Water enters the root through the root hairs. These extensions of epidermal cells have sickly walls and adhere tightly to soil particles with their film of moisture. Once within the epidermis, water passes through the cortex, mainly travelling between the cells. However, in order to enter the stele, it must pass through the cytoplasm of the cells of the endodermis (symplastic path). Once within the stele, water is free again to move between cells as well as through them. In young roots, water enters directly into the xylem. In older roots, it may have to pass first through a band of phloem and cambium. It does so by traveling through horizontally-elongated cells, the xylem rays. Once in the xylem, water with the minerals that have been deposited in it (as well as occasional organic molecules supplied by the root tissue) move up in the vessels (angiosperms) and tracheids (conifers). At any level, the water can leave the xylem and pass laterally to supply the needs of other tissues. At the leaves, the xylem passes into the petiole and then into the veins of the leaf. Water leaves the finest veins and enters the cells of the spongy and palisade layers. Here some of the water may be used in metabolism, but most is lost in transpiration. What Forces Water Through the Xylem? Observations The mechanism is based on purely physical forces because the xylem vessels and tracheids are lifeless. Roots are not needed. This was demonstrated over a century ago by a German botanist who sawed down an oak tree and placed the base of the trunk in a barrel of picric acid solution. The solution was drawn up the trunk, killing nearby tissues as it went. However, leaves are needed. When the acid reached the leaves and killed them, the upward movement of water ceased. Removing a band of bark from around the trunk — a process called girdling — does not interrupt the upward flow of water. Girdling removes only the phloem, not the xylem, and so the foliage does not wilt. (In due course, however, the roots — and thus the entire plant — will die because the roots cannot receive any of the food manufactured by the leaves.) Cohesion-Tension Theory In 1895, the Irish plant physiologists H. H. Dixon and J. Joly proposed that water is pulled up the plant by tension (negative pressure) from above. Water is continually being lost from leaves by transpiration. Dixon and Joly believed that the loss of water in the leaves exerts a pull on the water in the xylem ducts and draws more water into the leaf. But even the best vacuum pump can pull water up to a height of only 10 m or so. This is because a column of water that high exerts a pressure (~1 bar) just counterbalanced by the pressure of the atmosphere. How can water be drawn to the top of a tree taller than 10 m? The answer to the dilemma lies the cohesion of water molecules; that is the property of water molecules to cling to each through the hydrogen bonds they form. Some support for the theory * If sap in the xylem is under tension, we would expect the column to snap apart if air is introduced into the xylem vessel by puncturing it. This is the case. * If the water in all the xylem ducts is under tension, there should be a resulting inward pull (because of adhesion) on the walls of the ducts. This inward pull in the band of sapwood in an actively transpiring tree should, in turn, cause a decrease in the diameter of the trunk. Problems with the theory When water is placed under a high vacuum, any dissolved gases come out of solution as bubbles (as we saw above with the rattan vine). This is called cavitation. Any impurities in the water enhance the process. So measurements showing the high tensile strength of water in capillaries require water of high purity — not the case for sap in the xylem. In summary, water to move from the soil to the atmosphere, has to win a series of hydraulic resistances, which can be imputed to apoplastic, symplastic and transcellular pathways. Resistances mostly regard frictional forces along the apoplastic water pathways, but they must be implemented by involving symplastic and transmembrane pathways, as far as concerns either radial transport of water through roots, or cell-to-cell water movements in shoots and leaves . Available evidence, reviewed by Holbrook et al. (2002), and more recently provided by Siefritz et al. (2002), Melcher et al. (2003) and by Hacke and Sperry (2003), suggests a central role of water channels (aquaporins) for transmembrane water movement in plants. In particular, aquaporins are thought to control the radial movement of water through roots (Steudle and Peterson, 1998), and in living tissues adjacent to xylem vessels, aquaporins are likely involved in embolism repair (Fujiyoshi et al., 2002; De Boer and Volkov, 2003). Aquaporins are ubiquitous in plant organs, but they are particularly abundant in the plasma membranes of root tissues (Otto and Kaldenhoff, 2000; Baiges et al., 2001) and in xylem parenchyma cells (Kaldenhoff et al., 1995; Barrieu et al., 1998; Sakr et al., 2003). The role played by aquaporins in water transport may become crucial under water stress, when the proportions of water flowing through different pathways, apoplastic, symplastic or transmembrane, may change (Steudle, 2000), when water movements between leaf cells and veins may regulate stomatal function (Cochard et al., 2002), when the frequency of cycles of embolization and refilling increases (Sperry et al., 2002), and when conditions of reduced transpiration do not allow high driving forces derived from significant water potential gradients (Javot et al., 2003). At the tissue and organ level, water channels contribute to the overall water flow and hydraulic conductivity. This is most important during the water uptake by roots which is measured in the lab using the root pressure probe. Different from the cell level, the apoplastic path contributes to the overall water movement in tissues. Steudle (2001) demonstrated that apoplastic water flow may be even dominant in tissues. The contribution of each pathway depends on the physiological and environmental conditions and on the existence of apoplastic barriers such as the Casparian bands in the exo- and endodermis of roots. The work in him group has shown that three pathways have to be considered in tissues, i.e.: - the apoplastic path around protoplasts, - the symplastic path within the cytoplasmic continuum and mediated by plasmodesmata, and - the transcellular path. In roots there are, in principle, all three different pathways of radial water flow, i.e. the apoplastic, the symplastic and transcellular path. The apoplastic path may be modified by apoplastic barriers (Casparian bands in the exo- and endodermis, suberin lamellae). Suberization may vary depending on growth conditions and age of the root. Along the transcellular path, water channel activity may affect the hydraulic conductance. Since the different pathways across the root cylinder are connected with each other, there is a network of transport processes into which solute transport is integrated as well. Overall transport is best decribed by the composite transport model . According to the model, at low or zero transpiration the active accumulation of nutrient solutes creates a water flow in the root xylem along the cell-to-cells path. This results in a root pressure and a back flow of some of the water and solutes along apoplastic bypasses. A circulation flow is set up which reduces the steady root pressure and root reflection coefficients. In the transpiring plant, there is a tension in the xylem and both the cell-to-cell and apoplastic pathways are used for water uptake. This tends to increase the hydraulic conductivity. The composite transport model explains variable root hydraulic conductivity and other effects which are known for a long time For experimental reasons, the symplastic and transcellular components cannot be separated to date. They are summarized as a cell-to-cell component or path. The cell-to-cell component can be derived from measurements at the level of individual tissue cells (cell pressure probe), and the apoplastic component by difference after measuring the overall water permeability. Bulk (tissue) values of solute permeability and of reflection coefficients are measured as well. This provides additional information about pathways and transport models (as for the membrane level). This basic knowledge is badly needed to understand the mechanisms of water movement at the tissue and organ levels. Composite transport predicts that root Lpr differs depending on the nature of the force which drives the water flow. Hydrostatic pressure forces cause a much larger flow (root Lpr) than osmotic. In tree roots, differences between hydraulic and osmotic water flow are up to three orders of magnitude. This is due to an apoplastic bypass flow which dominates in transpiring plants when the root xylem is under tension (hydrostatic pressure gradient across the root cylinder). At low or zero tension, apoplastic flow ceases and the osmotic component dominates which causes a small root Lpr. The existence of apoplastic barriers modifies apoplastic bypass flow, although Casparian bands do allow the passage of some water, at least during state I of the development of the endodermis. The composite transport model introduces ideas from irreversible thermodynamics into water flow across roots. Composite root structure results in composite root transport. This means that there are in a root (as in other plant tissue) pathways of quite different selectivity (reflection coefficient) arranged in parallel. There are also different cell layers and tissue arranged in series. These have to be crossed by water and solutes. Mathematical models of tissue transport in terms of a network of osmotic and hydraulic barriers have been developed in the group. They confirm the experimental results. When attempting to understand the role of water channels, the composite transport pattern of root (tissue) transport has to be understood as well. At the leaf level, a key question is how hydraulic resistance (Tyree et al., 1999) within the leaf is distributed among petiole, major veins, minor veins, and the pathways downstream of the veins (Salleo et al., 2004). To this aim, Sack et al. (2004) partitioned the leaf hydraulic resistance (Rleaf) for sugar maple (Acer saccharum) and red oak (Quercus rubra) by measuring the resistance to water flow through leaves before and after cutting specific vein orders. Simulations using an electronic circuit analog with resistors arranged in a hierarchical reticulate network justified the partitioning of total Rleaf into component additive resistances. On average 64% and 74% of the Rleaf was situated within the leaf xylem for sugar maple and red oak, respectively. Substantial resistance—32% and 49%— was in the minor venation, 18% and 21% in the major venation, and 14% and 4% in the petiole. The large number of parallel paths (i.e. a large transfer surface) for water leaving the minor veins through the bundle sheath and out of the leaf resulted in the pathways outside the venation comprising only 36% and 26% of Rleaf. Changing leaf temperature during measurement of Rleaf for intact leaves resulted in a temperature response beyond that expected from changes in viscosity. The extra response was not found for leaves with veins cut, indicating that water crosses cell membranes after it leaves the xylem. The large proportion of resistance in the venation can explain why stomata respond to leaf xylem damage and cavitation.

Apoplastic, symplastic and transcellular water transport in plants

LOVISOLO, Claudio
2005

Abstract

Water enters the root through the root hairs. These extensions of epidermal cells have sickly walls and adhere tightly to soil particles with their film of moisture. Once within the epidermis, water passes through the cortex, mainly travelling between the cells. However, in order to enter the stele, it must pass through the cytoplasm of the cells of the endodermis (symplastic path). Once within the stele, water is free again to move between cells as well as through them. In young roots, water enters directly into the xylem. In older roots, it may have to pass first through a band of phloem and cambium. It does so by traveling through horizontally-elongated cells, the xylem rays. Once in the xylem, water with the minerals that have been deposited in it (as well as occasional organic molecules supplied by the root tissue) move up in the vessels (angiosperms) and tracheids (conifers). At any level, the water can leave the xylem and pass laterally to supply the needs of other tissues. At the leaves, the xylem passes into the petiole and then into the veins of the leaf. Water leaves the finest veins and enters the cells of the spongy and palisade layers. Here some of the water may be used in metabolism, but most is lost in transpiration. What Forces Water Through the Xylem? Observations The mechanism is based on purely physical forces because the xylem vessels and tracheids are lifeless. Roots are not needed. This was demonstrated over a century ago by a German botanist who sawed down an oak tree and placed the base of the trunk in a barrel of picric acid solution. The solution was drawn up the trunk, killing nearby tissues as it went. However, leaves are needed. When the acid reached the leaves and killed them, the upward movement of water ceased. Removing a band of bark from around the trunk — a process called girdling — does not interrupt the upward flow of water. Girdling removes only the phloem, not the xylem, and so the foliage does not wilt. (In due course, however, the roots — and thus the entire plant — will die because the roots cannot receive any of the food manufactured by the leaves.) Cohesion-Tension Theory In 1895, the Irish plant physiologists H. H. Dixon and J. Joly proposed that water is pulled up the plant by tension (negative pressure) from above. Water is continually being lost from leaves by transpiration. Dixon and Joly believed that the loss of water in the leaves exerts a pull on the water in the xylem ducts and draws more water into the leaf. But even the best vacuum pump can pull water up to a height of only 10 m or so. This is because a column of water that high exerts a pressure (~1 bar) just counterbalanced by the pressure of the atmosphere. How can water be drawn to the top of a tree taller than 10 m? The answer to the dilemma lies the cohesion of water molecules; that is the property of water molecules to cling to each through the hydrogen bonds they form. Some support for the theory * If sap in the xylem is under tension, we would expect the column to snap apart if air is introduced into the xylem vessel by puncturing it. This is the case. * If the water in all the xylem ducts is under tension, there should be a resulting inward pull (because of adhesion) on the walls of the ducts. This inward pull in the band of sapwood in an actively transpiring tree should, in turn, cause a decrease in the diameter of the trunk. Problems with the theory When water is placed under a high vacuum, any dissolved gases come out of solution as bubbles (as we saw above with the rattan vine). This is called cavitation. Any impurities in the water enhance the process. So measurements showing the high tensile strength of water in capillaries require water of high purity — not the case for sap in the xylem. In summary, water to move from the soil to the atmosphere, has to win a series of hydraulic resistances, which can be imputed to apoplastic, symplastic and transcellular pathways. Resistances mostly regard frictional forces along the apoplastic water pathways, but they must be implemented by involving symplastic and transmembrane pathways, as far as concerns either radial transport of water through roots, or cell-to-cell water movements in shoots and leaves . Available evidence, reviewed by Holbrook et al. (2002), and more recently provided by Siefritz et al. (2002), Melcher et al. (2003) and by Hacke and Sperry (2003), suggests a central role of water channels (aquaporins) for transmembrane water movement in plants. In particular, aquaporins are thought to control the radial movement of water through roots (Steudle and Peterson, 1998), and in living tissues adjacent to xylem vessels, aquaporins are likely involved in embolism repair (Fujiyoshi et al., 2002; De Boer and Volkov, 2003). Aquaporins are ubiquitous in plant organs, but they are particularly abundant in the plasma membranes of root tissues (Otto and Kaldenhoff, 2000; Baiges et al., 2001) and in xylem parenchyma cells (Kaldenhoff et al., 1995; Barrieu et al., 1998; Sakr et al., 2003). The role played by aquaporins in water transport may become crucial under water stress, when the proportions of water flowing through different pathways, apoplastic, symplastic or transmembrane, may change (Steudle, 2000), when water movements between leaf cells and veins may regulate stomatal function (Cochard et al., 2002), when the frequency of cycles of embolization and refilling increases (Sperry et al., 2002), and when conditions of reduced transpiration do not allow high driving forces derived from significant water potential gradients (Javot et al., 2003). At the tissue and organ level, water channels contribute to the overall water flow and hydraulic conductivity. This is most important during the water uptake by roots which is measured in the lab using the root pressure probe. Different from the cell level, the apoplastic path contributes to the overall water movement in tissues. Steudle (2001) demonstrated that apoplastic water flow may be even dominant in tissues. The contribution of each pathway depends on the physiological and environmental conditions and on the existence of apoplastic barriers such as the Casparian bands in the exo- and endodermis of roots. The work in him group has shown that three pathways have to be considered in tissues, i.e.: - the apoplastic path around protoplasts, - the symplastic path within the cytoplasmic continuum and mediated by plasmodesmata, and - the transcellular path. In roots there are, in principle, all three different pathways of radial water flow, i.e. the apoplastic, the symplastic and transcellular path. The apoplastic path may be modified by apoplastic barriers (Casparian bands in the exo- and endodermis, suberin lamellae). Suberization may vary depending on growth conditions and age of the root. Along the transcellular path, water channel activity may affect the hydraulic conductance. Since the different pathways across the root cylinder are connected with each other, there is a network of transport processes into which solute transport is integrated as well. Overall transport is best decribed by the composite transport model . According to the model, at low or zero transpiration the active accumulation of nutrient solutes creates a water flow in the root xylem along the cell-to-cells path. This results in a root pressure and a back flow of some of the water and solutes along apoplastic bypasses. A circulation flow is set up which reduces the steady root pressure and root reflection coefficients. In the transpiring plant, there is a tension in the xylem and both the cell-to-cell and apoplastic pathways are used for water uptake. This tends to increase the hydraulic conductivity. The composite transport model explains variable root hydraulic conductivity and other effects which are known for a long time For experimental reasons, the symplastic and transcellular components cannot be separated to date. They are summarized as a cell-to-cell component or path. The cell-to-cell component can be derived from measurements at the level of individual tissue cells (cell pressure probe), and the apoplastic component by difference after measuring the overall water permeability. Bulk (tissue) values of solute permeability and of reflection coefficients are measured as well. This provides additional information about pathways and transport models (as for the membrane level). This basic knowledge is badly needed to understand the mechanisms of water movement at the tissue and organ levels. Composite transport predicts that root Lpr differs depending on the nature of the force which drives the water flow. Hydrostatic pressure forces cause a much larger flow (root Lpr) than osmotic. In tree roots, differences between hydraulic and osmotic water flow are up to three orders of magnitude. This is due to an apoplastic bypass flow which dominates in transpiring plants when the root xylem is under tension (hydrostatic pressure gradient across the root cylinder). At low or zero tension, apoplastic flow ceases and the osmotic component dominates which causes a small root Lpr. The existence of apoplastic barriers modifies apoplastic bypass flow, although Casparian bands do allow the passage of some water, at least during state I of the development of the endodermis. The composite transport model introduces ideas from irreversible thermodynamics into water flow across roots. Composite root structure results in composite root transport. This means that there are in a root (as in other plant tissue) pathways of quite different selectivity (reflection coefficient) arranged in parallel. There are also different cell layers and tissue arranged in series. These have to be crossed by water and solutes. Mathematical models of tissue transport in terms of a network of osmotic and hydraulic barriers have been developed in the group. They confirm the experimental results. When attempting to understand the role of water channels, the composite transport pattern of root (tissue) transport has to be understood as well. At the leaf level, a key question is how hydraulic resistance (Tyree et al., 1999) within the leaf is distributed among petiole, major veins, minor veins, and the pathways downstream of the veins (Salleo et al., 2004). To this aim, Sack et al. (2004) partitioned the leaf hydraulic resistance (Rleaf) for sugar maple (Acer saccharum) and red oak (Quercus rubra) by measuring the resistance to water flow through leaves before and after cutting specific vein orders. Simulations using an electronic circuit analog with resistors arranged in a hierarchical reticulate network justified the partitioning of total Rleaf into component additive resistances. On average 64% and 74% of the Rleaf was situated within the leaf xylem for sugar maple and red oak, respectively. Substantial resistance—32% and 49%— was in the minor venation, 18% and 21% in the major venation, and 14% and 4% in the petiole. The large number of parallel paths (i.e. a large transfer surface) for water leaving the minor veins through the bundle sheath and out of the leaf resulted in the pathways outside the venation comprising only 36% and 26% of Rleaf. Changing leaf temperature during measurement of Rleaf for intact leaves resulted in a temperature response beyond that expected from changes in viscosity. The extra response was not found for leaves with veins cut, indicating that water crosses cell membranes after it leaves the xylem. The large proportion of resistance in the venation can explain why stomata respond to leaf xylem damage and cavitation.
Aquaporins: an international Course.
Torino
28/II-01/III/2005
Internat. Course on Aquaporins: biophysical and molecular mechanisms for water transport
Fondazione per le Biotecnologie
1
7
C. LOVISOLO
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