Proprioception drives tension wood formation for autotropic straightening and postural control in trees

Abstract

Postural control in plant shoots relies on gravi- and photo- tropisms, driven by angular sensing and actuated by differential growth or reaction wood formation (tension wood in dicots). Control theory and kinematical models predict that posture stabilization additionally requires active counter-curving. This led to the hypothesis that plants actively straighten through proprioception (curvature sensing) driving autotropic actuation. However, passive springback can be involved, especially in woody stems, and direct conclusive experimental evidence for proprioception-driven autotropism has been lacking. To assess this hypothesis, we designed a novel experimental setup, allowing us to suspend phototropic and gravitropic sensing on demand along the tropic movement. We then quantified stem movement and tension wood formation - an indicator of actuation - during curving and counter-curving in poplar stems (Populus tremula × alba). We show that counter-curving results from active tension wood formation on the convex side of curved stems until straightness is recovered. Quantitative analysis revealed the curvature-dependent control law governing this response and allowed estimation of proprioceptive sensitivity. Our results establish that reaction wood formation is driven by the balance between graviperceptive and proprioceptive feedbacks, revising our textbook view of tension wood formation. They provide direct evidence that proprioception-driven autotropism is the key process for active straightening in trees.