Oecologia (2009) 161:1524

DOI 10.1007/s00442-009-1364-3

C O N C E P T S , R E V I E WS A N D S Y N T H E S E S

The importance of nutritional regulation of plant water Xux

Michael D. Cramer Heidi-Jayne Hawkins
G. Anthony Verboom

Received: 14 July 2008 / Accepted: 23 April 2009 / Published online: 16 May 2009
Springer-Verlag 2009

Abstract Transpiration is generally considered a wasteful

but unavoidable consequence of photosynthesis, occurring
because water is lost when stomata open for CO2 uptake.
Additionally, transpiration has been ascribed the functions
of cooling leaves, driving root to shoot xylem transport and
mass Xow of nutrients through the soil to the rhizosphere.
As a consequence of the link between nutrient mass Xow
and transpiration, nutrient availability, particularly that of
NO3, partially regulates plant water Xux. Nutrient regulation of transpiration may function through the concerted
regulation of: (1) root hydraulic conductance through control of aquaporins by NO3, (2) shoot stomatal conductance
(gs) through NO production, and (3) pH and phytohormone
regulation of gs. These mechanisms result in biphasic
responses of water Xux to NO3 availability. The consequent trade-oV between water and nutrient Xux has important implications for understanding plant distributions, for
production of water use-eYcient crops and for understanding the consequences of global-change-linked CO2 suppression of transpiration for plant nutrient acquisition.
Keywords Agriculture Elevated carbon dioxide
Leaf size Nocturnal transpiration Water use eYciency

Communicated by Frederick C. Meinzer.

M. D. Cramer (&) H.-J. Hawkins G. A. Verboom
Department of Botany, University of Cape Town,
Private Bag X1, Rondebosch 7701, South Africa
e-mail: michael.cramer@uct.ac.za
M. D. Cramer
Faculty of Natural and Agricultural Sciences,
School of Plant Biology, The University of Western Australia,
35 Stirling Highway, Crawley, WA 6009, Australia

Introduction
The rate of global transpiration has recently been estimated
to be 0.52 mm day1, accounting for 41% of terrestrial
evapotranspiration (Lawrence et al. 2007). When combined
with estimates of global terrestrial gross primary productivity (GPP; 120 Pg C year1; Schlesinger 1997) and net primary production (NPP; 66 Pg C year1; Haberl et al. 2007),
this indicates a global terrestrial water use eYciency
(WUE; mmol CO2 mol1 H2O) of 7.9 for GPP and 3.4 for
NPP. Thus, transpiration consumes 297 mol H2O per mol
CO2 acquired by global NPP. On the basis of typical C
concentrations in crops (45%; Epstein and Bloom 2005)
and the likely maximum C concentration in wood (55%;
Lamlom and Savidge 2003), this equates to between 200
(crop) and 245 (wood) l H2O kg1 biomass produced globally. Since water availability is a major limitation on terrestrial plant production and a key determinant in the
structuring of vegetation worldwide (e.g. Sankaran et al.
2005), an understanding of the physiological factors that
determine this WUE is extremely important. For example,
agriculture consumes 8090% of water available for human
consumption worldwide (Hamdy et al. 2003), leading to
signiWcant eVorts to increase the eYciency of water use in
agriculture, partially through manipulation of plant WUE
(Condon et al. 2004).
Currently, our understanding of plant water use is
largely informed by the notion that transpirational water
loss is to some extent a micrometeorologically unavoidable evil (Kramer and Boyer 1995) that occurs because
evolution has not succeeded in producing a membrane that
is CO2-permeable but water-impermeable (Cowan 1977)
and water is lost when stomata open for CO2 uptake (von
Caemmerer and Baker 2007). As such, it has also been
described as the dilemma of land plants (Raschke 1976).

123

16

Consequently photosynthesis incurs a water cost and, over

a period of time (e.g. daily or weekly), plants are thought to
optimise their WUE by adjusting the rate of photosynthesis
(A) relative to that of transpiration (E) (Farquhar et al.
2002; Chaves et al. 2004). This is achieved through tight
stomatal control of water loss in most terrestrial plants, as
well as other traits that reduce water consumption (e.g. C4
and CAM photosynthesis, hairy leaves, sunken stomata,
etc.). This control of water Xux is essential for limiting variation in plant water potential (
) with changes in soil
moisture and evaporative demand, thus, preserving the
integrity of the soilplant hydraulic continuum (Sperry
et al. 2002).
Since photosynthesis and transpiration are both physiologically complex, WUE lacks a simple optimum and
plants display a broad range of WUE. For example, the
minimum and maximum quartiles for photosynthesis per
stomatal conductance (A/gs, as a proxy for WUE) across
430 C3 species are 0.022 and 0.084 mmol mol1 (based on
the data presented by Wright et al. 2004). Various factors
determine the low WUE exhibited by some plants. Firstly,
A is strongly determined by photosynthate sink demand
(Wardlaw 1990; Ho 1992; Foyer et al. 1995; Paul and
Foyer 2001; Paul et al. 2001; McCormick et al. 2006, 2008)
due to the eVect of the latter on the activity of photosynthesis-related enzymes and expression of associated gene transcripts (Sheen 1990, 1994; Koch 1996; Pego et al. 2000;
Paul and Foyer 2001; Rolland et al. 2002). Thus, biochemical regulation of A provides a mechanism for the rapid
adjustment of WUE. Secondly, mesophyll resistance to
CO2 movement to the site of carboxylation is an important
and variable component of the overall conductance of a
leaf to CO2 (Warren and Adams 2006; Flexas et al. 2008;
Warren 2008). Both mesophyll resistance and biochemical
regulation can result in some mismatch between gs and
A. For example, across a range of C3 species A/gs was
smaller when gs exceeded 0.4 mol m2 s1 (Hetherington
and Woodward 2003), indicating a variable inXuence of gs
on photosynthesis. Finally, contrary to its interpretation
merely as an unavoidable consequence of CO2 uptake, transpiration may fulWl important physiological functions in its
own right.
The textbook functions of transpiration are to cool
leaves, in some situations, and to power the transport of solutes via the xylem from the root to the shoot (Lambers et al.
2008). While both of these functions are undoubtedly
important, neither fully accounts for the observed transpirational behaviour of plants. For example, a leaf cooling
function is not consistent with mid-day stomatal closure in
many plants (e.g. Roessler and Monson 1985; Jones 1992)
and does not explain the widely observed occurrence of
signiWcant nighttime transpiration (Howard and Donovan
2007). Also, measured rates of transpiration considerably

123

Oecologia (2009) 161:1524

exceed those required for root to shoot solute transport in

hydroponically grown Zea mays (Tanner and Beevers
1990) and Helianthus annuus (Tanner and Beevers 2001).
Here, we explore a third but frequently neglected function of transpiration, that of powering mass Xow in the soil,
where it is important in delivering nutrients to the rhizosphere (Barber 1962, 1995; Tinker and Nye 2000). Interception of nutrients as roots grow through the soil depends
on root density (Kage 1997), but generally accounts for a
small proportion of nutrient acquisition, the balance arriving at the root surface as a consequence of mass Xow or
diVusion (Clarkson 1981). This mass-Xow component of
soil nutrient transport, Wrst propounded by Woodward
(1699), is widely recognised and is a standard inclusion in
models of soil nutrient Xuxes (e.g. Nye and Marriott 1969;
HoZand et al. 1990; Rengel 1993; Greenwood and
Karpinets 1997). Transpiration-driven mass Xow may result
in substantial delivery of nutrients to the root surface; for
example, Zea mays, growing in a fertile loam, potentially
accumulated 79% N, 5% P, 18% K, 73% Ca, 88% Mg and
95% S by mass Xow, the remainder being taken up through
diVusion and interception by the roots (Barber 1995). Mass
Xow and diVusion of nutrients into the rhizosphere is
followed by uptake into the root tissue and transport across
a plasmalemma by an appropriate transport system for a
given nutrient (e.g. the H+ symporters responsible for NO3
uptake; Miller and Cramer 2004). However, for many nutrients mobility in the soil limits the uptake by the root, rather
than the activity of the plasmalemma transport systems
(Clarkson 1981; Kage 1997). The eVectiveness of mass
Xow depends on factors that inXuence transpiration (e.g.
temperature; Lambers et al. 2008) as well as nutrient type,
due to its dependence on nutrient concentration, solubility
and mobility in the soil (Barber 1995). This results in considerable variation in the extent to which species depend on
mass Xow for delivering particular nutrients, this being
additionally determined by edaphic and climatic factors
(Rengel 1993). Unlike the situation with diVusion to the
root, which is partially driven by root uptake, mass Xow is
less discriminate and all soluble components in the soil
solution will be moved into the rhizosphere. This accounts
for the accumulation of Ca at the surface of roots (Barber
and Ozanne 1970) and the consequent formation of rootassociated carbonates in some plants (e.g. root casts;
Cramer and Hawkins 2009).
If transpiration-driven mass Xow is an important nutrient
acquisition strategy, then soil nutrient availability may at
least partially regulate transpiration. The reported eVects of
nutrition on transpiration are variable (e.g. Radin and
Ackerson 1981; Chapin et al. 1988; Ciompi et al. 1996; Cechin
and Fumis 2004). This variability is probably the consequence of whole plant water Xux being determined by the
combination of both root and shoot hydraulic conductivities

Oecologia (2009) 161:1524

and also variability of nutrient forms (e.g. NO3 vs. NH4+)

and availability between experiments. In a direct test of the
prediction that soil nutrient availability may regulate transpiration-driven mass Xow, the C3 grass Ehrharta calycina
showed a 60% increase in transpiration when forced to
acquire nutrients through mass Xow, and accumulated several nutrients (e.g. Na, Ca) in accord with the relatively
indiscriminate nature of mass Xow compared to diVusion
(Cramer et al. 2008). The observation of increased transpiration in response to nutrient limitation is in accord with the
common observation that WUE is reduced under nutrient
limitation as a consequence of changes in gs and density
and, consequently, overall leaf conductance (reviewed by
Raven et al. 2004). The possibility that nutrition regulates
transpiration may underpin the trade-oV between WUE and
nutrient use eYciency (e.g. Field et al. 1983; Fredeen et al.
1991; Patterson et al. 1997; Wright et al. 2003). In particular, a regulatory role for N may result in WUE being
traded-oV against N use eYciency (NUE; e.g. Patterson
et al. 1997). Thus, the hypothesis that nutrient availability
partially regulates transpiration is consistent with an extensive body of literature, but further direct tests of the hypothesis are still required.

Mechanisms for the trade-oV between water

and nutrient use eYciencies
The correlation between photosynthesis and leaf [N] provides a mechanism for the trade-oV between WUE and
NUE. The bulk of leaf N is associated with photosynthetic
enzymes, particularly rubisco (Lambers et al. 2008). This
results in a strong positive correlation between A and leaf
[N] (e.g. Shulze et al. 1994; Wright et al. 2003), despite the
fact that photosynthesis is a highly regulated process, under
the control of multiple metabolic regulatory elements
(e.g. Stitt and Krapp 1999), not only leaf [N] and [CO2].
With higher leaf [N], the increased availability of photosynthetic protein is thought to increase the draw-down of
internal CO2, resulting from higher A at a given gs (Patterson
et al. 1997; Wright et al. 2003), and consequently higher
WUE. We suggest, however, that the requirement for transpiration-driven mass Xow of nutrients provides a powerful
additional mechanistic reason for the trade-oV of WUE and
NUE.
Nutrient regulation of water Xux through plants may be
through N-Xux-linked signalling mechanisms (e.g. Wilkinson
et al. 1998, 2007; Clarkson et al. 2000; Desikan et al. 2002;
Gloser et al. 2007) that operate in both roots and shoots.
Root hydraulic conductance varies on a diurnal basis
(Parsons and Kramer 1974; Carvajal et al. 1996) due to
changes in the expression of water channels (i.e. aquaporins). These aquaporins are plasma membrane intrinsic

17

proteins that facilitate water Xux by increasing root hydraulic

conductivity, and are strongly expressed in the roots of several species, particularly in the exodermis, endodermis and
vascular tissue (Maurel et al. 2008). Aquaporins are gated
through phosphorylation by Ca-dependent kinases (Maurel
2007) providing a potential mechanism for nutrient-mediated regulation of water Xux (Chaumont et al. 2005).
Although the molecular and cellular mechanisms involved
in regulation of aquaporins are still not fully understood,
there are strong indications that aquaporin activity modiWes
water Xux in roots, in response to nutrients. For example,
deprivation of N, P, or S results in a signiWcant inhibition of
water transport associated with aquaporin functioning in
whole roots or individual root cells within a few days
(reviewed by Maurel et al. 2008). Conversely, increasing
rhizosphere [NO3] above deWciency has been shown to
rapidly increase aquaporin-mediated root hydraulic conductivity (Carvajal et al. 1996; Clarkson et al. 2000; Gloser
et al. 2007; Gorska et al. 2008). Since tungstate inhibited
nitrate reductase (NR), its failure to inhibit aquaporinmediated hydraulic conductivity suggests that NO3 itself
(Fig. 1), rather than its reduction/assimilation products, is
responsible for regulating aquaporin expression (Gorska
et al. 2008). These authors speculated that the functional
signiWcance of NO3-induced increases of water Xux is to
facilitate mass Xow of NO3 to the roots when NO3 was
available. This may be particularly important when soil N
availability is limited, but not deWcient.
[NO3] has a biphasic inXuence on gs (Wilkinson et al.
2007), increasing from deWciency to a maximum and
decreasing with further increases in [NO3]. Increasing
[NO3] above suYciency rapidly (hours) elicits concentration-dependent stomatal closure (Wilkinson et al. 2007),
possibly mediated by changes in xylem pH, abscisic acid
(ABA) signalling (Wilkinson et al. 1998) and NO signalling (Desikan et al. 2002; Neill et al. 2008). This signalling
system becomes ineVective with prolonged N deWciency
resulting in decreased water Xux (Radin and Parker 1979),
probably in response to N starvation.
The induction of root water Xux by NO3 may at Wrst
seem inconsistent with the biphasic inXuence on gs and
observed transpirational responses of plants to nutrient deWciency. Transpirational responses to nutrients, however,
represent the result of complex and overlapping regulatory
mechanisms that allow plants to modulate water Xux in
response to diverse nutritional and other environmental
challenges. The site of NO3 reduction and subsequent
assimilation of NH4+ in the plant varies between root and
the shoot tissues, depending on species, developmental
stage and nutritional environment (Wallace 1986). Above a
minimum threshold, determined by the capacity of NR in
the root (Andrews 1986), the proportion of NO3 that is
reduced in the shoot increases with [NO3] (Oaks 1986;

123

18

Oecologia (2009) 161:1524

Amino
acids
Stoma

NH4+

Protein

NO2-

NO
Stoma

H2O

Leaf

Stem

NO3-

Xylem
Mass-flow
Amino
acids
NH4+
NO2-

H2O
NO3-

H2O
NO3-

Mass-flow

NO3-

H2O
NH4+

Root
Root cap

NH4+
N flux
Water flux
Root hair
Aquaporin
NO3- transporter
NH4+ transporter
Positive regulation

Fig. 1 Proposed mechanism for the biphasic control of water Xux by

NO3 and the lack of similar control by NH4+ of water Xux. Uptake of
NH4+ is shown to occur closer to the root tip than that of NO3 (Bloom
et al. 2003) which enters with water in the region in which root hairs
occur (Javot and Christophe 2002). NH4+ uptake and its assimilation
products do not alter water Xux directly, possibly resulting in aspects
of the ammoniacal syndrome. In contrast, NO3 stimulates (positive
feedback) expression/activity of root aquaporins. NO3 uptake in excess of the capacity of root nitrate reductase (NR) for reduction is
transported to the shoot where NO is produced by NR during its reduction to NO2 (Desikan et al. 2002; Neill et al. 2008). NO is indicated
to induce stomatal closure. NO2 is reduced to NH4+ by nitrite reductase and NH4+ is assimilated into amino acids through the activity of
glutamine synthetase/glutamate-2-oxoglutarate amino-transferase.
Details of associated pH changes, phytohormone Xuxes (e.g. Wilkinson
et al. 2007), energetic Xuxes (e.g. ATP or NAD(P)H) or C Xuxes have
not been indicated

Wallace 1986). Below this threshold, Xuxes of NO3 into

the root are likely to result in increased root hydraulic conductivity, such as that demonstrated by Gorska et al.
(2008), and consequently sustained transpiration. However,
NO3 Xuxes in excess of the root NR capacity will result
in NO3 being transported to the shoot where its conversion to NO by NR induces stomatal closure (Desikan et al.
2002; Neill et al. 2008) and reduced water Xux. Transpiration and NR activity do co-vary (Rufty et al. 1987), consistent with NO3 regulation of NR activity and NO
production from NO3. We suggest that this provides a

123

novel mechanism for the biphasic regulation of water Xux

in intact plants by NO3 concentration that was observed
by Wilkinson et al. (2007). Changes in loading of NO3
into the xylem may also result in alteration of xylem pH
(Mengel et al. 1994) with additional consequences for stomatal regulation through enhanced ABA transport to guard
cells (Wilkinson et al. 2007), accounting for the synergistic
eVects of xylem NO3 and ABA on gs observed by Jia and
Davies (2007). The mechanism proposed here would facilitate transpiration-driven mass Xow when NO3 supply is
limited and decrease mass Xow when NO3 is suYcient to
trigger stomatal closure (Fig. 1). Importantly, an N-mediated signalling mechanism would enable plants to measure
inorganic N Xux and increase transpiration rates to drive
mass Xow when soil N is limited (but not deWcient).
Unlike NO3, NH4+ nutrition does not alter root hydraulic conductance or increase the expression of aquaporins in
the root (Guo et al. 2007a). In most species, NH4+ taken up
by roots is assimilated into amino acids in the roots
(reviewed by Miller and Cramer 2004), and NH4+ does not
appear to elicit the closing response of stomata. Plants supplied with NH4+ generally have lower WUE than those supplied with NO3 (Raven et al. 2004; Guo et al. 2007a, b)
and the symptoms of NH4+ toxicity include growth inhibition, wilting and other indications of water stress (Cramer
and Lewis 1993). These changes, dubbed the ammoniacal
syndrome (Chaillou and Lamaze 2001), have previously
been ascribed to cation/anion imbalances (reviewed by
Miller and Cramer 2004). This water stress, however,
probably additionally results from the lack of co-ordinated
regulation of root hydraulic conductance and gs. High
concentrations of NH4+ associated with agriculture are
uncommon in natural ecosystems and plants may thus lack
the mechanisms to respond to these conditions. The biphasic sensitivity of transpiration-driven water Xow to NO3
also provides a mechanism for plants to sense the eYcacy
of mass Xow to the root, since NO3 is readily mobilised by
mass Xow in many soils; in contrast, NH4+ cations bind to
soil more readily and are less likely to be mobilised by
mass Xow. The mechanism proposed here (Fig. 1) provides
a novel explanation for the observed disparate eVects of
NO3 or NH4+ nutrition on plant water relations.
The foregoing discussion neglects some of the complexity of soilroot interactions. NO3 and NH4+ availabilities
in soil can vary by an order of magnitude over the course of
a day and over a the space of a few centimetres (Jackson
and Bloom 1990). Altering the hydraulic properties of a
small part of the root system in response to local conditions
would enable eVective control of the utilisation of water by
that portion of the root. For example, as a root depletes
NO3 in the soil zone, the consequently reduced hydraulic
conductance would potentially allow diversion of water to
other portions of the soil where NO3 is less limiting. Root

Oecologia (2009) 161:1524

responses to NO3 and NH4+ also diVer strongly. Roots of

many plants proliferate rapidly in patches of NO3, but not
in patches of NH4+ (reviewed by Miller and Cramer 2004).
This diVerential sensitivity of root proliferation to NO3
and NH4+ has been argued to occur because roots have
evolved to use NO3 rather than NH4+ as a signal molecule
owing to their diVerential mobilities in the soil (Zhang and
Forde 2000). Consistent with the lower mobility of NH4+,
plants develop thinner and longer roots when NH4+ is the
primary N source (Bloom et al. 2003). In both rice and
maize, NH4+ absorption was higher at the root apex,
whereas NO3 absorption was greatest in the root hair zone
(Colmer and Bloom 1998), where hydraulic conductivity
associated with aquaporins is concentrated (Javot and
Christophe 2002; Hachez et al. 2006). Thus, as the root
grows through the soil the tip may Wrst take up more of the
relatively immobile NH4+ than NO3 and subsequently, as
the root continues to grow, the region of the root around the
root hairs takes up NO3 transported into the rhizosphere
by mass Xow (Fig. 1).
The mass Xow of nutrients other than N depends on the
Xux of water, the soil concentration of the nutrient and its
mobility (Barber 1995). Thus, N regulation of water Xux
provides a mechanism for N Xux to regulate the mass Xow
of other nutrients to the rhizosphere (e.g. Cramer et al.
2008, 2009). It is, however, possible that nutrients other
than N could also play a role in controlling water Xux. At
the root level, for example, relief from P deWciency rapidly
increased root hydraulic conductivity (Radin and Eidenbock
1984; Carvajal et al. 1996) probably due to increased
aquaporin expression (Clarkson et al. 2000). Increased P
supply has also been shown to increase WUE in several
species (reviewed by Raven et al. 2004), but this may be
largely due to the relief of photosynthesis from P limitation
(e.g. Jacob and Lawlor 1991), rather than any P-induced
decrease in transpiration. While there may be a role for P in
regulating water Xux, its eVectiveness in this role may be
limited by its low mobility in many high cation exchange
capacity (CEC) soils (Barber 1995; Kramer and Boyer
1995). However, mass Xow of P can be substantial in
low-CEC soils, raising the possibility that mass Xow could
contribute to P supply to roots in such soils (Cramer and
Hawkins 2009), although this requires further investigation.

Adaptations that promote water loss

Supporting the idea that transpiration is a design feature of
plants, rather than a design Xaw, plants have several attributes that enhance water loss. These attributes ensure water
Xux into the leaf tissue to meet the demands for water
imposed by transpiration, whether as a consequence of the
micrometeorology associated with CO2 Xux or the other

19

functions of transpiration. An example of such an attribute

is the extent and density of venation in leaves, which dictates the hydraulic conductivity of leaf tissue (Brodribb
et al. 2007). This considerably exceeds that which is necessary to meet the minimal water requirements of tissue
expansion and photosynthetic water splitting. In addition,
aquaporins in the mesophyll cells of several species function to promote water Xux (KaldenhoV and Fischer 2006;
Sakurai et al. 2008). In Juglans regia, light-mediated activation of leaf aquaporins resulted in a rapid (<1 h) and
spectacular 400% increase in hydraulic conductivity which
was independent of its eVect on gs (Cochard et al. 2007).
This light-induced increase in hydraulic conductivity is at
odds with the notion that water loss is necessitated only by
leaf micrometeorology.
Further, the widespread lack of features that might
reduce water loss, such as leaf hair and sunken stomata,
may be construed as mechanisms that promote water loss,
although these features generally inXuence both water and
CO2 Xux. However, changes in leaf attributes inXuencing
gas exchange do not necessarily inXuence water loss and
CO2 gain equally. For instance, stomatal crypts have a
greater impact on water conservation than on CO2 Xux
(Roth-Nebelsick 2007). Although reduced or highly dissected leaves are usually interpreted as a mechanism to
ensure close coupling of leaf and air temperatures, they
also promote water loss (Parkhurst and Loucks 1972;
Roth-Nebelsick 2001) through decreased boundary layer
resistance (Nobel 1999). This may explain why small or
dissected leaves are common in nutrient-impoverished
Mediterranean-type ecosystems in which nutrients are most
available for acquisition in the cold and wet winter period.
For example, Nicotra et al. (2008) found that leaf dissection
in Pelargonium species native to such an ecosystem (South
African fynbos) did not correlate with climatic variables,
and concluded that dissected leaves, high A, and relatively
low WUE had evolved as a strategy to optimize water
delivery and C gain during short-lived periods of high soil
moisture. We suggest that this optimization of water
delivery during periods of high soil moisture serves to drive
mass Xow of nutrients to the roots, a process that may be
particularly important in low-CEC soils.
The extent to which plants close their stomata at night
has been considered a vexing question (Darwin 1898) for
a long time. Nighttime water loss does account for a substantial proportion of seasonal water loss in some systems
(e.g. >10% in paper birch; Daley and Phillips 2006).
Dawson et al. (2007) list four potential functions for nighttime water loss, suggesting that it: facilitates CO2 uptake
early in the day because stomata are already open; enhances
root to shoot nutrient translocation; maintains O2 supply to
woody tissues at night; occurs because cuticles, particularly
of older leaves, are leaky. Recent evidence indicates,

123

20

however, that nighttime water loss is considerably faster

than cuticular leakage and is regulated much like daytime
water loss (Caird et al. 2007). The possible role of nighttime transpiration in nutrient acquisition has been raised by
several authors. In some species nighttime water loss is
responsive to the availability of nutrients (e.g. Scholz et al.
2007), while in others no response has been found (e.g.
Howard and Donovan 2007). Decreased day and night gs of
Helianthus anomalus in response to N and P fertilizers
were interpreted as a consequence of lower plant

imposed by greater water consumption by bigger, fertilized
plants (
= 0.49 MPa) compared to control plants
(
= 0.42 MPa; Ludwig et al. 2006). However, these
s
are not very negative and the diVerences between them are
small. Alternatively, these data are consistent with the proposed N regulation of water Xux (Fig. 1), both during the
day and night. As implied by Howard and Donovan (2007),
the diversity of responsiveness of nighttime water Xux to
nutrients may be the consequence of the diVerences in the
control of water loss between species, environmental conditions and variation in concentration and forms of nutrients
available to the plants. We think that a nutritional role for
nighttime water loss is likely, but further research is
required to fully resolve the responsiveness of nighttime
water Xux to nutrients.

Increased atmospheric [CO2] increases WUE

Elevated CO2 has been shown to reduce aboveground plant
tissue [N] by 14% (both C3 and C4), with C3 plants
responding more strongly (16%) than C4 plants (7%) or C3
legumes (7%) (Cotrufo et al. 1998). Although increased
total non-structural carbohydrates (TNC) may provide a
partial explanation for this [N] reduction through a dilution
eVect (Krner 2000), the eVect remains even after correcting for increased TNC (Schppi and Krner 1997; Krner
2000; Onoda et al. 2007). The decline of tissue [N] with
elevated CO2 could be ascribed to a reduced N requirement
for rubisco formation, combined with sugar-sensing of
increased photosynthate availability (Stitt and Krapp 1999).
This is consistent with the smaller sensitivity of C4 plant
tissue [N] to elevated CO2 due to smaller changes in C4
sugar concentrations, but does not explain why legume [N]
was not reduced to the same extent as that in other C3
plants. An alternative explanation is that mass-Xow-driven
nutrient acquisition was constrained by CO2-induced stomatal closure. In free-air CO2 enrichment experiments, the
average decrease in gs in response to elevated CO2 (ca.
567
mol mol1) was 22% (including C3 and C4 plants),
this change being associated with a reduction in stomatal
aperture rather than stomatal density (Ainsworth and
Rogers 2007). Reduced mass Xow has previously been

123

Oecologia (2009) 161:1524

invoked as an explanation for limited plant N acquisition in

response to elevated CO2 (Conroy and Hocking 1993). In
Populus deltoids reduced N uptake was ascribed to reduced
gs in response to both high CO2 and humidity (McDonald
et al. 2002). Since the rate of mass Xow of individual nutrients depends on soil chemistry rather than plant demand,
reduced mass Xow may be expected to limit the uptake of
several nutrients simultaneously. A general decline in the
concentrations of several nutrients (P, K, Ca, S, Mg, Fe, Zn,
Mn and Cu) with elevated CO2 has been reported from a
meta-analysis based on 19 herbaceous and 11 woody species (Loladze 2002). The extent of this general decrease in
plant nutrient concentrations may be dictated by N regulation of plant water Xux (Fig. 1), consistent with the reported
NO-induced stomatal closure triggered by elevated CO2
(Kolla and Raghavendra 2007). Suppression of transpiration-driven mass Xow may contribute to the unresponsiveness of many natural ecosystems to increased atmospheric
[CO2] noted by Krner (2006).

WUE in agriculture
Crop water use is determined by a large variety of factors
including soil physical characteristics (e.g. clay content),
crop density, genotype, root interception of water and the
proportion of exposed soil surface (Gregory 2004), providing diverse opportunities for manipulating crop water use.
The responsiveness of crop water use eYciency to N application rates results partially from N-induced crop intensiWcation occurring because of greater biomass per land area
(Asseng et al. 2001). However, manipulation of leaf-level
WUE has been proposed as a mechanism to improve overall crop water use. Some success in manipulating leaf WUE
has been reported for wheat, although this was related to
early vigour of the crop during the cool, wet part of the
growing season (Condon et al. 2004). Considering that leaf
WUE increases with nutrition (Raven et al. 2004), it is
likely that increased N application rates over the past
decades (reviewed by Miller and Cramer 2004) have
already increased the WUE of crops through decreased
dependence on mass Xow. The trade-oV of water Xux for
nutrient availability, however, means that the viability of
breeding or genetic modiWcation to reduce crop transpiration (e.g. Condon et al. 2004), depends on nutrient availability, since reducing water consumption by the plants
may limit productivity, especially in nutrient-limited soils.
There are relatively few reports that directly compare the
respective importance of mass Xow, diVusion and root
interception for nutrient acquisition (e.g. Barber 1962;
Strebel and Duynisveld 1989; Kramer and Boyer 1995;
Kage 1997; Lambers et al. 2008). However, the role of
mass Xow in nutrient delivery varies with many factors

Oecologia (2009) 161:1524

including soil nutrient concentrations, soil CEC, water

availability, atmospheric vapour pressure deWcit and plant
genotype. This lack of information is a glaring oversight in
eVorts directed towards maximising crop WUE.

Conclusion
Although water availability has long been recognised as
an important determinant of nutrient diVusive mobility in
the soil, the potential importance of transpiration-driven
mass Xow strengthens the interaction between water and
nutrient availability, providing an additional mechanism
for the trade-oV of water Xux and nutrient acquisition.
This raises the possibility that some plants are designed
not to conserve water, but rather to maximise the Xux of
water when it is abundant. This has far-reaching implications for the interpretation of the distributions of plants
and their adaptations, in relation to environmental gradients. Furthermore, the notion that nutrients, particularly
N, partially regulate transpiration could inform crop management and the understanding of issues such as the
mechanism through which N fertilization, particularly
using NO3 rather than NH4+, reduces salinity toxicity
(e.g. Hawkins and Lewis 1993).
Acknowledgments Funding was from the University of Cape Town
URC awards, National Research Foundation and Protea Producers of
South Africa. We are grateful for useful comments from the anonymous reviewers.

References
Ainsworth EA, Rogers A (2007) The response of photosynthesis and
stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258270
Andrews M (1986) The partitioning of nitrate assimilation between
root and shoot of higher plants. Plant Cell Environ 9:511519
Asseng S, Turner NC, Keating BA (2001) Analysis of water- and nitrogen-use eYciency of wheat in a Mediterranean climate. Plant Soil
233:127143
Barber SA (1962) A diVusion and mass-Xow concept of soil nutrient
availability. Soil Sci 93:3949
Barber SA (1995) Soil nutrient bioavailability: a mechanistic
approach, 2nd edn. Wiley, New York
Barber SA, Ozanne OG (1970) Autoradiographic evidence for the
diVerential eVect of four plants species in altering the calcium
content of the rhizosphere soil. Soil Sci Soc Am Proc 34:635637
Bloom AJ, MeyerhoV PA, Taylor AR, Rost TL (2003) Root development and absorption of ammonium and nitrate from the rhizosphere. J Plant Growth Regul 21:416431
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol
144:18901898
Caird MA, Richards JH, Donovan LA (2007) Night-time stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol
143:410

21
Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat
plants to nutrient deprivation may involve the regulation of waterchannel function. Planta 199:372381
Cechin I, Fumis TD (2004) EVect of nitrogen supply on growth and
photosynthesis of sunXower plants grown in the greenhouse.
Plant Sci 166:13791385
Chaillou S, Lamaze T (2001) Ammoniacal nutrition of plants. In:
Morot-Gaudry J-F (ed) Nitrogen assimilation by plants. Science
Publishers, NH, pp 5369
Chapin FSIII, Walter CHS, Clarkson DT (1988) Growth response of
barley and tomato to nitrogen stress and its control by abscisic
acid, water relations and photosynthesis. Planta 173:352366
Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant
aquaporin activity. Biol Cell 97:749764
Chaves MM, Osrio J, Pereira JS (2004) Water use eYciency and
photosynthesis. In: Bacon MS (ed) Water use eYciency in plant
biology. Blackwell, Oxford
Ciompi S, Gentili E, Guidi L, Soldanti GF (1996) The eVect of nitrogen
deWciency on leaf gas exchange and chlorophyll Xuorescence
parameters in sunXower. Plant Sci 118:177184
Clarkson DT (1981) Nutrient interception and transport by root
systems. In: Johnson CB (ed) Physiological factors limiting plant
productivity. Butterworths, London, pp 307314
Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ,
Cooke DT, Steudle E (2000) Root hydraulic conductance: diurnal
aquaporin expression and the eVects of nutrient stress. J Exp Bot
51:6170
Cochard H, Venisse J-S, Barigah TS, Brunel N, Herbette S, Guilliot A,
Tyree MT, Sakr S (2007) Putative role of aquaporins in variable
hydraulic conductance of leaves in response to light. Plant Physiol
143:122133
Colmer TD, Bloom AJ (1998) A comparison of NH4+ and NO3 net
Xuxes along roots of rice and maize. Plant Cell Environ 21:240
246
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use eYciency. J Exp Bot 55:24472460
Conroy J, Hocking P (1993) Nitrogen nutrition of C3 plants at elevated
atmospheric CO2 concentrations. Physiol Plant 89:570576
Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Chang Biol 4:4354
Cowan IR (1977) Stomatal behavior and environment. Adv Bot Res
4:117228
Cramer MD, Hawkins H-J (2009) A physiological mechanism for the
formation of root casts. Palaeogeogr Palaeoclimatol Palaeoecol
274:125133
Cramer MD, Lewis OAM (1993) The inXuence of NO3 and NH4+
nutrition on the growth of wheat (Triticum aestivum) and maize
(Zea mays) plants. Ann Bot 72:359365
Cramer MD, HoVmann V, Verboom GA (2008) Nutrient availability
moderates transpiration in Ehrharta calycina. New Phytol
179:10481057
Daley MJ, Phillips NG (2006) InterspeciWc variation in night-time
transpiration and stomatal conductance in a mixed New England
deciduous forest. Tree Physiol 26:411419
Darwin F (1898) Observations on stomata. Proc R Soc Lond 63:413
417
Dawson TE, Burgess SSO, Tu KP, Oliveira RS, Santiago LS, Fisher JB,
Simonin KA, Ambrose AR (2007) Night-time transpiration in woody
plants from contrasting ecosystems. Tree Physiol 27:561575
Desikan R, GriYths R, Hancock J, Neill S (2002) A new role for an old
enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis
thaliana. Proc Natl Acad Sci USA 99:1631416318
Epstein E, Bloom AJ (eds) (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer, Sunderland

123

22
Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control
in relation to leaf area and nitrogen content. Silva Fenn 36:625
637
Field C, Merino J, Mooney HA (1983) Compromises between wateruse eYciency and nitrogen-use eYciency in Wve species of
California evergreens. Oecologia 60:384389
Flexas J, Ribas-Carb M, Diaz-Espejo A, Galmsl J, Medrano H
(2008) Mesophyll conductance to CO2: current knowledge and
future prospects. Plant Cell Environ 31:602621
Foyer CH, Chaumont M, Murchie E, Galtier N, Ferrario S (1995)
End-product modulation of carbon partitioning with a view to
improved biomass production. In: Madore MA, Lucas WJ (eds)
Carbon partitioning and sourcesinks interactions in plants.
American Society of Plant Physiologists, Rockville, pp 4555
Fredeen AL, Gamon JA, Field CB (1991) Responses of photosynthesis
and carbohydrate-partitioning to limitation in nitrogen and water
availability in Weld-grown sunXower. Plant Cell Environ 14:963
970
Gloser V, Zwieniecki MA, Orians CM, Holbrook NM (2007) Dynamic
changes in root hydraulic properties in response to nitrate availability. J Exp Bot 58:24092415
Gorska A, Ye Q, Holbrook NM, Zwieniecki MA (2008) Nitrate control
of root hydraulic properties in plants: translating local information to whole plant response. Plant Physiol 148:11591167
Greenwood DJ, Karpinets TV (1997) Dynamic model for the eVects of
K-fertilizer on crop growth, K-uptake and soil-K in arable cropping. 1. Description of the model. Soil Use Manage 13:178183
Gregory PJ (2004) Agronomic approaches to increasing water use eYciency. In: Bacon MA (ed) Water use eYciency in plant biology.
Blackwell, Oxford, pp 142170
Guo S, KaldenhoV R, Uehlein N, Sattelmacher B, Brueck H (2007a)
Relationship between water and nitrogen uptake in nitrate- and
ammonium-supplied Phaseolus vulgaris L. plants. J Plant Nutr
Soil Sci 170:7380
Guo S, Shen O, Brueck H (2007b) EVects of local nitrogen supply on
water uptake of bean plants in a split root system. J Integr Plant
Biol 49:472480
Haberl H, Erb KH, Krausmann F, Gaube V, Bondeau A, Plutzar C,
Gingrich S, Lucht W, Fischer-Kowalski M (2007) Quantifying
and mapping the human appropriation of net primary production
in earths terrestrial ecosystems. Proc Natl Acad Sci USA
104:1294212947
Hachez C, Moshelion M, Zelazny E, Cavezl D, Chaumont F (2006)
Localization and quantiWcation of plasma membrane aquaporin
expression in maize primary root: a clue to understanding their
role as cellular plumbers. J Plant Mol Biol 62:305323
Hamdy A, Ragab R, Scarascia-Mugnozza E (2003) Coping with water
scarcity: water saving and increasing water productivity. Irrig
Drain 52:320
Hawkins H-J, Lewis OAM (1993) Combination eVect of NaCl Salinity, nitrogen form and calcium concentration on the growth, ionic
content and gaseous exchange properties of Triticum aestivum L.
cv. Gamtoos. New Phytol 124:161170
Hetherington AM, Woodward FI (2003) The role of stomata in sensing
and driving environmental change. Nature 424:901908
Ho LC (1992) The possible eVects of sink demand for assimilate on
photosynthesis. In: Murata N (ed) Research in photosynthesis, vol
IV. Kluwer, Dordrecht, pp 729736
HoZand E, Bloemhof HS, LeVelaar PA, Findenegg GR, Nelemans JA
(1990) Simulation of nutrient uptake by a growing root system
considering increasing root density and inter-root competition.
Plant Soil 1124:149155
Howard AR, Donovan LA (2007) Helianthus night-time conductance
and transpiration respond to soil water but not nutrient availability. Plant Physiol 143:145155

123

Oecologia (2009) 161:1524

Jackson LE, Bloom AJ (1990) Root distribution in relation to soil
nitrogen availability in Weld-grown tomatoes. Plant Soil 128:115
126
Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of
photosynthesis in phosphate deWcient sunXower; maize and wheat
plants. J Exp Bot 42:10031011
Javot H, Christophe M (2002) The role of aquaporins in root water
uptake. Ann Bot 90:301313
Jia W, Davies WJ (2007) ModiWcation of leaf apoplastic pH in relation
to stomatal sensitivity to root-sourced ABA signals. Plant Physiol
143:6877
Jones HG (1992) Plants and microclimate: a quantitative approach to
environmental plant physiology, 2nd edn. Cambridge University
Press, Cambridge
Kage H (1997) Is low rooting density of faba beans a cause of high
residual nitrate content of soil at harvest? Plant Soil 190:4760
KaldenhoV R, Fischer M (2006) Aquaporins in plants. Acta Physiol
187:169176
Koch KE (1996) Carbohydrate-modulated gene expression in plants.
Annu Rev Plant Physiol Mol Biol 47:509540
Kolla VA, Raghavendra AS (2007) Nitric oxide is a signaling intermediate during bicarbonate-induced stomatal closure in Pisum sativum. Physiol Plant 130:9198
Krner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl
10:15901619
Krner C (2006) Plant CO2 responses: an issue of deWnition, time and
resource supply. New Phytol 172:393411
Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San Diego
Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology. Springer, New York
Lamlom SH, Savidge RA (2003) A reassessment of carbon content in
wood: variation within and between 41 North American species.
Biomass Bioenergy 25:381388
Lawrence DM, Thornton PE, Oleson KW, Bonan GB (2007) The partitioning of evapotranspiration into transpiration, soil evaporation, and canopy evaporation in a GCM: impacts on land
atmosphere interaction. J Hydrometeorol 8:862880
Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward
globally imbalanced plant stoichiometry? Trends Ecol Evol
17:457461
Ludwig F, Jewitt RA, Donovan LA (2006) Nutrient and water addition
eVects on day- and night-time conductance and transpiration in a
C3 desert annual. Oecologia 148:219225
Maurel C (2007) Plant aquaporins: novel functions and regulation
properties. FEBS Lett 581:22272236
Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins:
membrane channels with multiple integrated functions. Annu Rev
Plant Biol 59:595624
McCormick AJ, Cramer MD, Watt DA (2006) Sink-strength regulates
photosynthesis in sugarcane. New Phytol 171:759770
McCormick AJ, Cramer MD, Watt DA (2008) Changes in photosynthetic rates and gene expression of leaves during a sourcesink
perturbation in sugarcane. Ann Bot 101:89102
McDonald EP, Erickson JE, Kruger EL (2002) Can decreased transpiration limit plant nitrogen acquisition in elevated CO2? Funct
Plant Biol 29:11151120
Mengel K, Planker R, HoVmann B (1994) Relationship between leaf
apoplast pH and iron chlorosis of sunXower (Helianthus annuus
L.). J Plant Nutr 17:10531065
Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:136
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris
P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and
abiotic stress. J Exp Bot 59:165176

Oecologia (2009) 161:1524

Nicotra AB, Cosgrove MJ, Cowling A, Schlichting CD, Jones CS
(2008) Leaf shape linked to photosynthetic rates and temperature
optima in South African pelargonium species. Oecologia
154:625635
Nobel PS (1999) Physicochemical and environmental plant physiology. Academic Press, San Diego
Nye PH, Marriott FHC (1969) A theoretical study of the distribution of
substances around roots resulting from simultaneous diVusion
and mass-Xow. Plant Soil 30:459472
Oaks A (1986) Biochemical aspects of nitrogen metabolism in a whole
plant context. In: Lambers H, Neeteson JJ, Stulen I (eds) Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. NijhoV, Dordrecht, pp 133151
Onoda Y, Hirose T, Hikosaka K (2007) EVect of elevated CO2 levels
on leaf starch, nitrogen and photosynthesis of plants growing at
three natural CO2 springs in Japan. Ecol Res 22:475484
Parkhurst DF, Loucks OL (1972) Optimal leaf size in relation to environment. J Ecol 60:505537
Parsons LR, Kramer PJ (1974) Diurnal cycling in root resistance to
water movement. Physiol Plant 30:1923
Patterson TB, Guy RD, Dang QL (1997) Whole-plant nitrogen- and
water-relations traits, and their associated trade-oVs, in adjacent
muskeg and upland boreal spruce species. Oecologia 110:160
168
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp
Bot 52:13811400
Paul M, Pellny T, Goddijn O (2001) Enhancing photosynthesis with
sugar signals. Trends Plant Sci 6:197200
Pego JV, Kortsee AJ, Huijser C, Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot
51:407416
Radin JW, Ackerson RC (1981) Water relations of cotton plants under
nitrogen deWciency. III. Stomatal conductance, photosynthesis,
and abscisic acid accumulation during drought. Plant Physiol
67:115119
Radin JW, Eidenbock MP (1984) Hydraulic conductance as a factor
limiting leaf expansion of phosphorus-deWcient cotton plants.
Plant Physiol 75:372377
Radin JW, Parker LL (1979) Water relations of cotton plants under
nitrogen deWciency. I. Dependence upon leaf structure. Plant
Physiol 64:495498
Raschke K (1976) How stomata resolve the dilemma of opposing priorities. Philos Trans R Soc Lond B 273:551560
Raven JA, Handley LL, Wollenweber B (2004) Plant nutrition and
water use eYciency. In: Bacon MS (ed) Water use eYciency in
plant biology. Blackwell, Oxford
Rengel Z (1993) Mechanistic simulation models of nutrient uptake: a
review. Plant Soil 152:161173
Roessler PG, Monson RK (1985) Mid-day depression in net photosynthesis and stomatal conductance in Yucca glauca: relative contributions of leaf temperature and leaf-to-air water vapor
concentration diVerence. Oecologia 67:380387
Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in
plants. Plant Cell 14:S185S205
Roth-Nebelsick A (2001) Computer-based analysis of steady-state and
transient heat transfer of small-sized leaves by free and mixed
convection. Plant Cell Environ 24:631640
Roth-Nebelsick A (2007) Computer-based studies of diVusion through
stomata of diVerent architecture. Ann Bot 100:2332
Rufty TW Jr, Volk RJ, MacKown CT (1987) Endogenous NO3 in the
root as a source of substrate for reduction in the light. Plant Physiol 84:14211426
Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008)
Tissue and cell-speciWc localization of rice aquaporins and their
water transport activities. Plant Cell Physiol 49:3039

23
Sankaran M, Hanan NP, Scholes RJ, Ratnam J, Augustine DJ, Cade BS,
Gignoux J, Higgins SI, Le Roux X, Ludwig F, Ardo J, Banyikwa F,
Bronn A, Bucini G, Caylor KK, Coughenour MB, Diouf A, Ekaya
W, Feral CJ, February EC, Frost PGH, Hiernaux P, Hrabar H,
Metzger KL, Prins HHT, Ringrose S, Sea W, Tews J, Worden J,
Zambatis N (2005) Determinants of woody cover in African
savannas. Nature 438:846849
Schppi B, Krner CH (1997) In situ eVects of elevated CO2 on the carbon and nitrogen status of alpine plants. Funct Ecol 11:290299
Schlesinger WH (1997) Biogeochemistry: an analysis of global
change, 2nd edn. Academic Press, London, p 134
Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, MirallesWilhelm F (2007) Removal of nutrient limitations by long-term
fertilization decreases nocturnal water loss in savanna trees. Tree
Physiol 27:551559
Sheen J (1990) Metabolic repression of transcription in higher plants.
Plant Cell 2:10271038
Sheen J (1994) Feedback control of gene expression. Photosynth Res
39:427438
Shulze E, Kelliher FM, Korner C, Lloyd J, Leuning R (1994) Relationships among maximum stomatal conductance, ecosystem surface
conductance, carbon assimilation rate, and plant nitrogen nutrition: a global ecology scaling exercise. Annu Rev Ecol Syst
25:629662
Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deWcits and
hydraulic limits to leaf water supply. Plant Cell Environ 25:251263
Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583621
Strebel O, Duynisveld WHM (1989) Nitrogen supply to cereals and
sugar beet by mass Xow and diVusion on a silty loam soil. Z Pfalnzenernhr Bodenkd 152:135141
Tanner W, Beevers H (1990) Does transpiration have an essential function in long-distance ion transport in plants? Plant Cell Environ
13:745750
Tanner W, Beevers H (2001) Transpiration, a prerequisite for longdistance transport of minerals in plants? Proc Natl Acad Sci USA
98:94439447
Tinker PB, Nye PH (2000) Solute movement in the rhizosphere.
Oxford University Press, New York
von Caemmerer S, Baker N (2007) The biology of transpiration: from
guard cells to globe. Plant Physiol 143:3
Wallace W (1986) Distribution of nitrate assimilation between the root
and shoot of legumes and a comparison with wheat. Physiol Plant
66:630636
Wardlaw IF (1990) The control of carbon partitioning in plants. New
Phytol 116:341381
Warren CR (2008) Stand aside stomata, another actor deserves centre
stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:14751487
Warren CR, Adams MA (2006) Internal conductance does not scale
with photosynthetic capacity: implications for carbon isotope
discrimination and the economics of water and nitrogen use in
photosynthesis. Plant Cell Environ 29:192201
Wilkinson S, Corlett JE, Oger L, Davies WJ (1998) EVects of xylem
pH on transpiration from wild-type and Xacca tomato leaves: a
vital role for abscisic acid in preventing excessive water loss even
from well-watered plants. Plant Physiol 117:703709
Wilkinson S, Bacon MAZ, Davies WJ (2007) Nitrate signalling to stomata and growing leaves: interactions with soil drying, ABA, and
xylem sap pH in maize. J Exp Bot 58:17051716
Woodward J (1699) Some thoughts and experiments concerning vegetation. Philos Trans R Soc Lond 21:193227
Wright IJ, Reich PB, Westoby M (2003) Least-cost input mixtures of
water and nitrogen for photosynthesis. Am Nat 161:98111

123

24
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F,
Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M,
Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont
BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets
, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI,

123

Oecologia (2009) 161:1524

Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R
(2004) The world-wide leaf economics spectrum. Nature
428:821827
Zhang HM, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:5159