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hydraulic conductance (Kleaf – calculated as the ratio of


Abscisic acid and stomatal transpiration rate and the water potential gradient between
closure: a hydraulic conductance solution and leaf, which in detached leaves simplifies to the
ratio of transpiration rate to leaf water potential) of both WT
conundrum? and ost2-2 plants by c. 35% (Pantin et al.), suggesting dual
hydraulic and chemical mechanisms by which ABA could elicit
stomatal closure.
The discovery that the plant hormone abscisic acid (ABA) had a Another recent report corroborates this decrease in Kleaf in
pronounced antitranspirant effect when supplied to detached leaves response to feeding ABA to detached leaves. When WT Arabid-
(Mittelheuser & van Stevenick, 1969) initiated extensive research opsis leaves were xylem-supplied with 10 lM ABA, Kleaf decreased
activity aimed at discovering its mode of action, which continues to by c. 50%, yet foliar application of the same ABA concentration
this day. Successive generations of researchers have aimed to (while decreasing transpiration rate) had no statistically significant
determine the biochemical and genetic mechanism(s) regulating its effect on detached leaf Kleaf (Shatil-Cohen et al., 2011). This
biosynthesis, transport and metabolism, its binding to receptors disparity highlighted the role of bundle sheath cells (which enclose
and their location, and its downstream effects on intracellular signal dead, conductive xylem vessels) in sensing long-distance ABA
transduction, gene expression and cellular ionic regulation in signals. In contrast to previous reports where incubation of WT leaf
diverse cell types. Much of this work has used stomatal guard cells as protoplasts in 1 lM ABA for 3 h had no significant effect on
a model, in view of the over-arching importance of ABA in osmotic water permeability (Morillon & Chrispeels, 2001),
regulating plant water loss, as exemplified by the higher transpira- incubating bundle sheath protoplasts in 1 lM ABA for 1 h
tion rates and lower water status of ABA-deficient mutants decreased osmotic water permeability by c. 40% (Shatil-Cohen
compared with wild-type (WT) plants. An enduring controversy et al., 2011). Reconciliation of these results in the same study would
has been the relative importance of the roles of tissue water relations confirm the intriguing possibility that ionic regulation of different
(hydraulic effects) and ABA status (chemical signalling) in regulat- cell types is differentially responsive to ABA, which would interact
ing transpiration (Christmann et al., 2007). Thus various with spatial differences in ABA concentration observed in different
experimental techniques have attempted to separate these effects cell types (Christmann et al., 2007) in regulating hydraulic
(e.g. by growing ABA-deficient and WT plants at different relative responses to ABA.
humidities), even though stomatal response to ABA depends on
tissue water status (Tardieu & Davies, 1992). Recent work of
Pantin et al., in this issue of New Phytologist (pp. 65–72), further
indicates the futility and artificiality of this paradigmatic separa-
‘Do root and shoot tissues show completely opposing
tion. Their work apparently indicates that ABA not only directly responses to ABA?’
mediates stomatal closure (chemical signalling), but also system-
ically decreases leaf hydraulic conductance (Kleaf) upstream of the
stomata.
Whole plants and detached leaves of various ABA-insensitive However, reports of ABA-induced declines in hydraulic
Arabidopsis mutants (abi1-1, abi2-1, ost2-1, ost2-2, slac1-1), conductance apparently contradict the stimulation of root cell
when either sprayed with an ABA solution (400 lM) or (Hose et al., 2000) and root system (Beaudette et al., 2007)
supplied with ABA (50 lM) via the transpiration stream, hydraulic conductivity (Lp) by exogenously supplied ABA and in
showed partial stomatal closure (Pantin et al.). Detached leaves ABA overproducing transgenics (Thompson et al., 2007). Such
of these mutants showed a 36–85% decrease in stomatal work indicated that ABA acted at the plasmalemma to stimulate
conductance (in some cases equivalent to the WT response of symplastic water transport across the root cylinder (Hose et al.,
an 83% decrease) in response to xylem-supplied ABA. 2000), which has more recently been correlated with enhanced
Furthermore, transpiration of intact abi1-1, abi2-1, ost2-2 activity and expression of aquaporin proteins. Do root and shoot
plants was decreased by 22–36% following a foliar ABA spray tissues show completely opposing responses to ABA? In trying to
(400 lM), a similar response to WT plants. Previous work reconcile these apparently opposing effects of exogenous ABA on
(discussed in Pantin et al.) indicates that supplying ABA to root and shoot hydraulic conductance, the percentage change in
epidermal strips of the same mutants was unable to elicit response was plotted against ABA concentration for several
stomatal closure, indicating a disparity in the cellular and literature reports (Fig. 1a), and compared with the dose–response
tissue responses to ABA. Measurements in detached leaves curve for the effects of xylem-supplied ABA on detached leaf
indicated that xylem-supplied ABA (50 lM) decreased leaf transpiration (Fig. 1b). Interestingly, early reports of ABA

6 New Phytologist (2013) 197: 6–8 Ó 2013 The Author


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Phytologist Commentary Forum 7

was measured. In such cases, effects of ABA on Kleaf (hydraulic) and


(a)
transpiration rate (chemical) are confounded. Instead, measure-
ments of Kleaf using techniques that do not rely on quantifying
detached leaf transpiration rate (Sack et al., 2002), in plants of
contrasting ABA status (Thompson et al., 2007), would provide
direct evidence that xylem-supplied ABA does indeed act as a
regulator of Kleaf.
Historically, the role of xylem-supplied ABA in mediating
stomatal closure in response to soil water deficit has been extensively
questioned, since in vivo xylem ABA concentrations did not always
elicit stomatal closure when fed to detached leaves (see discussion in
Zhang & Davies, 1991). Observations that xylem sap pH altered the
distribution of ABA between apoplastic and symplastic compart-
(b) ments such that xylem alkalization enhanced apoplastic ABA
concentrations (Wilkinson & Davies, 1997) apparently accounted
for drought-induced stomatal closure before any increase in xylem
ABA concentration. An alternative view arising from the work of
Pantin et al. is that synergistic effects of xylem-supplied ABA (in the
nanomolar range) on both Kleaf and transpiration create a feed-
forward response eliciting stomatal closure, perhaps via transient
changes in leaf water status sensitizing guard cells to existing ABA
concentrations (Tardieu & Davies, 1992).
By slowing the rate of water loss, these changes are likely to be of
real adaptive significance when plants are exposed to prolonged
periods of soil drying inducing massive ABA accumulation. To
what extent these changes are readily reversible is also a key issue for
Fig. 1 (a) Fold change in detached leaf (closed symbols) and root system
plants growing in environments with fluctuating soil water
(open symbols) hydraulic conductance in response to xylem-supplied and availability, since xylem ABA concentrations can remain elevated
nutrient solution-supplied abscisic acid (ABA), respectively. Data are (and stomata remain partially closed) for several days after soil water
re-plotted from soil-grown Arabidopsis – Pantin et al. (this issue of New status returns to normal (Correia & Pereira, 1994). Whether the
Phytologist, pp. 65–72; closed triangle) and Shatil-Cohen et al. (2011; closed phenomenon described by Pantin et al. is amenable to genetic or
inverted triangle); and pea plants – Beaudette et al. (2007; open diamonds);
hydroponically grown bean – Markhart et al. (1979; open circles); and maize
environmental regulation, via crop breeding or agronomic manip-
– Hose et al. (2000; open square) plants, respectively. The box indicates a ulations, is a key unanswered question, which may assist in
hypothetical area where changes in leaf hydraulic conductance (Kleaf) are improving crop water use efficiency.
likely to be affected by in vivo xylem sap ABA concentrations. (b) Fold
change in detached leaf transpiration rate in response to xylem-supplied
ABA. Data are re-plotted from soil-grown Arabidopsis – Pantin et al. (closed Ian C. Dodd
triangle) and Shatil-Cohen et al. (2011; closed inverted triangle); lupin –
Correia & Pereira (1994; closed circles); pea – Dodd et al. (2008; closed Lancaster Environment Centre, Lancaster University, Lancaster,
diamonds); and wheat – Zhang & Davies (1991; closed squares) plants,
LA1 4YQ, UK
respectively. Second order regressions were fitted to the data in both panels,
but excluding data points from Arabidopsis, in SigmaPlot for Windows 2.01 (tel +44 1524 593809; email I.Dodd@lancaster.ac.uk)
(Jandel Scientific, Erkrath, Germany).

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New
8 Forum Commentary Phytologist

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