Journal of Experimental Botany, Vol. 65, No. 7, pp. 1751–1759, 2014
doi:10.1093/jxb/ert467 Advance Access publication 15 January, 2014
Review paper
Phloem transport and drought
Sanna Sevanto*
Earth and Environmental Sciences Division, Los Alamos National Laboratory, Bikini Atoll Road MS J495, Los Alamos, NM 87545, USA
* To whom correspondence should be addressed. E-mail: [email protected]
Received 29 August 2013; Revised 2 December 2013; Accepted 4 December 2013
Abstract
Drought challenges plant water uptake and the vascular system. In the xylem it causes embolism that impairs water
transport from the soil to the leaves and, if uncontrolled, may even lead to plant mortality via hydraulic failure. What
happens in the phloem, however, is less clear because measuring phloem transport is still a significant challenge to
plant science. In all vascular plants, phloem and xylem tissues are located next to each other, and there is clear evidence that these tissues exchange water. Therefore, drought should also lead to water shortage in the phloem. In this
review, theories used in phloem transport models have been applied to drought conditions, with the goal of shedding
light on how phloem transport failure might occur. The review revealed that phloem failure could occur either because
of viscosity build-up at the source sites or by a failure to maintain phloem water status and cell turgor. Which one
of these dominates depends on the hydraulic permeability of phloem conduit walls. Impermeable walls will lead to
viscosity build-up affecting flow rates, while permeable walls make the plant more susceptible to phloem turgor failure. Current empirical evidence suggests that phloem failure resulting from phloem turgor collapse is the more likely
mechanism at least in relatively isohydric plants.
Key words: Carbohydrate transport, carbon starvation, hydraulic failure, Münch flow, semi-permeable conduit, tree mortality.
Introduction
Recent forest mortality events (Allen et al., 2010), combined
with climate predictions of increasing drought severity and
frequency in many areas (Allison et al., 2009), have motivated a new focus area of plant mortality mechanisms during drought (McDowell et al., 2008; Adams et al., 2009; Sala
et al., 2010; McDowell, 2011; Zeppel et al., 2011; Anderegg
et al., 2012b, Mitchell et al., 2013). The theoretical frame
work for this focus area was set up by McDowell et al. (2008)
based on our understanding of plant water relations. During
drought plants close their stomata to avoid excessive water
loss that could lead to hydraulic failure or wilting (Sperry,
1986; Sperry et al., 1998; Cochard et al., 2002; Meinzer et al.,
2009), but closing of stomata inhibits photosynthesis leading to negative carbon balance which could cause mortality
if drought persists and carbon availability becomes insufficient (carbon starvation; McDowell et al., 2008; McDowell,
2011). The timing of stomatal closure varies with drought
severity and species-specific variation in xylem vulnerability
to cavitation (Sperry, 2000; Brodribb and Holbrook, 2003).
Relatively isohydric (dehydration avoiding) plants (Tardieu
and Simmoneau, 1998) close their stomata early during
drought, thus being theoretically more likely to die of carbon
starvation, while relatively anisohydric (dehydration tolerating) plants may be more susceptible to hydraulic failure.
This relatively simple theoretical framework is very useful
for categorizing and quantifying observations but, because of
its simplicity, it has provoked some criticism centred around
how exactly the mortality process progresses (McDowell and
Sevanto, 2010; Sala et al., 2010), how that affects plant survival time, and how we define the ultimate mortality mechanisms (Anderegg et al., 2012a; Sevanto et al., 2013). This
criticism has, for the first time, brought phloem transport
during drought into focus (McDowell and Sevanto, 2010;
Sala et al., 2010). Cessation of phloem transport could be the
key to understanding the progress of plant mortality because
phloem transport failure could promote carbon starvation
© The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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1752 | Sevanto
by prohibiting the redistribution of carbohydrate reserves
to starving tissues (McDowell and Sevanto, 2010; Sala et al.,
2010). It could also promote hydraulic failure if the relocation of carbohydrates was needed to ensure refilling of embolized conduits. Therefore, resolving how phloem transport
might fail during drought, and whether it can recover from
drought, are key questions that need to be answered before
mechanisms of drought mortality are understood.
This task, however, is very challenging because of our
sparse, although constantly increasing, knowledge on phloem
transport. At the moment, the majority of the existing phloem
transport studies have been conducted under well-watered
conditions (for a review see van Bel, 2003), and the majority
of drought experiments have focused on xylem vulnerability
to cavitation, stomatal control, and tissue carbohydrate stores
(for a review see Chaves et al., 2003; McDowell et al., 2008;
Choat et al., 2012) implicitly assuming that drought does not
affect phloem transport (Sala et al., 2010). Therefore, our
empirical evidence on how drought affects phloem transport
is very limited and mostly indirect. From the point of view of
understanding phloem transport, drought experiments provide a unique setting for testing theories, as the extreme conditions reveal the boundaries of phloem function and have
the potential for shedding light on the transport mechanisms
and controls. Thus, phloem transport experiments in drought
conditions would benefit both fields.
As a result of the scarcity of empirical work on phloem
transport during drought, this review will focus on the theories behind phloem transport models. It will use the classical
Münch hypothesis and the theory on flow in conduits with
semi-permeable walls, to develop arguments on how phloem
transport could fail during drought and how the failure
mechanisms depend on phloem conduit structure. The goal
is to make theoretical predictions that could serve as a basis
for a new set of experiments about phloem function during
drought. The predictions will be discussed in the light of
the anisohyric and isohydric stomatal response strategies to
drought, because of the interesting contrast in requirements
for phloem transport that these strategies reveal. This review
will focus on the effects of a rapid, severe drought on phloem
transport in a time-scale that does not allow for structural
adaptations. It will also focus on woody plants that are most
relevant in the context of forest mortality, but have exhibited
the largest challenges to the Münch hypothesis with almost
absent pressure gradients in the phloem and the long distance
between sources and sinks (for a review see Thompson, 2006;
Turgeon, 2010). The theories themselves are not restricted to
any particular plant type, but they mostly explain flow in a
single conduit and, therefore, the effects of sieve plates, sieve
areas or other occlusions in the conduits are mostly omitted
here.
Classical view and viscosity limitation
The currently most accepted theory of phloem transport, the
Münch hypothesis (Münch, 1930; see also Knoblauch and
Peters, 2010) states that carbohydrates needed for metabolism
and storage travel from source tissues (mature leaves and
other photosynthesizing tissues or transient storage) to sink
tissues through a conduit system consisting of sieve cells.
Solutes loaded into the conduits increase the osmotic potential that attracts water from the surroundings through the
semi-permeable cell walls at the sources (Fig. 1). At the sinks,
unloading of solutes reduces the osmotic potential allowing
water flow back to the surrounding tissues and reducing the
hydrostatic pressure in the sieve cells. The pressure difference
between the sources and sinks drives the bulk flow of solutes
between these tissues. Thus, the phloem transport system consists of three parts: the source, the transport pathway, and the
sink. The flow rate depends on the strength of both the source
and the sink and the resistance of the pathway between the
two ends. The water drawn to the conduits osmotically at the
source ultimately originates from the xylem, which builds a
close relationship between phloem transport and xylem water
status (Thorpe and Minchin, 1996; Hölttä et al., 2009). The
higher the xylem water tension (drier the plant), the higher
the osmotic potential that is required to pull water from the
xylem to the phloem. Thus, maintaining phloem transport in
dry conditions requires a strong source.
In this classical view of phloem transport, the flow rate in
each phloem conduit is described by the Hagen–Poiseuille
law where flow rate (J; m s–1) is proportional to the pressure
(P; Pa) difference between the source and the sink, which
can be approximated as the solute concentration (c; mol m–3)
Fig. 1. A schematic presentation of the original Münch pressure–
flow hypothesis where both the semi-permeable sink and the
source areas are in the same water bath, but they are connected
to each other via an impermeable transport conduit. Sugar
concentration (C1) at the source end is higher than that at the sink
end (C2) resulting in a pressure gradient between the source and
the sink. This pressure gradient drives carbohydrate transport in
the conduit and the flow in the conduit is covered by the Hagen–
Poiseuille law (equation 1).
Phloem transport and drought | 1753
difference between these locations (R is the gas constant and
T temperature; van’t Hoff relation for dilute solutions). The
coefficient of proportionality is a conductivity term that
depends on conduit size (radius r and length L) and fluid viscosity (µ)
J=
π r4
π r4
( Psource − Psink ) =
RT (csource −csink ) (1)
8Lµ
8Lπ
Based on equation (1), increases in fluid viscosity decrease
flow rate. Sucrose is the most commonly transported sugar in
the phloem (Thorne and Giaquinta, 1984), but viscosity of a
sucrose solution increases exponentially with increasing concentration (Morison, 2002). At ~5 MPa osmotic pressures the
viscosity would already be almost 30 times that of pure water
(for comparison, milk is three times more viscous than water
and castor oil is 1000 times). Xylem water tensions ~5 MPa
can easily be reached by relatively anisohydric species, but
isohydric species tend to close their stomata limiting xylem
water tensions to below ~3 MPa (McDowell et al., 2008; Plaut
et al., 2012). An increase in solute concentration is needed
during drought to attract water into the phloem from the drying xylem for transport purposes. Therefore, during drought,
increasing viscosity could lead to severe slowing down of
phloem transport, or even a complete phloem blockage, especially in anisohydric species (McDowell et al., 2013).
Equation (1) also shows that, to compensate for the viscosity increase, plants that are adapted for maintaining phloem
transport during drought should have wide conduits (large r).
Alternatively, plants could try to increase source–sink concentration gradient by lowering the sink concentration to
overcome the effects of viscosity increase, although that is a
less effective means than increasing conduit radius because
of the strong dependence of the flow rate on the radius to
the fourth power. If it is also assumed that phloem conduits
are independent of each other, the total sap flux through the
phloem can be calculated by simply adding the fluxes in each
conduit together (Hölttä et al., 2009). This leads to a prediction that having a larger phloem (more conduits) would
allow higher total transport rates even at high viscosity during drought.
Applying this theory to plants showing isohydric and anisohydric strategies suggests that, as long as phloem transport is
a prerequisite of photosynthesis, relatively anisohydric plants
that can photosynthesize at high xylem water tensions should
have wider phloem conduits or larger phloem (or both) compared with relatively isohydric plants. Interestingly, the opposite is true for xylem conduit size. Relatively anisohydric species
have smaller xylem conduits than relatively isohydric species to
allow xylem operation at high water tensions without cavitation
(Domec and Johnson, 2012; McDowell, 2011). Phloem transport rates during drought could still be comparable in these two
groups as long as isohydric plants can use carbohydrate stores
as sources when photosynthesis declines. Stomatal closure will
keep xylem water tensions low enough so that viscosity increase
will not be a challenge for transport in these plants.
There is evidence that high concentrations of mono- and
disaccharides in the leaves may feed back to the stomatal
guard cells inducing stomatal closure (Sheen, 1990; Krapp
et al., 1993; Paul and Foyer, 2001), which suggests that maintaining phloem transport may be essential for photosynthesis
(Nikinmaa et al., 2013). There are no data available for evaluating whether phloem conduits of anisohydric plants are
wider than those of isohydric plants. There is some evidence
of two-year old branches of one-seed juniper (Juniperus monosperma; a relatively anisohydric tree) having a larger phloem
area relative to the xylem area than similar branches of piñon
pine (Pinus edulis; a relatively isohydric tree) (S Sevanto,
unpublished data). But more evidence is needed before conclusions can be made. Therefore, these predictions remain to
be tested. It is clear, however, that according to this classical view of phloem transport, drought generates a challenge
that could lead to phloem transport failure through viscosity
build-up at the sources.
Semi-permeability of conduits walls
The Hagen–Poiseuille law was originally developed to describe
laminar flow in cylindrical tubes of impermeable walls (Bird
et al., 2002) and the classical view of phloem transport, based
on the experiments of Münch (1930), assumes that the walls
of the phloem conduits outside the source and sink areas are
impermeable. This model has been successfully applied to
explain sink priority in plants (Thornley and Johnson, 1990;
Minchin et al., 1993) and the Hagen–Poiseuille law is used
in most current phloem transport models for calculating the
pressure changes and flow rates in the axial direction (Henton
et al., 2002; Thompson and Holbrook, 2003; Hölttä et al.,
2006, 2009; Jensen et al., 2009). However, from relatively early
on there has been discussion about the role of the possible
semi-permeability of phloem conduit walls on flow rates and
phloem transport (Eschrich et al., 1972; Christy and Ferrier,
1973; Young et al., 1973; Phillips and Dungan, 1993). There
also is a growing amount of experimental evidence supporting
the view that the walls of sieve cells are semi-permeable allowing water to enter and exit everywhere along the conductive
pathway (Minchin and Thorpe, 1987; Knoblauch and Peters,
2010) and that this water exchange is essential for phloem
transport (Zimmermann and Brown, 1980). Therefore, even
the models that use the Hagen–Poiseuille law for calculating axial pressure gradients, have relaxed the impermeability
assumption and allow water exchange in radial direction for
the total length of the phloem conduit (Henton et al., 2002;
Thompson and Holbrook, 2003; Hölttä et al., 2006, 2009;
Jensen et al., 2009, 2011).
Semi-permeability of the conduit walls generally makes
phloem transport less vulnerable to increasing viscosity, but
more susceptible to changes in xylem water tension than the
classical model. If the conduit walls are impermeable, xylem
water tension affects transport only at the sink and source
regions and once in the transport phloem, the flow is affected
only by the geometry of the conduit and properties of the
fluid inserted into the conduit at the source. If the viscosity
of the fluid is too high for the system (conduit geometry and
existing pressure gradient) flow will simply cease. When the
1754 | Sevanto
semi-permeability of the walls is taken into account, more
water can enter the phloem conduits along the entire transport length, diluting the solution and reducing the effects of
high viscosity along the way (Phillips and Dungan, 1993).
Flow in conduits with semi-permeable walls can be characterized using two dimensionless parameters H and L p
(Phillips and Dungan, 1993; called F and R in Thompson
and Holbrook, 2003). H describes the relative importance of
osmotic forces to viscous, frictional pressure losses in generating the axial flow, and L p is the dimensionless hydraulic permeability of the conduit walls.
H=
Lp =
is diluted by the incoming water along the way (Phillips and
Dungan, 1993; Eschrich et al., 1972).
In conduits with semi-permeable walls, the axial flow is
entirely generated by the water potential difference between
the conduit and its surroundings. The flow ceases if water
exchange through the conduit walls is hindered. In the above
discussion, an infinite water pool surrounding the conduits
has been assumed. Drought and increasing xylem water
Φ0r2
(2)
µLU
Lp L2 µ
r3
(3)
where Φ0 is the initial osmotic force at the source (here zero
concentration at the sink end is assumed), U is the characteristic axial flow velocity, L is the conduit length, and Lp is
the hydraulic permeability of the conduit walls. If H is large,
radial water flow through the conduit wall is caused by the
presence of osmotically active solutes. Small H means that
the radial flow is due to viscous pressure drop in the conduit
(Phillips and Dungan, 1993).
Parameter H, however, cannot simply be used to assess
the flow type (osmotic versus viscous), but the influence of
L p on the flow, in the form of the product of H and L p , has
to be used (Phillips and Dungan, 1993). If that product is
large, even if L p was small, osmotic forces will dominate the
flow, and the axial solute flux in a conduit will be constant
(Haaning et al., 2013; Eschrich et al., 1972). The maximum
osmotically obtainable flow rate (v; m s–1) can be calculated as
a product of the initial osmotic force at the source (Φ0) (here
zero concentration at the sink end is assumed), the hydraulic
permeability of the conduit wall (Lp) and the aspect ratio (α;
length per radius) of the conduit
vmax _ osmotic = 2Φ0 Lp α(4)
where Φ0 can be estimated, for example, from the van’t Hoff
relation (Haaning et al., 2013).
If L p is large, but H is so small that the product becomes
small, the axial flow is affected by viscous effects on the pressure gradient but, as long as the conduit walls are permeable, the flow velocity and axial pressure profiles differ from
those predicted by the Hagen–Poiseuille equation (equation
1) (Phillips and Dungan, 1993). The viscous forces generate
an additional pressure drop which speeds up flow and, instead
of being constant, the flow rate will actually increase towards
the ends of the conduits (Phillips and Dungan, 1993). This is
because the water attracted to the conduit pushes the contents
of the conduit with increasing flow velocity, which decreases
the pressure inside the conduit attracting even more water
from the surroundings (Fig. 2). Interestingly, if the viscous
effects are strong enough, this radial water cycle between the
conduit and its surroundings will occur even if the solution
Fig. 2. A schematic presentation of flow in a semi-permeable
tube. High sugar concentration at the source area (here top)
attracts water from the surroundings to the semi-permeable
conduit (Πin>Πout) increasing the pressure (Pin) at the sugar front.
This pushes water inside the tube and forces it out back to the
surroundings below the sugar front creating a pressure gradient
(Pin>P) that drives the flow (velocity, v). If the conduit is wide and
flow rates small, the flow is solely driven by the osmotic potential
difference between the conduit and the surroundings. If the
conduit is narrow and the flow rate fast, viscous forces will create
an additional pressure gradient that will increase the flow velocity
and flow will not be affected by the dilution of the sugar front
(Phillips and Dungan, 1993; Jensen et al., 2009).
Phloem transport and drought | 1755
tension will affect the water pool ultimately leading to shortage of water to support this kind of flow, but increasing fluid
viscosity will speed up axial flow rather than hinder it. This is
because increasing viscosity increases L p and the importance
of the viscous effects on the pressure gradient in the conduit,
but it decreases H in equal proportion so that the product
of H and L p does not depend on viscosity at all leaving the
importance of the osmotic forces unchanged. Drought could
also reduce H by decreasing source strength, which would lead
to viscous forces dominating the flow, but this does not mean
that solute transport would cease as long as there is some kind
of a sugar source and enough water in the surrounding tissue.
If we imagine that sugars can be loaded to a conduit along the
way while the fluid is already initially moving with a certain
velocity, the flow rate will increase along the way, although the
relative gain in flow velocity resulting from enhanced osmotic
water exchange through the walls decreases with increasing
initial velocity (Haaning et al., 2013). Therefore, this kind of
an action would be most effective in increasing the flow rate
close to the sources where flow rates are initially small.
The permeability of conduit walls has also been treated by
allowing radial water exchange, but using the Hagen–Poiseuille
law to drive the flow and calculating the pressure differences
in axial direction. This method correctly makes phloem flow
more sensitive to xylem water tensions than the impermeable wall model (Hölttä et al., 2009), but it does not take the
real effects of conduit wall permeability on the flow rate into
account. This can be seen by applying a dimensionless parameter obtained from this approach to drought conditions. This
parameter (Mü) resembles L p, the dimensionless conduit wall
permeability, but is interpreted as describing the ratio of flow
resistance in the axial and radial directions (R in Thompson
and Holbrook, 2003; Mü in Jensen et al., 2009, 2011).
Mü = 16
µLp L2
r3
(5)
Applied to drought, Mü could be used for estimating a viscosity limit for flow in a single conduit by arguing that axial flow
is too slow to be efficient when axial conduit resistance equals
radial conduit wall resistance (i.e. Mü=1). This limit is based
on the simple argument that having wide conduits (see equation 1) would not benefit the plant if axial conductivity equals
radial conductivity (normally they differ by several orders of
magnitude (Sevanto et al., 2011)), and thus flow in such system
would be very inefficient. This calculation leads to an inverse
relationship between viscosity and conduit wall permeability
stating that the less permeable the conduit walls are, the more
viscous flow the conduits can transport, which is contradictory to the theories presented above. Even if results from the
models using this approach are useful and valid in moist conditions, during drought, and at the limit of increasing viscosity this approach does not give reasonable results, and should
be avoided. Flow in conduits with semi-permeable walls differs from flow in impermeable conduits in that the apparent
hydraulic conductance of the conduits is not proportional to
the fourth power of conduit radius as stated by equation (1),
the basis for developing equation(5). Instead, flow rates tend
to be higher in conduits with smaller radii (Eschrich et al.,
1972) resulting in a constant axial solute flux (flow rate per
conduit area) [see equation (2) and Haaning et al., 2013],
which would reduce the effect of sieve plates or other occlusions along the flow path. Source and sink strength affect the
initial flow velocity (Eschrich et al., 1972), and may direct the
flow towards the strongest sinks but, unlike in the classical
impermeable conduit model, source and sink strength does
not drive the flow. The pressure and concentration gradients
are solely created by the interaction between the conduit and
its surroundings (Young et al., 1973), and therefore the axial
flow resistance cannot be treated in the way it is treated when
developing equations (1) and (5).
During drought, high conduit wall permeability would
allow easy water exchange between the tissues, and higher
flow rates (see equation 4), but the trade-off would be that,
at high wall permeability, the solute concentration changes
in the phloem would have to be fast enough to balance the
changes in xylem water tension to prevent turgor loss of the
cells and to maintain water potential equilibrium with the
xylem along the whole pathway (Thompson and Holbrook,
2003). With semi-permeable conduit walls protecting the
phloem turgor is critical because the driving force for the
flow is based on water exchange between the conduit and
its surroundings (Eschrich et al., 1972; Young et al., 1973).
Therefore, one could argue that relatively anisohydric species with relatively high xylem water tensions need either low
conduit wall permeability in the phloem or a very fast and
efficient osmoregulation system to keep water from leaking
to the xylem. In the first case, the flow would resemble the
classical Hagen–Poiseuille flow, and relatively anisohydric
plants could reduce viscosity build-up by using solutes such
as potassium (Talbott and Zeiger, 1996) that do not increase
fluid viscosity. The second case would require a high capacity to mobilize solutes for osmoregulatory needs (e.g. convert
storage carbohydrates to smaller molecules for increasing
osmotic strength). Conduit wall permeability will thus determine drought impacts on phloem flow and what anatomical
and physiological traits are important for the integrity of
the system. Low permeability would prevent phloem turgor
collapse during drought, but phloem transport rates would
generally be lower than with more permeable conduits. This
could have consequences on plant growth rate (Van Bel,
1996) and competition. High wall permeability would ensure
fast phloem transport and an advantage in growth and competition but, during drought, it could lead to mortality via
turgor collapse. Fast osmoregulation could also require active
phloem loading, which is less energy-efficient than passive,
diffusion-driven, loading. Therefore, having highly permeable
conduit walls might prove a more risky strategy especially in
environments with regular droughts.
Does phloem transport cease during
drought?
All terrestrial plants face the trade-off between water loss and
carbon gain. Avoiding excessive water loss via stomatal closure
1756 | Sevanto
during drought inevitably leads to reduced photosynthesis
and carbohydrate production, which reduces source strength.
Also, the turgor-related reduction of growth is one of the first
drought responses in plants (Hsiao et al., 1976), reducing sink
strength. However, there is evidence that both non-woody
and woody plants can cycle water and carbohydrates without
a photosynthetic source (Tanner and Beevers, 2001; Sevanto
et al., 2013). Thus, reduced source or sink activity will not necessarily lead to the complete cessation of phloem transport as
long as carbohydrate reserves can be utilized (Sevanto et al.,
2013) but, in the absence of a photosynthetic source, access to
carbohydrate reserves becomes essential.
What determines the extent to which plants can deplete
their carbohydrate reserves is currently unclear. Mild drought
seems to enhance the access in crops (Rodrigues et al., 1996;
Yang et al., 2001), and there is evidence that nitrogen could
play a role both in crops (Yang et al., 2000, 2001) and in trees
(Millard and Grelet, 2010; Chapin et al., 1990; Millard et al.,
2007; Sala et al., 2012). High water availability clearly helps
in the utilization of the reserves in trees (Sevanto et al., 2013)
but, during extreme drought (no water supply until trees
die), trees of the same species in the same environment can
lose access to their reserves at very different times (Sevanto
et al., 2013). It seems clear both theoretically and experimentally that, if the drought is long and severe enough, phloem
transport failure will occur, but when it occurs and where the
threshold between mild and severe drought is for different
species, and even individuals, is an open question.
How does phloem failure occur, and is it
important for survival?
The classical impermeable conduit model predicts that phloem
transport could cease during drought even with active sources
and sinks because of viscosity blockage in the transport pathway (Hölttä et al., 2009; McDowell and Sevanto, 2010). The
permeable conduit wall model, predicts that phloem transport would primarily cease because of reduced source and
sink activity or because of reduced water content of the tissue
surrounding the phloem conduits.
The only experiment to date, that has tested phloem failure
during tree mortality used a relatively isohydric tree species
(piñon pine; Pinus edulis). In this experiment phloem turgor
collapse occurred at ~2 MPa xylem water tension preceding
mortality by several weeks, and the timing of phloem turgor collapse predicted both the amount of carbohydrates
the trees could utilize and the survival time (Sevanto et al.,
2013). At 2 MPa the viscosity of a sucrose solution is only
roughly twice the viscosity of pure water (Morison, 2002),
which should not produce any challenge to transport yet. One
could thus argue that failing turgor maintenance rather than
viscosity build-up caused phloem failure in these trees consistent with the semi-permeable conduit wall model, and that
the timing of turgor collapse determined the level of access to
stored carbohydrates.
Turgor maintenance during drought can be obtained by two
means: (i) by increasing solute concentration inside the cells or
(ii) by reducing cell wall permeability (or both). The failure of
these would result in water leaking to the xylem, possibly temporarily refilling embolism. This, however, would not be a permanent solution to progressing hydraulic failure because of
the limited amount of water available from the phloem tissue.
At present, it is not known which one of these mechanisms
fails when phloem turgor collapses and why, and at which
stage of the collapse turgor can still recover. It is only known
that phloem turgor loss can occur even without depletion of
carbohydrate reserves (Sevanto et al., 2013), and it seems to
be an important predictor of carbohydrate storage use and
plant survival. It is possible that plants control cell wall permeability during drought to reduce the risk of phloem turgor
failure by, for example, by controlling aquaporins (Secchi and
Zwieniecki, 2010; Sevanto et al., 2011). However, an increase
in water tension in the xylem could effectively lead to an
apparent reduction of conduit wall permeability even if the
qualities of the walls did not change. This is because, independent of the model considered, at high xylem water tensions increased solute concentrations in the cells surrounding
the phloem conduits are required for maintaining operationality. In the classical model, this is needed to initiate flow and
to compensate for viscosity build-up; in the semi-permeable
conduit wall model, it is needed to maintain the water pool
around the conduits. Solutes reduce the mobility of water molecules (lower the water potential; Nobel, 2005), which means
that more energy (higher pressure gradient) is required to pull
water out from the cells to produce the same flux with solutes
than without solutes (Darcy’s law). Conductivity is usually
defined as the factor determining how large a flux one obtains
with a certain pressure gradient (see equation 1). Therefore,
the magnitude of conductivity also depends on the fluid that
was used to measure it. This means that to separate the effects
of high solute concentration and low wall permeability and
to understand the drought responses of the phloem, one has
to use methods that reveal changes in conduit wall properties
separate from changes in cellular solute content.
Consistently with the increased osmoregulatory demands,
many plants show an initial accumulation of sugars in the
leaves (Körner, 2003; Sala et al., 2010, and references therein)
or the sieve tubes (Cernusak et al., 2003) under drought.
Supported by the observations of reduced turgor difference
between the source and sink under water stress (Roberts, 1964;
for a review see Crafts, 1968; Ruehr et al., 2009), this has been
interpreted as sink strength (growth) reacting to drought earlier and/or more strongly than photosynthesis (Körner, 2003;
McDowell and Sevanto, 2010). The accumulation of carbohydrates, however, could also be interpreted as reduced phloem
transport rate (Sala et al., 2010). The accumulation tends to
occur at the early stages of drought when xylem water tensions are so low that viscosity should not produce too large
a challenge for transport. In the semi-permeable conduit wall
model, reduced hydraulic permeability between the xylem
and the phloem could slow phloem transport down resulting
in carbohydrate accumulation, which could then feed back to
both photosynthesis (Nikinmaa et al., 2013) and growth, raising the question of which is the cause and which the reaction
and how the long-distance signalling in plants works.
Phloem transport and drought | 1757
One of the key questions brought up by this review is the
permeability of the phloem conduits walls, and its impact on
phloem transport. Currently, our knowledge on this topic is
very limited. Based on what is known about xylem conduit
walls (Sperry, 2003), one would expect the conduit walls to
be porous, unless they are sealed with a substance like lignin
or suberin, or the pores are air filled, in which case the continuum of water would be interrupted by air–water interfaces. For understanding tree mortality mechanisms during
drought, and phloem transport in both moist and drought
conditions, it would be of high importance to design experiments for measuring hydraulic permeability of phloem conduit walls as well as detecting whether the permeability can
change seasonally and with environmental conditions (e.g.
xylem water tension). Permeability of the conduit walls could
explain the small pressure gradients in the phloem tissue of
many trees (Thompson, 2006), and controlling the permeability could be an easy way for a plant to control water cycling
between the xylem and the phloem as well as between the
sources and sinks (Sevanto et al., 2011). Before more detailed
data on the hydraulic permeability of phloem conduit walls
are available for a variety of plant species with different strategies of coping with drought, it is impossible to say whether
phloem failure due to viscosity build-up can occur. Based on
current evidence, phloem transport seems to be susceptible
to the maintenance of the water status of the phloem tissue,
and phloem failure resulting from turgor collapse seems a
more likely phloem failure mechanism than viscosity buildup, although having impermeable conduits could be beneficial for relatively anisohydric plant species adapted to regular
droughts.
Phloem failure during drought seems to be a mechanism
that promotes plant mortality by, at least, affecting access
to carbohydrate reserves (Sevanto et al., 2013), but even if
there is evidence that carbohydrates could be necessary for
embolism repair (Secchi and Zwieniecki, 2011), there is little evidence that phloem function during drought could prevent hydraulic failure by increasing refilling. This is because
without additional water refilling one conduit would result
only in the embolization of an adjacent one (Secchi and
Zwieniecki, 2010; Sevanto et al., 2013) and not improving
overall xylem conductivity. However, embolism repair could
be critical to recovery from drought and recovery of the
phloem function from drought might play a key role there.
Theoretically, plants with isohydric and anisohydric stomatal control strategies would clearly benefit from different
phloem conduit properties, but how much phloem conduit
structure differs between species in reality is to be shown by
future experiments.
Acknowledgements
The author wants to thank Dr Matthew Thompson for
informative and interesting discussions on the topic as well
as Drs Nate McDowell and Chonggang Xu for comments
on the manuscript. This work was supported by a LANLLDRD grant.
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