Tree shoot bending generates hydraulic pressure pulses: a new long-distance signal?

Rosana Lopez,François Beaujard,Eric Badel,Sebastien Peraudeau,Bruno Moulia,Hervé Cochard,Nathalie Leblanc-Fournier,Jean-Louis Julien

doi:10.1093/jxb/eru045

Abstract

When tree stems are mechanically stimulated, a rapid long-distance signal is induced that slows down primary growth. An investigation was carried out to determine whether the signal might be borne by a mechanically induced pressure pulse in the xylem. Coupling xylem flow meters and pressure sensors with a mechanical testing device, the hydraulic effects of mechanical deformation of tree stem and branches were measured. Organs of several tree species were studied, including gymnosperms and angiosperms with different wood densities and anatomies. Bending had a negligible effect on xylem conductivity, even when deformations were sustained or were larger than would be encountered in nature. It was found that bending caused transient variation in the hydraulic pressure within the xylem of branch segments. This local transient increase in pressure in the xylem was rapidly propagated along the vascular system in planta to the upper and lower regions of the stem. It was shown that this hydraulic pulse originates from the apoplast. Water that was mobilized in the hydraulic pulses came from the saturated porous material of the conduits and their walls, suggesting that the poroelastic behaviour of xylem might be a key factor. Although likely to be a generic mechanical response, quantitative differences in the hydraulic pulse were found in different species, possibly related to differences in xylem anatomy. Importantly the hydraulic pulse was proportional to the strained volume, similar to known thigmomorphogenetic responses. It is hypothesized that the hydraulic pulse may be the signal that rapidly transmits mechanobiological information to leaves, roots, and apices.

Highlights

In nature the wind causes tree branches to bend transiently and repeatedly (Rodriguez et al, 2008)
Pressure pulse propagation as a candidate for longdistance mechanosensing signal transmission Pressure variations transported along the vascular system of plants have been found to generate rapid physiological responses (Malone and Stanković, 1991;Tyree and Zimmerman, 2002)
Since this hydraulic pulse is transported throughout the xylem, it could have a secondary impact on the turgor pressure of living cells, leading to cell deformation and physiological and molecular responses (Ortega, 2010)

Summary

Introduction

In nature the wind causes tree branches to bend transiently and repeatedly (Rodriguez et al, 2008). Less transient bending may occur when loads such as rainwater, snow, fruit, and sometimes the shoot itself weigh branches down (Cannell and Morgan, 1989; Alméras et al, 2004). A rather generic syndrome of physiological responses to transient bending has been described and named thigmomorphogenesis (reviewed in Telewski, 2006; Coutand, 2010; Moulia et al, 2011): branches and trunks tend to reduce their elongation (Coutand and Moulia, 2000) and to increase their radial growth (Coutand et al, 2009), thereby reducing bending stresses in the shoot.

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