The Plant Vascular System: Evolution, Development and FunctionsF

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observable pores of predicted air-seeding size in non-stressed membranes (Choat et al. 2008), as well as the tendency for pit membranes to be thicker, pit chambers shallower (less deflection), and apertures proportionally smaller in cavitationresistant species (Choat et al. 2008; Jansen et al. 2009; Lens et al. 2010). Furthermore, the KCl-induced decrease in membrane flow resistance does not translate into increased vulnerability to cavitation (Cochard et al. 2010b). This could mean there are few to no pores in the non-stressed water conducting pit membrane, with water penetrating the hydrated gel phase. Alternatively, this could support the diffuse-double layer hypothesis for the KCl effect which does not require changes in pore dimensions (Van Doorn et al. 2011b). The apparent interaction between membrane stress and air-seeding would be largely eliminated for “vestured” pits where, in some plant lineages, the membrane is supported by outgrowths from the pit chamber wall, a factor that must lie behind the elusive adaptive significance of these structures (Jansen et al. 2001; Choat et al. 2004). An additional complexity in linking cavitation resistance to pit structure is a seemingly inescapable role for probability. A single inter-conduit seal consists of hundreds if not thousands of individual pits. Not all of these pits will be created equal, and it only takes one leaky pit to air-seed the cavitation. According to the “rare pit” hypothesis, the more pits that constitute the seal, the weaker the seal will be, because by chance the leakier will be the leakiest pit (Wheeler et al. 2005). This will be true whether the air-seeding pores are pre-existing, or are created by mechanical stress. This hypothesis is supported by the general trend for larger vessels to be more vulnerable to cavitation (because they would have more pits), and by a correlation between the extent of inter-conduit pit area and increasing vulnerability (Hacke et al. 2006; Christman et al. 2009; Christman et al. 2012). It seems safe to conclude that both pit quantity and pit quality interact to set the ψP value at which air-seeding occurs and, hence, the cavitation resistance (Lens et al. 2010). Because cavitation appears to spread from conduit to conduit, the three dimensional connectivity of the conduit network should have an additional impact on cavitation resistance. Woody species differ considerably in the extent of overlap or connectivity between individual conduits (Carlquist 1984). Modeling studies suggest that greater connectivity would tend to facilitate the spread of embolism, whereas more limited connectivity would tend to confine it (Loepfe et al. 2007). However, limited comparative data do not always support this prediction. A greater vessel grouping index (higher connectivity) in some lineages correlates with higher cavitation resistance rather than enhanced vulnerability (Lens et al. 2010). This trend supports the earlier notion that the greater redundancy provided by high connectivity would be advantageous for minimizing the effect of embolism in xeric habitats (Carlquist 1984). Insights into Plant Vascular Biology 335 The evident complexity that links xylem conduit structure to cavitation resistance comes from the multitude of variables involved: features at the individual pit level (e.g. membrane porosity, thickness, Ca 2+ content, mechanical properties) can be balanced by features at the inter-conduit wall scale (e.g., pit number), which in turn can be balanced by features at the conduit network level (e.g., conduit connectivity). Thus, the same cavitation resistance is likely to be achieved by multiple structural combinations. Freeze-thaw associated cavitation Cavitation can also be induced by freeze-thaw cycles and likely by a “thaw expansion” nucleating mechanism (Pittermann and Sperry 2006) (Figure 18A). Freezing of the xylem sap in nature usually occurs under conditions where transpiration is minimal. Thus, xylem blockage by ice formation would normally not result in ψP becoming more negative. Instead, ψP would likely become less negative, or even become positive because of the expansion of ice. However, dissolved gases in the sap are insoluble in ice, and under typical freezing conditions will form bubbles in the middle of the conduit. On thawing, if these bubbles do not dissolve fast enough they can nucleate cavitation if the thawed sap ψP is sufficiently negative. Hence, cavitation would occur during the thawing rather than the freezing phase, a prediction supported by experimental observation (Mayr and Sperry 2010). Just as for cavitation by water stress, there is considerable variation between species in their vulnerability to freeze-thaw cavitation. It is scarcely detectible in some species regardless of the negative sap ψP values, and others are blocked completely by a single freeze-thaw event at ψP values close to zero (Davis et al. 1999) (Figure 18B). However, unlike the water stress situation, there appears to be a single structural variable of over-riding importance for determining vulnerability to freeze-thaw cavitation. That variable is the xylem conduit lumen diameter: wider conduits are uniformly more susceptible to cavitation than narrower ones, regardless of whether the conduit is a conifer tracheid or angiosperm vessel (Figure 18B). The simplest explanation is that wider vessels form larger bubbles during freezing because of their greater water volume, and large bubbles take longer to re-dissolve and, hence, are more likely to nucleate cavitation, post-thaw. As the thawexpansion model predicts, a more negative ψP post-thaw, or a more rapid thawing rate, will also induce more cavitation at a given conduit diameter (Langan et al. 1997; Pittermann and Sperry 2003, 2006). Similarly, the amount of embolism should decrease with a greater rate of freezing, which reduces gas bubble size (Sevanto et al. 2012). In some species, the amount of embolism increases with the minimum freezing temperature, an observation not necessarily predicted from the thaw-expansion mechanism (Pockman and
336 Journal of Integrative Plant Biology Vol. 55 No. 4 2013 Figure 18. Vulnerability of xylem to cavitation by freeze-thaw events. (A) The “thaw expansion” mechanism for cavitation by freezing and thawing. Freezing of a sap-filled functional vessel creates gas bubbles in the ice-filled frozen conduit. If bubbles persist long enough after thawing, and negative pressures are low enough, they will trigger cavitation and result in an embolized conduit (from Sperry 1993). (B) Loss of hydraulic conductivity caused by a single freeze-thaw cycle at -0.5 MPa versus the average conduit lumen diameter. Data are species averages for angiosperm vessels (black) and conifer tracheids (blue) (from Pittermann and Sperry 2003). Sperry 1997; Ball et al. 2006; Pittermann and Sperry 2006). It is possible that the lower ice temperature and consequent tissue dehydration creates, locally, a more negative sap ψP, postthaw (Ball et al. 2006), or perhaps causes tissue damage that nucleates cavitation, post-thaw. Acoustic emissions are often detected during the freezing phase, which could indicate that at least some cavitation occurs prior to the thawing of tissue (Mayr and Zublasing 2010). However, experiments indicate no loss of conductivity when stems frozen under negative ψP conditions are thawed at atmospheric pressure; the conductivity only drops when the thaw occurs under negative ψP values (Mayr and Sperry 2010). It is possible that other phenomena besides conduit cavitation are causing freezing-associated acoustic emissions. Importantly, not all embolism events during winter are necessarily caused by freeze-thaw cycles. Sublimation and cavitation by water stress in thawed and transpiring crowns with frozen boles or soil represent other potential causes (Peguero-Pina et al. 2011). Negative xylem sap ψ P and conduit collapse The cohesion-tension mechanism requires conduit walls that are sufficiently rigid to withstand collapse by the required negative ψP values. Hence, the evolution of secondary walls and lignification necessarily paralleled the evolution of xylem tissues. While many factors contribute to the strength of conduit walls to prevent implosion, a dominant variable is the ratio of wall thickness to conduit lumen radius. This ratio tends to increase with cavitation resistance, as expected from concomitantly more negative sap ψP values. A higher thickness-to-span ratio also increases wood density, consistent with the tendency for greater wood density in more cavitation-resistant trees that generally experience more negative ψP values (Hacke et al. 2001a; Domec et al. 2009). Estimates of wall strength give an average safety factor from implosion of 1.9 in woody angiosperm vessels and 6.8 in conifer stem tracheids (Hacke et al. 2001a). The lower value for vessels presumably reflects their minimal role in mechanical support of the tree, a function performed by wood fibers. However, conifer tracheids must be additionally reinforced because they not only have to hold up against negative sap ψP, but they also support the tree itself. Interestingly, not all conduits avoid implosion, as it has been observed in the axial tracheids of pine needles (Cochard et al. 2004), transfusion tracheids of podocarps (Brodribb and Holbrook 2005), and metaxylem vessels in maize (Kaufman et al. 2009). In each case, the collapse was apparently reversible. Not unexpectedly, implosion is also observed in conduits of lignin-deficient mutants (Piquemal et al. 1998). Trade-offs between efficiency and safety The cohesion-tension mechanism, and its limitation by cavitation and conduit collapse, suggest potential trade-offs in the xylem conduit structure for minimizing flow resistance on the one hand (efficiency), and sustaining greater negative ψP without cavitation or conduit collapse on the other hand (safety). With respect to greater resistance to collapse, large increases
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The Plant Vascular System: Evolution, Development and FunctionsF

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