Multiscale integration of environmental stimuli in plant tropism produces complex behaviors

Abstract

Plant tropism refers to the directed movement of an organ or organism in response to external stimuli. Typically, these stimuli induce hormone transport that triggers cell growth or deformation. In turn, these local cellular changes create mechanical forces on the plant tissue that are balanced by an overall deformation of the organ, hence changing its orientation with respect to the stimuli. This complex feedback mechanism takes place in a three-dimensional growing plant with varying stimuli depending on the environment. We model this multiscale process in filamentary organs for an arbitrary stimulus by linking explicitly hormone transport to local tissue deformation leading to the generation of mechanical forces and the deformation of the organ in three dimensions. We show, as examples, that the gravitropic, phototropic, nutational, and thigmotropic dynamic responses can be easily captured by this framework. Further, the integration of evolving stimuli and/or multiple contradictory stimuli can lead to complex behavior such as sun following, canopy escape, and plant twining. Significance StatementTo survive and to thrive, plants rely on their ability to sense multiple environmental signals, such as gravity or light, and respond to them by growing and changing their shape. To do so, the signals must be transduced down to the cellular level to create the physical deformations leading to shape changes. We propose a multiscale theory of tropism that takes multiple stimuli and transforms them into auxin transport that drives tissue-level growth and remodeling, thus modifying the plant shape and position with respect to the stimuli. This feedback loop can be dynamically updated to understand the response to individual stimuli or the complex behavior generated by multiple stimuli such as canopy escape or pole wrapping for climbing plants.