Variable plant hydraulic conductance

We sometimes think of xylem hydraulic conductance as though it is an absolute constant. However, in this issue of Tree Physiology, Trifilò et al. (2014) show that hydraulic parameters can change in the short term, and that the factors causing these changes may interact. The topic is important because whole plant hydraulic conductance (Kplant) and individual conductance components have been linked with transpiration, carbon gain and growth rate (Stiller et al. 2003, Tyree 2003, Brodribb 2009). Assuming that the soil–leaf water potential gradient cannot exceed a certain range, high transpiration rates can only be realized if Kplant also remains high. Analogous to soil hydraulic conductivity, Kplant is variable and declines as the water potential (Ψ) becomes more negative (Sperry et al. 2002). Changes in Kplant are not just caused by drought, but by many other factors, including the ones shown in Figure 1. Here, I will focus on the importance of the dynamic increases or decreases in Kplant that occur within minutes or hours, rather than on developmental changes that relate to the amount of xylem produced or the size of a plant. Illustration of some factors that may cause short-term changes in Kplant. Boxes in yellow indicate questions related to the so-called ionic effect. Boxes with bold letters indicate two of the most important factors impacting Kplant in the short term, changes in the conductivity of living tissues and embolism formation in the xylem. Water in the xylem is transported through a complex network of dead cells, but this does not mean that transport is not variable (Nardini et al. 2011). In the xylem, changes in hydraulic conductivity (k) are primarily due to cavitation and the subsequent formation of embolism. Wide and highly conductive vessels, which occur in the earlywood of many ring-porous trees or in roots, are often highly vulnerable to cavitation; the loss of function in these vessels has a large effect on xylem hydraulic conductivity (kxylem) (Hacke et al. 2006, Pratt et al. 2008, Christman et al. 2012). In loblolly pine, small roots have been found to be more vulnerable to cavitation than larger roots and stems (Hacke et al. 2000). However, roots may also be able to repair embolism when the soil regains sufficient moisture. The roots of woody savanna species exhibited diurnal and seasonal cycles of embolism formation and refilling (Domec et al. 2006). Similarly, leaf xylem of field-grown rice plants experienced 60–90% embolism, which limited gas exchange, but nocturnal root pressure led to the reversal of embolism and the recovery of Kplant and leaf diffusive conductance overnight (Stiller et al. 2003). These and other case studies highlight the significance of embolism and its repair for plant performance. Despite the capacity for embolism repair in some species, vessels can remain permanently air-filled in many cases. Vessels may also be blocked by gels or tyloses after they become embolized. In grapevine, gels can form in a relatively short period of time (<48 h), which has consequences for the way in which dehydration vulnerability curves should be constructed (Jacobsen and Pratt 2012). Blockage of vessels by embolism and tyloses reduces kxylem. However, kxylem may also increase. An enhancing effect of xylem sap ionic concentration on kxylem has been reported for many species (e.g., Zwieniecki et al. 2001, Lopez-Portillo et al. 2005). Trifilò et al. (2014) reported that the potassium concentration of the xylem sap underwent diurnal changes. They found higher concentrations at midday than in the morning, which is opposite to what would be expected based on diurnal trends in the water uptake rate (Tyree and Zimmermann 2002). As a consequence of the increase in potassium concentration, the ionic effect was significantly enhanced at midday (Trifilò et al. 2014). In addition, the authors reported that the ion-mediated increase in kxylem tended to be stronger in embolized stems than in fully hydrated segments. It was therefore suggested that the ionic effect is an effective mechanism to alleviate the impact of xylem embolism. While we may tentatively assign biological functions to the ionic effect, we still have an incomplete understanding of how ions affect kxylem. It was originally hypothesized that the ionic effect is due to the presence of pectins in inter-vessel pit membranes. These pectins were thought to form gels that change their volume in response to the ionic composition of the aqueous phase and other factors (Zwieniecki et al. 2001, van Ieperen 2007). Recent studies that tested for the presence of pectic homogalacturonans (HG) in inter-vessel pit membranes did not detect HG in the main part of mature pit membranes (Plavcová and Hacke 2011, Plavcová et al. 2011), although it was consistently detected in other pit types (including vessel-ray pits) as well as in developing (but not in mature) inter-vessel pit membranes (Kim and Daniel 2013). Pectins were consistently present in the annulus regions of inter-vessel pit membranes. New hypotheses have recently been presented that may explain how the ionic effect relates to the ultrastructure and chemical composition of inter-vessel pit membranes (van Doorn et al. 2011, Lee et al. 2012). Lee et al. (2012) used atomic force microscopy to view pit membranes of tobacco. Since no visible pores were found, it was suggested that ion-mediated increases in kxylem result from changes in membrane thickness and changes in permeability of the pectin hydrogel that was assumed to cover the fibrous structure of pit membranes (also see Zwieniecki and Secchi 2012). While these are promising findings, Lee et al. (2012) noted that sample preparation was extremely difficult. More work with better sample size, a wider range of species, and chemical analysis of pit membranes will be required before we can come to general conclusions. Given that there is currently no or minimal evidence for the presence of pectins in mature inter-vessel pit membranes (aside from its prominent occurrence at the edges of the membrane), van Doorn et al. (2011) suggested that the swelling/shrinking phenomena that have been solely ascribed to pectins apply to any other polyelectrolyte in the pit membrane. There is little doubt that more information on the chemical composition and native state structure of pit membranes (Pesacreta et al. 2005, Lee et al. 2012) would be helpful to unravel the mechanism(s) by which ions promote kxylem. In addition, it may also be useful to reconsider the assumption that the ionic effect is only associated with inter-conduit pit membranes. If this were true (and it may very well be), then there should not be a pronounced ionic effect in conifer xylem. Xylem with short and highly interconnected vessels may be expected to show a strong ionic effect. Additionally, the ionic effect should be more pronounced in long stem segments than in short ones in which most vessels are open. Interestingly, in one earlier study the opposite was observed: shortening stem segments from 20 to 3 cm reduced the number of inter-vessel pits in the flow path. Instead of decreasing the ionic effect with segment length, the ionic effect was stronger in short segments (van Ieperen et al. 2000). This finding led to the hypothesis that the ionic effect is caused by the cation exchange properties of xylem cell walls (van Ieperen et al. 2000). Several questions remain: Do diurnal changes in potassium concentration really translate into significant and meaningful conductivity changes in planta? Leaf-specific hydraulic conductivity remained unchanged in the species studied by Trifilò et al. (2014). What reference xylem fluid should be used—deionized water, mineral water or a solution with standardized levels of Ca2+ and other ions (van Ieperen 2007)? Do plants actively regulate the ion concentration in the xylem sap to modify kxylem or does any diurnal fluctuation in KCl concentration result from processes that are not primarily related to hydraulics? Studies like the one by Trifilò et al. (2014) may bring us closer to answering some of the questions outlined above. Water transport is not only affected by embolism and by changes in xylem sap ionic concentration, but also by changes in temperature. Between 20 and 30 °C, changes in root and shoot hydraulic conductance may be primarily due to changes in the viscosity of water with temperature (Lopez and Nobel 1991, Cochard et al. 2000, Tyree and Zimmermann 2002). However, to the extent that living cells are contributing to the flow path, we also have to consider temperature-related changes in membrane permeability and solute transport processes (Lopez and Nobel 1991). Over the course of a day, the temperature of aboveground plant organs may change substantially. Sun-exposed leaves are likely to experience the biggest temperature fluctuation while root temperature will likely remain relatively constant. From this perspective, we may expect that leaf hydraulic conductance will undergo large temperature-induced fluctuations. Based on a 10 °C increase in air temperature from dawn to early afternoon, Tyree and Zimmermann (2002) predicted an increase in whole shoot hydraulic conductance by ∼24–30%. While much of this commentary focused on the apoplast, it is clear that changes in the membrane permeability of living cells can quickly increase or decrease Kplant. Before entering the xylem conduits of absorbing roots, water flows radially through living tissues and passes the endodermis. In leaves, the pathway outside the xylem includes the bundle sheath and mesophyll cells. The hydraulic conductivity of the extraxylary portion of the flow path is highly variable because of changes in membrane permeability, changes in turgor pressure and other factors (Henzler et al. 1999, Shatil-Cohen et al. 2011, Prado and Maurel 2013). Shifts in root and leaf hydraulic conductance can account for much of the variation in Kplant. Water flow through cell membranes in these tissues is determined by the abundance, trafficking and gating of aquaporins (Heinen et al. 2009). Several recent reviews have summarized how aquaporins are regulated and how they impact the hydraulic properties of roots and leaves (Maurel et al. 2008, Heinen et al. 2009, Prado and Maurel 2013). For instance, we know that changes in the aboveground environment (such as light or relative humidity) can impact aquaporin expression and activity in roots (Sakurai-Ishikawa et al. 2011, Laur and Hacke 2013). How the signaling between different plant organs works and how signals are integrated is not well understood, and will be a fruitful area of research in the near future. None declared. Support from the Canada Research Chair program is acknowledged. Thanks to Danielle Way and two anonymous reviewers for helpful comments on an earlier version of the manuscript.

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