Modelling wood formation and structure: power and limits of a morphogenetic gradient in controlling xylem cell proliferation and growth

Abstract

Key message: The emergence of the characteristic tree-ring pattern during xylogenesis is commonly thought to be controlled by a gradient of morphogen (auxin, TDIF peptide..). We show that this hypothesis accounts for several developmental aspects of wood formation, but not for the final anatomical structure. Context: Wood formation is a dynamic cellular process displaying three generic features: (i) meristematic cell proliferation is restricted to the small cambial zone, preventing exponential xylem radial growth along the growing season; (ii) developmental processes result in a stable zonation of the developing xylem; (iii) the resulting mature wood cells form the typical tree-ring structure made of early and late wood with a gradient of cell sizes, an important trait for wood functioning in trees and for lumber quality. The mechanisms producing these spatial-temporal patterns remain largely unknown. According to the often-cited morphogenetic-gradient hypothesis, a graded concentration profile of a signalling molecule (e.g. auxin, TDIF) controls xylogenesis by providing positional information to differentiating cells. Aims: We assessed the predictions of the morphogenetic-gradient theory. Methods: We developed a computational model of wood formation implementing hypotheses on how a morphogen flows through the developing xylem and controls cell division and growth and we tested it against data produced by studies monitoring wood formation in conifers. Results: We demonstrated that a morphogenetic gradient could indeed control xylem radial growth and wood-forming tissue zonation. However, it failed to explain the pattern of final cell sizes observed in tree-rings. We discussed the features that candidate additional regulatory mechanisms should meet.