The woody vegetation, in particular trees, is facing difficult times in many regions
across the globe. Unprecedented rapid increases in average temperatures along with
increasingly frequent periods of extreme drought and heat outrun the acclimatory capacities
of many tree species and other woody plants. Observations of increased tree mortality
and severe forest decline are accumulating in all forested biomes (Allen et al. 2010,
Hartmann et al. 2018) and questions arise as to whether and how the woody vegetation
may be able to cope with these changes (Allen et al. 2015) and which species will
succumb to drought while others survive.
More than a decade ago, the seminal paper by McDowell et al. (2008) addressed this
question with the ‘hydraulic framework’, linking tree mortality mechanisms to the
stomatal behavior of a tree species and to duration and severity of a drought. It
was speculated that species that close stomates early during drought become dependent
on stored carbohydrates as photosynthetic rates and sugar production decline along
with the decline in gas exchange. In contrast, species that maintain high photosynthetic
rates by keeping stomates open longer during drought risk strains on the conducting
tissue as the decreasing water potential induces high tensions in the xylem, which
might lead to the formation of embolisms and their propagation to adjacent conduits.
The regulation of water potential has been described in terms of plant control of
stomatal conductance (Tardieu and Simonneau 1998). While more isohydric species maintain
leaf water potential (P
L) relatively constant during changing environmental conditions (soil and atmospheric
drought), more anisohydric species let P
L covary congruently with environmental fluctuations (Martínez-Vilalta and Garcia-Forner
2017) until the water potential at stomatal closure (P
st) is reached (Martin-StPaul et al. 2017). In perfectly anisohydric species, predawn
water potential (P
pd) thus corresponds to the soil water potential in the soil horizon where water is
taken up from (Plaut et al. 2012). Ultimately, when the soil–root interface is disconnected
(Carminati and Javaux 2020), P
pd should approximate P
st. According to the above-mentioned framework, isohydric species would be more prone
to carbon starvation, while anisohydric species are more likely to die from tissue
desiccation via hydraulic failure.
The iso/anisohydry concept was introduced by Berger-Landefeldt (1936) to classify
species groups that differed in their diurnal transpirational behavior and thus leaf
water content under non-drought conditions. His concept evolved from Walter’s (1931)
definition of thresholds for the water status regulation of different plant types
according to their osmotic potential into stenohydric (small fluctuation in water
status, hydro-stable) and euryhydric (large fluctuation in water status, hydro-labile)
species. Ever since, attempts to categorize species according to their water relations
strategy into isohydric or anisohydric have shown modest success (see Hochberg et al.
2018 and references therein). The regulation of plant water status across the continuum
of stomatal regulation is highly complex, and neither Walter (1931) nor Berger-Landefeldt
(1936) were able to report a sharp distinction between the two groups. Notwithstanding,
many subsequent studies referred to an ambiguous dichotomy between extremes along
this continuum (cf., Martínez-Vilalta et al. 2014). The apparent simplicity of the
concept may have led to misinterpreting isohydry as a simple functional trait or a
strategy defined by the isolated action of stomates and not a response of the entire
plant in order to regulate the water status (Hochberg et al. 2018). The work by Jiang
et al. breaks this boundary and offers a whole-plant perspective.
In their article, Jiang et al. investigate the regulation of water status during the
dry season in 24 woody species distributed along a gradient of isohydry. For the first
time, this study focuses on how this regulation relates to stem capacitance and non-structural
carbohydrate (NSC) storage, linking leaf-level responses to whole-plant regulation.
The main finding is that there is a trade-off between stem capacitance and stem NSC
storage, where species that make greater use of stem water storage have a smaller
NSC storage pool. Less isohydric water potential regulation is associated with greater
NSC storage depletion during the dry season, most likely as a consequence of osmotic
adjustment. More isohydric species, by contrast, are characterized by greater stem
water storage use. Surprisingly, and contrary to what the hydraulic framework would
predict, more isohydric species showed an accumulation of NSC during the dry season,
apparently because the use of stem water allowed earlier leaf flushing and higher
photosynthetic rates. As such, the contribution by Jiang et al. provides an additional
dimension to research on water regulation and drought responses and suggests a mechanistic
explanation for why NSC storage pools often—but not always—decline during drought
(Adams et al. 2017). These contrasting observations on NSC depletion during drought
are likely a result of differences in the species’ stomatal control strategy. Most
likely, only species that follow a more anisohydric stomatal control strategy rely
on the conversion of starch into osmotically active sugars in order to lower the osmotic
potential of living cells, in both leaves and stems.
A close coordination between stem and/or whole-plant hydraulic traits and stomatal
control has been found repeatedly (Martin-StPaul et al. 2017, McCulloh et al. 2019,
Pivovaroff et al. 2018). More isohydric species are often characterized by a relatively
vulnerable xylem and light wood, and must rely on a high stem capacitance (amount
of released stored water per unit change in water potential) as well as low modulus
of leaf elasticity (increased leaf cell wall elasticity) to maintain gas exchange
until P
st is reached (Plaut et al. 2012, Meinzer and McCulloh 2013, Leuschner et al. 2019,
Jiang et al. 2020b). Due to hydraulic vulnerability segmentation between leaf petioles
and stem xylem (Losso et al. 2019), drought-induced premature leaf senescence occurs
as a protective measure in these species (Figure 1). Osmotic adjustment, on the other
hand, seems more important in more anisohydric species, resulting in a larger plasticity
in the water potential at turgor loss point (P
tlp). The maintenance of water loss via declining P
L is facilitated by this biochemical mechanism that increases the concentration of
osmotically active substances to lower the osmotic potential for preventing turgor
loss in living plant cells (Blum 1958, Kozlowski and Pallardy 2002, Sanders and Arndt
2012). The larger potential for osmotic adjustment in more anisohydric plants permits
them to lower their P
tlp over the course of the growing season and thus to keep their stomates open and
maintain photosynthetic activity at more negative water potentials (Figure 1).
Figure 1.
Top: Whole-plant traits commonly associated with iso/anisohydry. Bottom: Conceptual
diagrams for two hypothetical species from the two ends of the continuum of isohydry
(left: more isohydric; right: more anisohydric). Adapted and modified from Meinzer
and McCulloh (2013) and Charrier et al. (2018). The upper panels of the inset figures
show branch and leaf vulnerability curves (percent loss of branch/leaf conductivity
vs xylem pressure) as well as stomatal response curves (reduction of stomatal conductance
with increasingly negative water potential; with yellow arrows indicating the potential
of NSC-driven osmotic adjustment). The lower panels show the relationship between
minimum and pre-dawn water potential and the corresponding HSA. Parameters used in
the figure: Isohydric—xylem pressure at 50% loss of xylem (P50×) and leaf (P
50l) conductance: −2.80 and −2.30 MPa, respectively; point of 50% stomatal closure
(P
gs50): −0.90 MPa; point of stomatal closure (P
st): −1.54 MPa; hydraulic safety margin (HSM = P
st − P
50x): 1.26 MPa; slope of the relationship between minimum and pre-dawn water potential
(β): 0.15 MPa MPa−1; corresponding intercept (α): −1.31 MPa; HSA: 1.00 MPa2. Anisohydric—P
50×: −5.50 MPa; P
50l: −5.50 MPa; P
gs50: −2.20 MPa; P
st: −3.48 MPa; HSM: 1.26 MPa; β: 0.35 MPa MPa−1; α: −2.26 MPa; HSA: 3.93 MPa2, PLC,
percent loss of conductivity.
Despite ongoing controversies about the usefulness of the iso/anisohydry concept (Klein
2014, Martínez-Vilalta and Garcia-Forner 2017, Hochberg et al. 2018, Fu and Meinzer
2019, Ratzmann et al. 2019), it appears still useful for describing hydraulic behavior
of plants as it integrates several relevant components of whole-plant responses to
drought. While a unique definition of isohydry is still missing (Martínez-Vilalta
and Garcia-Forner 2017), the recently introduced concept of the ‘hydroscape area’
(HSA) (Meinzer et al. 2016) represents a major step in that direction (cf., Li et al.
2019). Building upon the framework by Martínez-Vilalta et al. (2014), the HSA defines
the water potential landscape, i.e., the ranges of predawn and midday potentials,
over which stomata are able to regulate leaf water potential during soil drying and
prior to drought-induced stomatal closure (Meinzer et al. 2016, Fu and Meinzer 2019).
In the hydroscape framework, the degree of isohydry (i.e., the degree of stringency
in the stomatal response) of a plant is expressed based on the area between the 1:1
line and the regression through midday (P
md) versus pre-dawn (P
pd) leaf water potential (blue triangular area in Figure 1). As anisohydric species
under dry conditions tend to close their stomates later than isohydric species, their
P
md is below their P
pd over a wider range of water potentials, which results in a larger HSA. A low slope
β in this relationship (Fu and Meinzer 2019), for example, is indicative of a reliance
on internally stored water, while high values of β suggest an influence of osmotic
adjustment (Figure 1). Notably, as P
md has to approach P
pd after complete stomatal closure (Meinzer et al. 2016), which therefore dictates
the position of one of the points limiting the HSA, changes in P
st driven by osmotic adjustment may result in certain degree of plasticity in this
trait (Figure 1). Furthermore, the direct link between the HSA and P
st indicates that it may be useful as a complement to hydraulic safety margins based
on stomatal response (cf., Martin-StPaul et al. 2017), as they form a pair of composite
variables describing plant drought responses before and after reaching the point of
stomatal closure.
The study by Jiang et al. highlights the importance of a holistic whole-tree approach
that acknowledges the interdependency of the water and carbon balance of trees. As
identified by Martínez-Vilalta and Garcia-Forner (2017), isohydric species might not
be more carbon limited than anisohydric species, in contrast to the framework proposed
by McDowell et al. (2008). Instead, the conversion of starch to osmotically active
substances seems more important in more anisohydric species for shifting the P
tlp in response to seasonally declining P
L. Future research should assess the role of starch conversion in response to abscisic
acid signals (Thalmann and Santelia 2017) as a regulatory mechanism to lower the osmotic
potential in living cells. Several further interesting questions arise from the study
by Jiang et al. (i) Is osmotic adjustment only important for more anisohydric species,
and at what water potential does the conversion from starch to osmotically active
sugars begin? (ii) What happens with these sugars after returning to a normal water
status and are they still available for other biochemical processes? (iii) During
drought, how much carbon is used for osmotic adjustment and how much is available
for respiration? (iv) Does osmotic adjustment of the stomatal response confer a link
between NSC status and HSA?
Answering such questions would also feed back into the hydraulic framework of McDowell
et al. (2008), as both water and carbon relations become intertwined to a point where
carbon starvation does not merely refer to a lack of substrates for maintenance respiration,
but a supply shortness for the ensemble of plant functional processes, in particular
during drought. Measurements of carbohydrate concentrations thus lose their ability
to track the plant catabolic reservoir. Ultimately, to fully understand the causal
relationships between carbon metabolism and stomatal regulation as well as plant water
relations, it is imperative to study their behavior in response to the direct experimental
manipulation of NSC concentrations (cf., Sapes et al. 2020).