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

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          Summary

          Bending of trees causes a transient hydraulic overpressure signal that propagates rapidly along the vascular system in planta. This may be a mechanobiological remote signalling of the mechanical stress.

          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.

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          Most cited references21

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          Hydraulic signals in long-distance signaling.

          Higher plants are sessile organisms that continuously adapt their metabolism and development in response to a changing environment. Control of water uptake and the maintenance of water status are key for the survival and optimal growth of plants. Environmental factors such as radiation, air temperature, rainfall, and humidity have a high impact on plant water relations. Hence, plants require a coordinated and timely response in above-ground and below-ground organs to cope with the changing need to take up and preserve water. In this review we will focus on changes in plant water availability and on how information on the water status is communicated to remote plant organs. We will summarize the current knowledge of long-distance signaling by hydraulic cues and of potential sensors required to convert a physical signal into a chemical messenger, namely the plant hormone abscisic acid (ABA). Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Xylem wall collapse in water-stressed pine needles.

            Wall reinforcement in xylem conduits is thought to prevent wall implosion by negative pressures, but direct observations of xylem geometry during water stress are still largely lacking. In this study, we have analyzed the changes in xylem geometry during water stress in needles of four pine species (Pinus spp.). Dehydrated needles were frozen with liquid nitrogen, and xylem cross sections were observed, still frozen, with a cryo-scanning electron microscope and an epifluorescent microscope. Decrease in xylem pressure during drought provoked a progressive collapse of tracheids below a specific threshold pressure (P(collapse)) that correlates with the onset of cavitation in the stems. P(collapse) was more negative for species with smaller tracheid diameter and thicker walls, suggesting a tradeoff between xylem efficiency, xylem vulnerability to collapse, and the cost of wall stiffening. Upon severe dehydration, tracheid walls were completely collapsed, but lumens still appeared filled with sap. When dehydration proceeded further, tracheids embolized and walls relaxed. Wall collapse in dehydrated needles was rapidly reversed upon rehydration. We discuss the implications of this novel hydraulic trait on the xylem function and on the understanding of pine water relations.
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              Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2.

              Hydraulic properties (half-time of water exchange, T1/2, and hydraulic conductivity, Lp; T1/2 approximately 1/Lp) of individual cells in the cortex of young corn roots were measured using a cell pressure probe for up to 6 h to avoid variations between cells. When pulses of turgor pressure of different size were imposed, T1/2 (Lp) responded differently depending on the size. Pulses of smaller than 0.1 MPa, which induced a small proportional water flow, caused no changes in T1/2 (Lp). Medium-sized pulses of between 0.1 and 0.2 MPa caused an increase in T1/2 (decrease in Lp) by a factor of 4 to 23. The effects caused by medium-sized pulses were reversible within 5-20 min. When larger pulses of more than 0.2 MPa were employed, changes were not reversible within 1-3 h, but could be reversed within 30 min in the presence of 500 nM of the stress hormone ABA. Cells with a short T1/2 responded to the aquaporin blocker mercuric chloride (HgCl2). The treatment had no effect on cells which exhibited long T1/2 following a mechanical inhibition by the large-pulse treatment. Step decreases in pressure resulted in the same inhibition as step increases. Hence, the treatment did not cause a stretch-inhibition of water channels and was independent of the directions of both pressure changes and water flows induced by them. It is concluded that inhibition is caused by the absolute value of intensities of water flow within the channels, which increased in proportion to the size of step changes in pressure. Probable mechanisms by which the mechanical stimuli are perceived are (i) the input of kinetic energy to the channel constriction (NPA motif of aquaporin) which may cause a conformational change of the channel protein (energy-input model) or (ii) the creation of tensions at the constriction analogous to Bernoulli's principle for macroscopic pores (cohesion-tension model). Estimated rates of water flow within the pores were a few hundred micro m s-1, which is too small to create sufficient tension. They were much smaller than those proposed for AQP1. Based on literature data of single-channel permeability of AQP1, a per channel energy input of 200 kBxT (kB=Boltzmann constant) was estimated for the energy-input model. This should be sufficient to initiate changes of protein conformation and an inactivation of channels. The data indicate different closed states which differ in the amount of distortion and the rates at which they relax back to the open state.
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                Author and article information

                Journal
                J Exp Bot
                J. Exp. Bot
                jexbot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                May 2014
                20 February 2014
                20 February 2014
                : 65
                : 8
                : 1997-2008
                Affiliations
                1Anatomía, Fisiología y Genética vegetal, ETSI Montes, Universidad Politécnica de Madrid , Spain
                2INRA , UMR547 PIAF, F-63100 Clermont-Ferrand, France
                3Clermont Université, Université Blaise Pascal , UMR547 PIAF, F-63000 Clermont-Ferrand, France
                Author notes
                * These authors contributed equally to this work.
                To whom correspondence should be addressed. E-mail: eric.badel@ 123456clermont.inra.fr
                Article
                10.1093/jxb/eru045
                3991735
                24558073
                0d3daaa2-6a6d-48d2-be07-01ac64505b1b
                © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Pages: 12
                Categories
                Research Paper

                Plant science & Botany
                bending,conductivity,hydraulic,mechanosensing,poroelasticity,pressure,signalling,strain,trees,wood,water.

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