential hoop reinforcements to the hydraulic "cells" made from soft silicone dramatically improved its bending performance, and we hypothesized that biological pulvinus organs may contain analogous reinforcements that guide tissue swelling during rapid turgor changes. To validate this in vivo, we used osmotic baths to swell live, isolated pulvinus organs and tissues and screened for nonuniform changes in their 3D shape. Organs displayed strongly anisotropic swelling behavior at all hierarchical scales studied, indicating that structural specializations control turgor-induced shape changes at multiple spatial scales. Specialized cell wall and epidermis morphologies revealed by electron microscopy support this interpretation. Our findings provide insight into plant motor strategies, underscore the hierarchical, emergent nature of biomechanical systems, and highlight design principles that can inform the development of biologically inspired soft actuators.