The Plant Vascular System: Evolution, Development and FunctionsF

332 Journal of Integrative Plant Biology Vol. 55 No. 4 2013
Pit membrane chemistry interacts with xylem sap chemistry
to influence xylem flow resistance in a very complex and poorly
understood manner. According to the “ionic effect”, increasing
the concentration of KCl up to 50 mM (encompassing the
physiological range) can decrease resistivity anywhere from
2% to 37% relative to pure water, depending on the angiosperm
species and even the season (Nardini et al. 2011b). The
KCl effect is much less or even negative in the already
low-resistance torus-margo pits of conifer species (Cochard
et al. 2010b). Furthermore, this KCl effect can be reduced or
eliminated in the presence of as little as 1 mM Ca 2+ in some
species and conditions (Van Iepeeren and Van Gelder 2006),
but not in others (Nardini et al. 2011b). Skepticism about the
importance of the phenomenon in planta (Van Iepeeren 2007)
has been answered with observations indicating KCl-mediated
decreases in resistivity associated with embolism and exposure
of branches to sunlight (Nardini et al. 2011b). Interestingly,
adaptive adjustments in KCl concentration may be mediated
by xylem-phloem exchange (Zwieniecki et al. 2004).
The ionic effect has been localized to the pit membranes,
but the mechanism remains unknown. A “hydrogel” model implicates
ionic shrinkage of pit membrane pectins or equivalent
hydrogel polymers, and, hence, a widening of membrane pores
(Zwieniecki et al. 2001b). However, recent observations with
atomic force microscopy do not support a pore-widening effect.
Although KCl was observed to thin the membrane, pores were
not observed, suggesting that the decrease in resistance resulted
from membrane thinning and perhaps increased permeability
of non-porous gel material (Lee et al. 2012). The extent of
pectins or similar gel materials in pit membranes appears to be
highly variable across species, perhaps underlying the extreme
variation in the ionic effect (Nardini et al. 2011b). Uncertainty
about the extent of hydrogel components of pit membranes has
led to an alternative (and perhaps complementary) hypothesis
that ions increase permeability by reducing the diffuse-double
layer of cations lining negatively charged nano-scale pores
in the membrane (Van Doorn et al. 2011b). All of these
hypotheses are consistent with a minor effect in torus-margo
pit membranes, with their large micro-scale pores between
cellulosic strands having presumably minimal pectin content.
Although inter-conduit pits have the disadvantage of adding
substantial flow resistance, they perform the highly advantageous
function of trapping an air-water meniscus and minimizing
the embolism event such that it does not compromise
the conducting system (Figure 16B, C). The homogenous pits
of angiosperm vessels have pores narrow enough to trap
themeniscuswithaPmin negative enough to hold against a
substantial range of negative ψP values (Figure 16D). The torusmargo
pits function somewhat differently. The wider margo
pores cannot sustain a very negative Pmin, but they can
generate just enough pressure difference to aspirate the solid
torus against the pit aperture on the water-filled side (Petty
1972). In this way, the torus can seal off the pit with a sufficiently
negative Pmin to minimize air passage (Figure 16D).
While inter-conduit pits minimize the propagation of embolism,
as the next section indicates, they nevertheless play
a major role in limiting the tensional gradient that can be
generated by the cohesion-tension mechanism.
Limits to negative ψ P values: the problem of cavitation
Periodically, the cohesion-tension mechanism comes under
question for its prediction of liquid pressures that fall below
the vapor pressure of water, and also below pure vacuum for
a gas (Canny 1998; Zimmermann et al. 2004). A tree 30 m tall
requires a ψP of −0.3 MPa on its stationary water column just
to balance the gravity component. To this we need to add,
say, −0.3 MPa to balance a favorable soil water potential
of −0.3 MPa. Finally, we need to add the typical ψP of
−1 MPa needed to overcome frictional resistance under midday
transpiration rates. The required ψP totals −1.6 MPa. At sea
level and 20 ◦ C, a vapor pressure of only −0.098 MPa will
bring water to its boiling point, and −0.1013 MPa corresponds
to pure vacuum for a gas. Clearly, for the cohesion-tension
mechanism to operate, transition from the liquid phase to the
vapor phase must be suppressed, and the xylem sap must
remain in a metastable liquid state. The xylem sap is in effect
super-heated, although “super-tensioned” is more descriptive.
The liquid water column becomes analogous to a solid whose
strong atomic and intermolecular bonds allow it to be placed
under tension; i.e., water is a tensile liquid!
The concept of metastable water is foreign to the macroscopic
world of normal human experience, hence the cohesiontension
skeptics. Water boils at 100 ◦ C, and vacuum pumps become
gas-locked at or above −0.098 MPa. But in these familiar
cases, the phase change to vapor (cavitation) is nucleated by
contact with foreign agents that destabilize the inter-molecular
hydrogen-bonding of liquid water (Pickard 1981). Such “heterogeneous
nucleation” of cavitation is typically triggered by
minute and ubiquitous gas bubbles in the system. When care
is taken to minimize such heterogeneous nucleation, liquid
water can develop substantially metastable negative ψP values.
Theoretical calculations, based on equations of state for water,
put the limiting ψP at homogeneous cavitation (where energy
of the water molecules themselves is sufficient to trigger the
phase change) below −200 MPa at 20 ◦ C(Mercury and Tardy
2001). Experiments with a variety of systems ranging from
centrifuged capillary tubes to water-filled quartz crystals have
reached values well below −25 MPa, with some as low as −180
MPa and approaching the theoretical limit (Briggs 1950; Zheng
et al. 1991). Such values dwarf even the most negative ψP in
plants, which is about −13 MPa (Jacobson et al. 2007); more
typical plant ψP values are less negative than −3 MPa.