The Plant Vascular System: Evolution, Development and FunctionsF

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Figure 14. The cohesion-tension mechanism for transpirationdriven xylem flow. (A) The basic hydraulic lift process: evaporation from a meniscus coupled to bulk liquid flow by capillary action. (B) In plants, surface tension created at the surface of narrow pores within the cell walls (w) acts as the energy gradient to drive longdistance bulk flow through a low-resistance network of dead xylem conduits (c). Conduits are connected by pits (p), which also protect against air-entry and embolism in the inevitable event of damage (see Figures 15, 16). Water is filtered through living cell membranes at the root endodermis (en) by reverse osmosis. (C) Living cells (rounded rectangles enclosed by hatched cell walls) do not generate transpirational flow (ep, leaf epidermis; m, mesophyll; cs, Casparian strip of the endodermis; rc, root cortex). Water flows through them to the site of evaporation via symplastic (s arrows) and apoplastic routes (a arrows). In the root, the apoplastic route (a’) is interrupted by the Casparian strip. Transpiration is actively regulated by stomatal opening through which the waterfor-carbon exchange occurs (from Sperry 2011). the cylinder radius (Pmin proportional to 1/radius), whereas the hydraulic resistivity (resistance per unit length) through the cylinder increases with 1/radius 4 . The higher the resistivity, the lower the flow rate at which P drops to Pmin, pulling the meniscus down the tube and drying out the wick. The evaporating menisci of the plant are held in the nanometerscale pores of primary walls facing internal (intercellular) air spaces. Although ideal for generating a potentially substantial driving force for pulling up the transpiration stream, the high resistivity of these pores to bulk flow limits the distance and rate of water flow. Hence, high flow resistivity of parenchymatous plant ground tissue was a major factor limiting the size of nonvascular (pre-tracheophyte) plants. Insights into Plant Vascular Biology 329 With the evolution of xylem conduits, the wick paradox was solved: maximum capillary action at nano-scale cell wall pores is coupled to minimum bulk flow resistivity in micro-scale xylem conduit lumens for carrying the transpiration stream over most of the soil-to-leaf distance (Figure 14B). The conduits are dead cell wall structures that resist collapse by having lignified secondary walls. They form a continuous apoplasmic pipeline from terminal leaf vein to root tip, propagating the tensional component to the supply of water in the soil. As water is pulled into the stele of the absorbing root tissues, it is forced across the endodermal membrane by reverse osmosis, providing a mechanism for filtration and selective uptake (Figure 14B, en). Like cell wall water, the soil water is held by capillary and absorptive forces. In short, the cohesion-tension mechanism is a “tug-of-war” on a rope of liquid water between capillary forces in soil vs. plant apoplasm. Living protoplasts do not participate in driving the transpiration stream, but draw from it by osmosis during cell expansion growth and to stay hydrated and turgid (Figure 14C). Low resistivity xylem facilitates larger plants and higher flow rates (equals greater photosynthetic productivity), and xylem evolution is a history of innovations for presumably moving water more efficiently. The increasing literature on the topic is beyond the more physiological emphasis of this section of the current review, but one example will suffice. The rise of high-productivity angiosperms appears to coincide with the evolution of greater vein density within leaves, which minimizes the distance the transpiration stream flows in high-resistance parenchymatous ground tissue (Boyce et al. 2009). Presumably, the evolutionary pressure for maximizing hydraulic efficiency varied over geological time scales, being less during periods of higher atmospheric CO2 and arid (dry) conditions, and increasing during periods of low CO2 and mesic (wet) conditions (Boyce and Zwieniecki 2012). The reason that lower frictional resistance correlates with greater photosynthetic rate is because it also correlates with greater diffusive conductance of the stomatal pores (Meinzer et al. 1995; Hubbard et al. 2001). The physics of the xylem conduit does not account for this coupling between low flow resistance and high diffusive conductance (equates to high evaporation rate). As long as the integrity of the xylem conduit remains constant, its evaporation rate is essentially independent of its internal liquid phase flow resistance. The observed coupling must result from a physiological response of the plant. The simplest explanation for the coordination of low hydraulic resistance and high diffusive conductances is that stomata are responding in a feedback manner to some measure of leaf or plant water status (Sperry 2000; Brodribb 2009). Increased plant hydraulic resistances result in a greater tensional component (i.e., more negative values of ψP) at a given transpiration rate and soil water status. If the ψP falls below some regulatory set-point (which need not be constant), hydraulic or chemical
330 Journal of Integrative Plant Biology Vol. 55 No. 4 2013 signals are sent to the stomatal complex, reducing the stomatal aperture and transpiration rate, which causes the ψP to rise back above the set-point. This ψP feedback is at least broadly consistent with most observed stomatal behavior in response to hydraulic resistance, as well as to evaporative demand and soil moisture stress (Oren et al. 1999; Brodribb 2009; Pieruschka et al. 2010). Recent evidence indicates that the ancestral feedback was entirely passive, as indeed it appears to still be in many seedless vascular plants (Brodribb and McAdam 2011). Accordingly, as ψP becomes more negative, guard cell turgor drops without any chemical signaling or active osmotic adjustment. Ensuing stomatal closure reduces the transpiration rate, which causes ψP to stop falling and rise back up. Only with the divergence of the seed plants 360 Mya did apparently active signaling evolve, which involves ψP sensing mechanisms, triggering of abscisic acid and other chemical signaling molecules, and active osmotic adjustment via ion pumps at the stomatal complex (McAdam and Brodribb 2012). The details of how this active feedback is achieved, the extent of active vs. passive mechanisms, the actual sites of evaporation within the leaf, the sites of water potential sensing, and the extent of hydraulic coupling between the stomatal complex and xylem are basic questions that are still poorly understood, and are the subject of considerable research and debate (Pieruschka et al. 2010; Mott and Peak 2011). Regardless of the feedback details, plants appear to have evolved to regulate ψP at the expense of sacrificing photosynthesis via reduced stomatal diffusive conductance. Presumably, this response avoids deleterious consequences of excessively negative ψP. Certainly most physiological processes are more energy-demanding at more negative ψP: the xylem conduit has to be stronger, and protoplasmic osmotic concentrations have to be greater. The implication is that there is some optimal midday ψP, in so far as it maximizes the cost/benefit margin of water transport vs. CO2 processing (Holtta et al. 2011). A priori, the optimal ψP would differ across habitats. For example, it would need to be more negative in drier habitats where plants have to pull harder to extract soil water as compared to wetter habitats. A full understanding of the costs associated with xylem transport requires detailed consideration of how xylem structure relates to its role in the water conducting process. Confining embolism with inter-conduit pitting While the evolution of xylem conduits solved the so called “wick” paradox, a new problem was created: the low-resistivity xylem conduits are necessarily too wide to generate, in and of themselves, much of a tension, i.e., a negative ψP value. In the inevitable event that a conduit becomes damaged and exposed to air, the surface tension present in the new meniscus spanning the conduit lumen is too weak to resist retreat (Pmin is not negative enough), and so water is pulled from this specific conduit into neighboring conduits and becomes embolized; i.e., it eventually is filled with N2, O2, CO2 and water vapor gases. Thus, capillary rise within the xylem conduit lumen cannot do the job of pulling up the transpiration stream. For the system to function, the xylem conduits must be primed by being water filled from inception, as they are, having developed from living cells. Nevertheless, there must be a means of limiting the spread of embolism when inevitably a conduit is damaged, even if by normal developmental events such as abscission of parts or protoxylem rupture. The problem of embolism is mitigated most fundamentally by dividing the fluid conducting space into thousands of overlapping and inter-connected conduits (Figure 14B, C). Each one embolizes as a unit because the inter-connections consist of porous partitions (inter-conduit pits) fine enough to trap and hold an air-water meniscus against a sufficiently negative ψP to minimize further gas propagation (Figure 14B,p). This multi-conduit system necessarily compromises hydraulic conductance because of the added resistance to flow through the inter-conduit pitting. Presumably, the lowest hydraulic resistance would be achieved by a single branching tube akin to the animal positive-pressure cardiovascular system. But a tensional system of such design would fail completely from a single point of air entry without any partitions to check the influx of gas. The presence of inter-conduit pitting is of great consequence for xylem functioning. The distribution of pitting and the structure and chemistry of individual pits influence both the flow resistance through the xylem and the Pmin for the xylem system (Choat et al. 2008). Although there is tremendous variation in inter-conduit pit structure across lineages, their basic structure has three elements held in common (Figure 15). As water flows from one conduit lumen to another, it passes through a pit aperture in the secondary wall, which opens into a usually wider pit chamber. Spanning the chamber is a porous pit membrane through which the water filters before passing out the downstream aperture. The pit membrane is the modified primary cell walls plus middle lamella of the adjacent conduits. There is no cell membrane or protoplasm in the dead but functioning conduit. Hydrolysis during xylem cell death is thought to remove all hemicelluloses and a debatable portion of pectins from the pit membrane, leaving a porous cellulosic mesh of microfibrils (Butterfield 1995). However, atomic force microscopy suggests that the microfibrillar structure lies beneath a non-porous coating of amorphous non-fibrillar material (Pesacreta et al. 2005). Pit membrane chemistry, structure, and development are crucial to understanding the frictional resistance to flow as well as the ability of the xylem to sustain significant tensions in the water column (Choat et al. 2008; Lee et al. 2012).
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The Plant Vascular System: Evolution, Development and FunctionsF

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