Download Hydraulic and chemical signalling in the control of stomatal

Journal of Experimental Botany, Vol. 53, No. 367, pp. 195–200, February 2002
Hydraulic and chemical signalling in the control of
stomatal conductance and transpiration
Jonathan P. Comstock1
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853, USA
Received 25 September 2001; Accepted 23 October 2001
Abstract
Abscisic acid (ABA) transported in the xylem from
root to shoot and perceived at the guard cell is now
widely studied as an essential regulating factor in
stomatal closure under drought stress. This provides
the plant with a stomatal response mechanism in
which water potential is perceived in the root as an
indication of soil water status and available water
resources. There is also ample evidence that stomata
respond directly to some component of leaf water
status. This provides additional information about
water potential gradients developing between root
and shoot as the result of water transport, allowing
for a more stable regulation of shoot water status
and better protection of the transport system itself.
The precise location at which leaf water status
is sensed, however, and the molecular events transducing this signal into a guard cell response are
not yet known. Major questions therefore remain
unanswered on how water stress signals perceived
at root and leaf locations are integrated at the guard
cell to control stomatal behaviour.
Key words: ABA, drought response, humidity response,
hydraulic conductance, leaf water potential, stomatal
regulation, xylem cavitation.
Introduction
The past decade has seen considerable progress in
understanding both chemical and hydraulic signals in
the regulation of stomatal conductance, and this parallel
growth has also led to some debate on the relative
importance of the two signal types in controlling
transpiration. Although sometimes framed in eitheruor
1
E-mail: [email protected]
ß Society for Experimental Biology 2002
terms, the positive results in both areas suggest that the
important questions are when, where and how the two
types of signal are integrated in the regulatory process.
Foliage, in which photosynthesis and 95% or more of
the plant’s water consumption will occur, is distantly
removed from the sources of water in the soil, but is
connected to the source pool by an elaborate xylem
transport system and the absorptive surfaces of the roots.
This system is wonderfully efficient, extracting water from
the soil matrix and maintaining plant hydration despite
frequently high transpiration rates. While the hydration
states of different tissues are very sensitive to the
magnitude of the hydraulic conductance, direct physical
control of transpiration itself resides almost entirely in
environmental conditions of temperature and humidity
and the stomatal regulation of gas-phase diffusion
between leaf air spaces and the atmosphere (van den
Honert, 1948). While the opening and closing of the
stomatal pore is actually achieved by turgor regulation in
the guard cell, these are generally actively controlled
processes of osmotic regulation and not passive consequences of bulk tissue water potential (Buckley and
Mott, 2001). Tremendous importance has therefore been
placed on understanding the regulatory signals that
govern stomatal behaviour. These signals must generate
behaviour that protects the plant from dehydration while
still allowing ample diffusive exchange for CO2 capture.
Guard cell regulation has become an important model
system in plants because of the central importance and
accessibility of guard cells, the fact that several distinct
signal transduction mechanisms are known to exist and
thus provide a model to study the processes of signal
integration, and because the phenotypic responses of
turgor regulation and aperture control are relatively easy
to score (Schroeder et al., 2001). This signal transduction
matrix allows an integration of both the opening signals
related to the need for carbon capture and closing signals
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Comstock
related to water management and hydraulic constraints.
This enormous topic can only be touched upon in this
commentary. Therefore the focus will be on the stomatal
closure response to water deficits with an evaluation of
(1) root-based assessment of soil water status (Qs),
transmitted to the guard cells via long-distance chemical
signals such as abscisic acid (ABA), (2) sensing of the
proximal leaf water potential (Ql) near or at the guard
cell, and (3) the integration of these signals in guard cell
behaviour.
Evidence for chemical signalling
Reports on long-distance chemical signalling have
pointed out that declining stomatal conductance during
drought is consistently correlated with changes in Qs,
while it is only weakly or only in some species wellcorrelated with Ql. Conceptually, it can be argued that
soil moisture represents the available resource pool, and
the status of that resource should logically govern the
modulations of growth and plant water use, including
stomatal closure during drought (Davies and Zhang,
1991). The root is in intimate contact with the soil,
and root water potential (Qr) may be the logical point to
sense changes in Qs most effectively. Further, numerous
and co-ordinated responses to drought are needed, and a
chemical signal proceeding from the root throughout
the plant may better achieve such co-ordination than
independent responses to local water status by scattered
diverse tissues located at different positions along the
flow path in the plant. These ideas are supported by an
extensive and growing database of studies showing that
ABA synthesis in roots increases in response to soil water
deficits, that this leads to elevated xylem wABAx and
increased xylem transport of ABA from root to shoot.
A wealth of data has also accumulated on the efficacy of
ABA in causing stomata closure, now a standard assay in
the study of guard cell physiology. Although the specific
receptor(s) for ABA remain to be identified, the cascade
of events triggered by ABA that lead to stomatal closure
are intensely studied, and at least the broad outlines of
these mechanisms are now understood at the molecular
level (Schroeder et al., 2001). Particularly important in
much of the root-signal research has been the use of splitroot culture, where individual plants are grown with the
root system divided among two or more separated soil
volumes with independent moisture contents. These have
been used to show that having a portion of the roots
in dry soil can trigger strong stomatal closure even when
shoot water potential does not noticeably decline. Even
more importantly, they have sometimes demonstrated
that a positive signal is present (an inducible signal added
to the transpiration stream under drought), rather than a
negative signal (a constitutive signal removed during
drought), by showing that stomatal closure responses
are much stronger if half the root system is droughted
than if half the root system is simply excised (Gowing
et al., 1990).
Evidence for hydraulic signalling
In contrast, studies focused on the hydraulic architecture
of plants and the vulnerability of the transport system to
failure under stress emphasize that a lack of response to
distal shoot water potentials would be dangerous and
potentially fatal to plants. Many plants operate close
to the hydraulic limits of transport where cavitation of
the xylem under excess tension can cause a rapid loss of
conducting capacity with a strong potential for positive
feedback (Sperry et al., 2001). This would result in total
loss of hydraulic conductance in the absence of stomatal
regulation of the flux, and the empirically observed
margins for safety become even tighter during drought
stress. While root-sourced signals might anticipate such
stresses in a general manner, they could not respond
to specific cavitation events because the progressive failure
of the xylem under a constant transpiration rate would at
first have no effect at all on upstream Qr, and, in the final
stages where xylem continuity was lost entirely, Qr would
be more positive.
An essential component of this debate is the number
of forms that ‘hydraulic signalling’ can take. Much of
the literature assumes that hydraulic signals must
involve stomatal responses to steady-state changes in Ql,
such that there would be a strong correlation between
declining stomatal conductance and Ql during drought.
This, however, is only one limited possibility. If Ql is
regulated homeostatically (Comstock and Mencuccini,
1998; Saliendra et al., 1995), at least in the sense that
it is not allowed to drop below some minimum value,
then several kinds of ‘hydraulic signals’ are suggested
by simply considering the common Ohm’s law analogy
for water flux. The water flux must be equal to both
the loss through the stomata (gsD) and liquid-phase
transport (hcDQ), where D is the leaf to air vapour
pressure gradient, gs the stomatal conductance, and
hc the hydraulic conductance. Setting these equal at
steady-state lets us write:
hc (Ys Yl )
(1)
gs ¼
D
This suggests that under high transpiration conditions
when Ql has approached a constant Qmin, stomatal
conductance should be directly proportional to hydraulic
conductance, drop linearly with Qs during drought, and
respond inversely to evaporative demand by the atmosphere. All of these behaviours are frequently reported
(Buckley and Mott, 2001; Sperry et al., 2001). Stomatal
conductance has also been shown to respond as predicted
to experimental manipulations of hydraulic conductance
Hydraulic and chemical signalling
through wounding or artificially induced cavitation
in the stem (Sperry et al., 2001). It is important to note
that in this context, many of the split-root experiments
showing stomatal closure, despite no reduction in Ql
while half the root system is droughted, are entirely
consistent with hydraulic signalling through reduced
hydraulic conductance. In this view, it is the reduction
in hydraulic conductance caused by soil drying, flooding
or other perturbation which has required a reduction in
stomatal conductance in order to maintain the observed,
stable Ql. On the other hand, experiments discussed above
in which a partially severed root treatment behaves more
like a fully watered control than the half-droughted
treatment, thus indicating the presence of a positive
signal, do argue against the sole operation of an hydraulic
signal. The reduction of hydraulic conductance would be
analogous to a negative signal.
Evidence for integration of chemical and
hydraulic signals
While it is difficult to reject the strong evidence for
positive, root-sourced signals in a great many studies,
and the likely identity of ABA as at least one of the
most common of these important signals, it has also
been hard to escape from invoking interactions with Ql
to explain the full range of responses in stomatal
conductance. For example, to reconcile the dosageu
response characteristics of the guard cells to ABA with
observed xylem imports over a drought sequence, it is
often necessary to assume increased sensitivity to ABA
at low Ql, an inherent merging of the earlier concepts
of chemical versus hydraulic signalling (Tardieu and
Davies, 1993). Further, the very stability of Ql in so many
reports is an extremely challenging observation that
needs to be fully explained, as illustrated by a simple
rearrangement of Equation 1:
gs D
Yl ¼ Ys (2)
hc
Numerous reports in the literature detail a wide range
of different stress treatments in various experiments
which are associated with remarkably constant values of
Ql when comparing stressed and control plants. This
constancy of Ql is often cited as evidence against a
hydraulic signal. Such a conclusion, however, implies
that the diverse treatments are (1) as a side effect, causing
large alterations in hydraulic conductance, (2) that ABA
is having an entirely independent effect on stomatal
conductance and (3) that these independent effects on
hydraulic and stomatal conductances (weighted by the
prevailing humidity, another independent factor) just
happen to be so consistently well balanced that they
compensate perfectly in Equation 2 and produce no
measurable perturbation in Ql. This is possible in some
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cases, but it seems an improbable explanation of such
general behaviour. More likely hypotheses would be
either that both chemical and hydraulic signals are
operative and being integrated at the level of stomatal
regulation, or even that hydraulic conductance itself is
somehow being actively regulated. As has been pointed
out previously (Tardieu and Davies, 1993; Tardieu and
Simonneau, 1998) it is often precisely in those species
in which Ql shows the least variation that a component
of hydraulic signalling may be most clearly present.
Nevertheless, statements that observed homeostatic
conservation of Ql during various treatments rules out
hydraulic signals are still common in the literature.
Recent advances
Pressurization of the soil air spaces independently of the
shoot environment is now a common treatment in many
experiments. When using this technique, both gas and
liquid compartments of the soil become equally pressurized, and these altered pressures extend into both
respective phases in the root tissues. Because both liquid
and gas phases are equally affected, it is argued that
turgor–volume relations of the root system and the
relative water contents of its tissues are not altered.
Thus the root is not thought to perceive these treatments as altering its water status or that of the soil.
When xylem fluids pass out of the soil pressure chamber
into the shoot environment, however, the water pressure
is still elevated, but perceived by the shoot against
a background of normal ambient air pressure. The
soil airspace pressurization is thus experienced as an
increased total water potential, turgor, and relative
tissue water content in the shoot, but not the root
(Comstock and Mencuccini, 1998; Passioura, 1980). The
technique is also now one of the preferred approaches
to obtaining xylem sap under active gas-exchange
conditions in intact plants, because the soil can be pressurized until the shoot xylem develops a positive
pressure and exudes into a sample vial. It has also
been extensively used to evaluate direct responses of
stomatal conductance to Ql. In just one example of the
importance of time scale, in several long-term treatments lasting for days or weeks, stomatal conductance
of continuously pressurized plants declined in a similar
manner to unpressurized controls (Passioura, 1988a;
Schurr and Schulze, 1996), but in the great majority of
cases where soil pressurization treatments lasted for a few
hours only, large stomatal opening effects could be
initiated by elevating Ql (Comstock and Mencuccini,
1998; Else et al., 2001; Fuchs and Livingston, 1996;
Matzner and Comstock, 2001; Mencuccini et al., 2000;
Saliendra et al., 1995). In many of these studies, the
elevation of Ql was a transient phenomenon, and, at
steady-state, variations in soil pneumatic pressure
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Comstock
ultimately translated into variation in stomatal conductance at relatively constant Ql, consistent with hydraulic
signalling as discussed above in relation to Equation 1.
Other studies also provide strong evidence of rapid
changes in local foliar water status because of altered
flux dynamics in the surrounding tissues being rapidly
translated into stomatal responses (Buckley and
Mott, 2000).
A great deal of progress has been made in elucidating
the nature and dynamics of ABA signalling. For rootbased ABA signals targeting the guard cell, the concentration of ABA in xylem sap rather than total ABA
delivery appears to be the primary signal (Jia and Zhang,
1999). Nonetheless, xylem-borne ABA must move
through the leaf apoplast in contact with mesophyll
and epidermal tissues before reaching the guard cell.
Variable rates of ABA sequestration and metabolism by
these tissues can have a strong impact on concentrations
at the guard cell apoplast where it will be transduced
into a closing signal (Hartung et al., 1998). While this process creates many possibilities for interactions dependent on Ql, most current results indicate control by a
complement of xylem-borne signals rather than regulatory integration with leaf water status (Wilkinson and
Davies, 1997). Thus, at low Qs, the leaf apoplast has a
more alkaline pH which reduces uptake of ABA by
intervening tissues and increases the concentration near
the guard cell, but if it is solely the change in xylem
sap pH controlling the leaf apoplast there is no
regulatory role for Ql. Other studies, however, have
found evidence for a direct influence of Ql on ABA
partitioning within a leaf ( Popova et al., 2000), and
considerable room for signal integration exists in this
area, which needs exploration in future studies.
Transpiration itself, independent of stomatal closure
owing to lowered soil or plant water status, is most
often varied experimentally by varying ambient humidity.
Most species show considerable stomatal closure as
humidity decreases (Popova et al., 2000), and, at
moderate to high water vapour gradients between leaf
and air, such closure may be sufficient to compensate
fully for variation in humidity, holding transpiration
(and Ql) constant. The role of ABA in these diurnal
modulations is much less clear than in soil drying.
Increased water flux per se should dilute and lower
xylem wABAx, but to the degree that the root tissues
feel a flux-dependent depression in Qr, increased
synthesis and release of ABA might compensate for
this in intact plants (Schurr and Schulze, 1995, 1996).
Nonetheless, the common reversibility of lowered stomatal conductance at high vapour pressure gradients with
soil pressurization, and reports from studies that
wild-type humidity responses are seen in ABA-deficient
mutants (Assmann et al., 2000) suggests that hydraulic
signals and Ql regulation may dominate in these
responses. Other recent studies, however, have shown
that wABAx of the guard cell apoplast (as well as other
chemical and osmotic factors) do in fact increase
substantially in response to increased transpiration
rates (Zhang and Outlaw, 2001) and this might explain
why soil pressurization usually fails to achieve complete
stomatal recovery. Here again, multiple concurrent
signals are indicated.
Issues for the future
One of the most limiting issues in assessing these
relationships is that current knowledge of ABA signal
transduction has greatly outstripped information on
exactly how and where Ql is sensed when generating
stomatal responses. It is not known to what degree
these dynamics are intimately linked with the ABA story,
or if there is a completely distinct signal carried to
the guard cell. Buckley and Mott recently concluded
that Ql was likely to be sensed in the mesophyll or
epidermis but not the guard cell, because of the dramatic
turgor-fluctuations associated with guard cells (Buckley
and Mott, 2001). By contrast, Assman et al. concluded
that numerous conflicting observations on behaviour
might be most easily reconciled if the guard cells were
themselves the site of Ql sensing (Assmann et al., 2000).
These contrasting conclusions are still speculative,
however, and indicate the great need to identify the
actual signal transduction events associated with
responses to Ql.
The possibility exists, however, that, rather than
adjusting stomatal conductance in response to Ql as
hydraulic conductance is altered by treatments, hydraulic
conductance might itself be under dynamic adjustment
to control Ql under the prevailing conditions of transpiration. This runs counter to the most commonly accepted
paradigm (Passioura, 1988b), in which hydraulic conductance is viewed to be somewhat variable at very low
values of transpiration only, but more stable and fixed
by anatomy at high transpiration until xylem cavitation
begins at excessive flux rates and depression of Ql. This
paradigm of stable hydraulic conductance is consistent
with many datasets (Comstock and Mencuccini, 1998;
Sperry et al., 2001) in which hydraulic conductance is
clearly constant as stomatal conductance is regulated in
response to both humidity and moderate soil drying, or
in which variation in hydraulic conductance is clearly
explained by altered environmental conditions such as
temperature fluctuations (Matzner and Comstock, 2001).
There are, however, several recent reports that variability
in hydraulic conductance may be seen even at high
transpiration and at various points in the flow pathway
(Clarkson et al., 2000; Makoto and Tyree, 2000;
Steudle, 2001; Zwieniecki et al., 2001). This behaviour is
reported to be under reversible physiological control via
Hydraulic and chemical signalling
the gating of aquaporins, changes in the ionic composition of the xylem or other unspecified mechanisms.
It is far from clear yet how common these phenomena
are in creating variable hydraulic conductance at high
transpiration, but they raise the possibility that hydraulic
conductance could be adjusted secondarily, after chemical
signals have regulated stomatal conductance, perhaps in
order to hold Ql constant and maintain stable osmotic
relationships in the leaf. This could possibly be an
important aspect for the stability of other signalling
mechanisms at the guard cell, but such behaviour is not
yet well described or understood. In this context it is
worth noting that the water flow pathway leaving the
xylem network at the leaf veins is, like the radial, extraxylary flow of water in roots, one of the largest single
resistances in the flow pathway for many plants
(Comstock and Mencuccini, 1998; Matzner and
Comstock, 2001; Tiekstra et al., 2000), and likely to
involve a symplastic step in the bundle sheath parenchyma around veins (Canny, 1990). Variable hydraulic
conductance from aquaporin expression and gating could
conceivably act here to stabilize Ql at low to moderate
transpiration without adding to the tensions and cavitation vulnerability of the xylem network, but such
regulatory effects are wholly speculative and have not
been documented in any extensive studies. It seems
unlikely that hydraulic conductance at high transpiration,
when damaging levels of tension are approached in the
xylem, would be allowed to remain at less than its
physiological maximum in any event.
Of increasing interest in the next several years will be
broader comparative studies on the differences of
behaviour in different species. Anisohydric versus isohydric species, herbaceous versus woody with their
contrasting capacitances and xylem volumes, and plants
with a range of different water-use patterns may all
have strongly contrasting patterns of the relative importance of chemical versus hydraulic signals in the
responses to different environmental variables. Timecourses of responses are also poorly understood, but
often suggest that not only are multiple signals present
in the induction anduor maintenance of stomatal
closure, but they may have a strong temporal variation
in which signals predominate under different conditions
(Else et al., 2001; Liang and Zhang, 1999). The increasing
availability of mutants and other genetic tools to probe
specific responses and interactions will be important
approaches in resolving some of these issues (Assmann
et al., 2000; Borel et al., 2001).
Conclusions
Both hydraulic and chemical signalling are probably
important in the stomatal regulation of most plants. The
199
tight regulation of Ql is best viewed as evidence for
hydraulic signaling and not the lack of it. Even a more
positive value of Ql during a stress treatment is only
conclusive evidence that other signals are present and
may have increased in importance, and not necessarily
that hydraulic signalling is absent at that time. Rootsourced and hydraulic signals are likely to have different
kinds of information in them about environmental
conditions as well as the internal state of the plant and
its transport system, and therefore it is expected that
both would be important components in regulating
stomatal behaviour. These dual components are supported by strong evidence in both cases, and guard cells
are apparently influenced by both, as well as numerous
other signals in their integrated responses.
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