Modelling the spatial crosstalk between two biochemical signals explains wood formation dynamics and tree-ring structure.

Félix P Hartmann,Meriem Fournier,Éric Badel,Cyrille B K Rathgeber,Bruno Moulia,Simon Turner

doi:10.1093/jxb/eraa558

Abstract

In conifers, xylogenesis during a growing season produces a very characteristic tree-ring structure: large, thin-walled earlywood cells followed by narrow, thick-walled latewood cells. Although many factors influence the dynamics of differentiation and the final dimensions of xylem cells, the associated patterns of variation remain very stable from one year to the next. While radial growth is characterized by an S-shaped curve, the widths of xylem differentiation zones exhibit characteristic skewed bell-shaped curves. These elements suggest a strong internal control of xylogenesis. It has long been hypothesized that much of this regulation relies on a morphogenetic gradient of auxin. However, recent modelling studies have shown that while this hypothesis could account for the dynamics of stem radial growth and the zonation of the developing xylem, it failed to reproduce the characteristic tree-ring structure. Here, we investigated the hypothesis of regulation by a crosstalk between auxin and a second biochemical signal, by using computational morphodynamics. We found that, in conifers, such a crosstalk is sufficient to simulate the characteristic features of wood formation dynamics, as well as the resulting tree-ring structure. In this model, auxin controls cell enlargement rates while another signal (e.g. cytokinin, tracheary element differentiation inhibitory factor) drives cell division and auxin polar transport.

Highlights

Tree radial growth relies on the production of new cells by the cambium and their subsequent differentiation
Other signals than auxin are involved, such as the small peptide TDIF from the CLAVATA family, which enters the cambium from the phloem and maintains vascular stem cells (Hirakawa et al 2008; Etchells et al 2015); or the plant hormone cytokinin, whose regulatory effect on cambial activity has been reported in aspen (Nieminen et al 2008)
In a previous work (Hartmann et al 2017), we have shown that the morphogenetic-gradient hypothesis was not compatible with the anatomical structure of conifer tree rings

Summary

Introduction

Tree radial growth relies on the production of new cells by the cambium and their subsequent differentiation. This process presents a high level of plasticity, contributing to the ability of trees to acclimate to changing environmental conditions (Ragni and Greb 2018). Xylem radial growth generally follows a typical Gompertz curve, whose parameters depends on internal and external factors (Camarero et al 1998; Rossi et al 2003; Cuny et al 2012). The monitoring of wood formation, through microcore samplings along the growing season, reveals that the developing xylem generally displays a zonation pattern composed of (1) a division zone (or cambial zone sensu stricto), where cells grow and divide; (2) an enlargement zone, where cells grow without dividing;

Methods

Results

Conclusion