Gravity‐induced PIN3b polarization redirects auxin fluxes and transcriptional reprogramming to drive tension wood formation in Populus

ABSTRACT

Tension wood formation enables angiosperm trees to maintain upright growth through asymmetric secondary xylem development; yet, the primary physical signal that initiates this process remains unclear. Here, using Populus as a model system, we experimentally decoupled gravitational orientation from mechanical strain through clinostat rotation and controlled stem bending. We show that a persistent gravity vector is essential for tension wood (TW) induction, whereas mechanical strain alone is insufficient. Gravity perception in secondary growth stems is associated with endodermal amyloplast sedimentation and coincides with gravity‐dependent lateral repolarization of the auxin efflux carrier PIN3b. This polarity shift establishes a sustained auxin maximum on the upper side of the cambial cylinder and leads to coordinated transcriptional repression of regulators controlling cambial cell proliferation, vessel differentiation, and lignification. Targeted reactivation of individual auxin‐repressed transcription factors in TW‐forming tissues selectively restores these developmental outputs, demonstrating that tension wood formation is genetically modular rather than governed by a single unified program. Together, these findings define a gravity‐driven signaling pathway linking gravity perception to hormone transport polarity and cambial fate specification, extending classical models of gravitropism to secondary growth and providing a molecular basis for adaptive wood formation and the engineering of wood properties.