Journal of Experimental Botany, Vol. 51, No. 342, pp. 61-70,
January 2000
© 2000 Oxford University Press
Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress
1 Department of Plant Sciences, IACR—Long Ashton Research Station, University of Bristol, Bristol BS41 9AF, UK
2 Nutricion y Fisiologia Vegetal, CEBAS-CSIC, PO Box 4195, 30080 Murcia, Spain
3 Lehrstuhl Pflanzenökologie, Universität Bayreuth, D-95440 Bayreuth, Germany
Received 19 January 1998; Accepted 16 July 1999
 |
Abstract |
|---|
 Top Abstract IntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
It has been shown that N-, P- and S-deficiencies result in major reductions of root hydraulic conductivity (Lpr) which may lead to lowered stomatal conductance, but the relationship between the two conductance changes is not understood. In a variety of species, Lpr decreases in the early stages of
, H2
and 
deprivation. These effects can be reversed in 4–24 h after the deficient nutrient is re-supplied. Diurnal fluctuations of root Lpr have also been found in some species, and an example of this is given for Lotus japonicus. In nutrient-sufficient wheat plants, root Lpr is extremely sensitive to brief treatments with HgCl2; these effects are completely reversible when Hg is removed. The low values of Lpr in N- or P-deprived roots of wheat are not affected by Hg treatments. The properties of plasma membrane (PM) vesicles from wheat roots are also affected by -deprivation of the intact plants. The osmotic permeability of vesicles from N-deprived roots is much lower than that of roots adequately supplied with , and is insensitive to Hg treatment. In roots of L. japonicus, gene transcripts are found which have a strong homology to those encoding the PIP1 and PIP2 aquaporins of Arabidopsis. There is a very marked diurnal cycle in the abundance of mRNAs of aquaporin gene homologues in roots of L. japonicus. The maxima and minima appear to anticipate the diurnal fluctuations in Lpr by 2–4 h. The temporal similarity between the cycles of the abundance of the mRNAs and root Lpr is most striking. The aquaporin encoded by AtPIP1 is known to have its water permeation blocked by Hg binding. The lack of Hg-sensitivity in roots and PMs from N-deprived roots provides circumstantial evidence that lowered root Lpr may be due to a decrease in either the activity of water channels or their density in the PM. It is concluded that roots are capable, by means completely unknown, of monitoring the nutrient content of the solution in the root apoplasm and of initiating responses that anticipate by hours or days any metabolic disturbances caused by nutrient deficiencies. It is the incoming nutrient supply that is registered as deficient, not the plant’s nutrient status. At some point, close to the initiation of these responses, changes in water channel activity may be involved, but the manner in which monitoring of nutrient stress is transduced into an hydraulic response is also unknown. Key words: lotus japonicus, hydraulic conductivity, diurnal cycle, aquaporin, root, plasma membrane.
|
Introduction |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
A plant can have its transpiration, stomatal conductance (Gs) and root hydraulic conductivity (Lpr) influenced strongly by its supply of certain mineral nutrients. This much has been recognized for many years ( Desai, 1937
), but while it is agreed that these responses occur without there being any gross perturbation in leaf water status, they are not completely explained. When they are deficient in the growth medium, three plant nutrients, nitrate, phosphate and sulphate, which are transported, metabolized and utilized in different ways, all produce similar effects on Gs and Lpr. It seems improbable that these effects are caused by completely separate sequences of events. Thus, one should not, for instance, expect to explain stomatal closure in P-deficent plants solely by reference to P-metabolism or tissue distribution of P; when there is no P-limitation, Gs is equally sensitive to N-deficiency and S-deficiency. Similarly, root Lpr is strongly responsive to the N supply, but it may also be affected by P and S deficiency ( Radin and Eidenbock, 1984; Karmoker et al., 1991). One might ask, therefore, whether stomatal closure and diminished Lpr are central objectives of the nutrient-stress response, elicited by some common sequence of events. The idea that there may be a centralized stress response system had already been advanced (Chapin, 1990).
It is important to consider the timing of events and the order in which they unfold. In Fig. 1 the sequence has been divided arbitrarily into two branches: the first embraces nutrient-specific responses of transport systems, while the second, more general branch, is concerned with hydraulic and morphological events. It must be stressed that this scheme of things, particularly in the general branch, is speculative. The response of plants to potassium deficiency seems to be restricted to the specific branch. As with other nutrient deficiencies, K-deprivation de-represses K transport systems in roots, appearing to make the root a more avid absorber of K from dilute solutions. But, unlike N, P or S deficiency, K does not appear to influence the events in the general branch. In itself, this is a most interesting issue but not one which can be treated in this short paper.
|
In this paper the hypothesis is advanced that anion fluxes (in which energized transport dominates the overall process) are linked with the hydraulic conductivity (Lp) of root plasma membranes (PM), possibly through the activity of water channels. The essence of this idea is that nutritional information is transduced into an hydraulic response.
|
Nutrient deficiencies and water relations of crop plants |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
There were a number of early reports that certain nutrient deficiencies resulted in partial or complete stomatal closure in plants adequately supplied with water ( Desai, 1937
; Wallace and Frohlich, 1965). In more recent times, the work of John Radin and his colleagues has given the clearest insights into the relationships between N and P nutrition, stomatal conductance and leaf expansion. Work with cotton plants, grown in a controlled environment, revealed that both N- and P-deficient conditions restricted leaf expansion, reduced transpiration and decreased the hydraulic conductivity of the plants, without there being any effect on leaf water potential ( Radin and Ackerson, 1981; Radin and Eidenbock, 1984). With P-deficient plants it was established that the root was the site of diminished hydraulic conductance and that this could be detected well in advance of measurable effects on leaf expansion ( Radin and Eidenbock, 1984), but that the effect on Lpr diminished if the temperature of the roots was increased to values >30 °C ( Radin, 1990). A cell pressure probe, inserted into cortical cells of cotton roots, showed the Lp of the PM was smaller, than in nutrient-sufficient controls, by approximately 60% and 85% in P- and N-stressed plants, respectively. The effects could be picked up within 1 d of N-deprivation ( Radin and Matthews, 1989).
N-deficiency in barley and tomato plants lowered Lpr in advance of effects on Gs and photosynthesis (Chapin et al., 1988). In barley, it was found that S-deprivation diminished root Lpr progressively over 4 d to a value <20% of S-replete controls ( Karmoker et al., 1991); these effects preceded reductions in transpiration and net asimilation rate ( Gilbert et al., 1997). In wheat plants, effects on root Lpr, caused by N- and P-deprivation, were quickly reversed when nutrient supplies were resumed (Carvajal et al., 1996). Rapid reversibility of effects on Lpr have been reported in Zea mays when N-starved roots were supplied with either or 
; the effect being dependent on reduction ( Barthes et al., 1996).
In summary it can be said that depriving plants of adequate supplies of the three major nutrient anions results in a prompt diminution of cell and root hydraulic conductivity which is fully reversible when the nutrient supply is restored. Effects can be detected before those on photosynthesis, but may be concomitant with the slowing of leaf expansion. The authors are not aware of any report that K-deficiency affects root Lpr.
|
Nutrient deficiencies and root growth |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
It has been observed frequently that plants which are N- or P-limited in their growth allocate a greater proportion of their total assimilated carbon to root growth ( Robinson, 1994
). Not all species respond in this way and examples can be found of closely related ones which behave differently, for example, Plantago spp. ( Lambers et al., 1981a, b) and Agropyron spp. ( Jackson and Caldwell, 1989). The relative expansion of the root system when plants experience scarcity of an essential nutrient conforms to a commonsense notion that this is a ‘sensible’ strategy to maximize resource capture below ground. It has been questioned, however, whether or not this is as sensible as it appears at first, especially in the case of N-deficiency ( Robinson, 1996). Nitrate is free to diffuse towards root surfaces and will do so more rapidly if influx at the root surface is increased. Following this logic there is no ‘need’ to expand the root surface, an increase in absorption rate should increase the rate at which diffuses to the root surface, and yet the effect is very widely seen. When conditions of N-supply are shifted from a sufficient to a sub-sufficient level there is usually a period during which the root:shoot weight ratio increases, but, after some time, it reaches a new steady value (for example, in young plants of Betula pendula, McDonald et al., 1986).
Local sources of N (both as or ) or P, in media which are generally nutrient deficient, elicit local root proliferation ( Drew and Saker, 1975, 1978). The nutrient absorption that occurs in the zone where roots proliferate can compensate, to some extent, for deficiencies in other root zones. Much work of this kind has been reviewed ( Robinson, 1994). Interestingly, neither the root:shoot ratio response nor the localized proliferation of roots is elicited by K-deficiency. It should be noted, however, that S-deprivation in barley, while de-repressing sulphate transporter genes ( Smith et al., 1998) and causing a major diminution of Lpr, had relatively little effect on the root:shoot ratio ( Karmoker et al., 1991). There is, therefore, no invariable linkage between the various effects in the general branch of Fig 1.
|
Root Lpr and transpiration |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
The apparent value of root Lpr has been reported to increase with transpiration rate ( Mees and Weatherley, 1957
; Passioura and Tanner, 1985). This phenomenon has been interpreted in several ways, but all of them fall short of describing, in molecular terms, a resistance which decreases as flow increases. Explanations in terms of additive effects of osmotic and hydrostatic driving forces ( Fiscus, 1975), or of changes in the dominant pathways for the lateral movement of water across the root cylinder ( Steudle, 1994; Steudle and Peterson, 1998) have been advanced as alternatives or have been incorporated into models in which effects of different pathways are compensatory ( Steudle and Peterson, 1998). In these models, however, the role of water transport across root cell membranes remains to be quantified, although there have been attempts in which water relations have been worked out in great detail at the cell and root level ( Zhu and Steudle, 1991; Azaizeh et al., 1992). In these studies, cell Lp appeared to be quite variable. The discovery of aquaporins in tonoplast and plasma membranes (Daniels et al., 1994; Kammerloher et al., 1994) and the demonstration that some of them at least, do function as PM water channels ( Kammerloher et al., 1994; Kaldenhoff et al., 1998; Tyerman et al., 1999) provides an opportunity to see if they play a role in the apparent variability of Lpr.
Both transpiration rate and Lpr have been found to vary diurnally, but a simple cause and effect was seemingly ruled out in a classic experiment ( Parsons and Kramer, 1974) which showed that the diurnal rhythm continued for several cycles after root systems of cotton had been excised; the phases of the rhythm seemed to be set by the onset of light. In some of the experiments summarized below, it is shown that there are also diurnal cycles in the expression of mRNAs which are homologous to those encoding Arabidopsis aquaporins, but that their abundance is not influenced by concurrent transpiration rate.
|
Behaviour of wheat roots during N- and P-deprivation |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
Both N- and P-deprivation decreased the apparent value of Lpr in excised wheat roots (Carvajal et al., 1996
); in these experiments the flow of water was driven by osmotic pressure differences between the xylem sap and the solution in the root apoplasm. The measurements were made, therefore, at low rates of water flow, equivalent to, or less than those normally occurring during the dark period. A marked diurnal fluctuation in the value of root Lpr was found in plants sampled at different times during day and night; the amplitude of the cycle was much reduced by N- or P-deprivation, but remained significant (Table 1). If the roots of wheat plants were divided between solutions containing, or lacking , those in the - half had lower root Lpr than those in the + half (Carvajal et al., 1996).
|
Root Lpr was extremely sensitive to brief exposure to 50 µM HgCl2. The inhibition was removed when roots were rinsed with the mercury scavanging reagent dithiothreitol (Fig. 2
). The value of Lpr in N- and P-deprived roots was unaffected by the Hg treatment; evidently, some Hg-sensitive component had been lost during nutrient deprivation. While it is tempting to suggest that the lack of Hg inhibition corresponds with a lack of PM water channels of the PIP1 type, which have been shown to be Hg-sensitive ( Kammerloher et al., 1994; Kaldenhoff et al., 1998), some caution is necessary. When expressed in Xenopus oocytes, PIP1 type aquaporins were inhibited only when concentrations of HgCl2 in the mM range were used (R Kaldenhoff, personal communication). However, in Chara internode cells, a 50 µM HgCl2 treatment was effective in apparently blocking water channels ( Henzler and Steudle, 1995). Mercury can hardly be thought of as a very specific inhibitor, especially when high concentrations are applied to tissues, but, if Lpr decreased because of a general metabolic blockade by Hg, rather than because of a direct interaction of Hg with water channels, one would expect to see a similar proportional collapse in Lpr in control and nutrient-deprived roots. This did not happen, even though, for example, Hg would be expected to have some effect on membrane potential. There is a report in the literature that water-flow through roots of tomato, driven by an applied external pressure, was severely inhibited by 500 µM HgCl2 ( Maggio and Joly, 1995). Where relatively great rates of water flow are measured, interactions of Hg with ion transport to the xylem may be less important.
|
In an attempt to resolve this question of whether or not there can be a direct interaction between Hg and water conductance, PM was prepared from wheat roots grown for 4 d with or without
in the culture medium, and their rate of shrinkage during exposure to hypertonic solutions was observed. Changes in volume, monitored by changes in light scattering at 500 nm in suspensions of PM vesicles, are very rapid and can be observed only with stopped-flow spectrophotometry. This technique has been explored rigorously by other researchers ( Maurel et al., 1997; Niemietz and Tyerman, 1997). Figure 3a and b show the time-course of vesicle shrinking in PM vesicles from control and N-deprived roots. The initial rate, determined graphically, was much slower in the PM from N-deprived roots. This difference was maintained over a temperature range of 15–30 °C (data not shown). The initial rate of shrinkage was slowed down by approximately 50% by the treatment of control PM with 50 µM HgCl2 for 5 min prior to osmotic challenge. There was no effect on the slower shrinking rate of the PM vesicles from N-deprived roots (Table 2). PM and tonoplast vesicles from wheat roots have been studied ( Niemietz and Tyerman,1997), but, in this case, the water permeability of PM vesicles was not Hg-sensitive; the difference between their results and the results of this study may be related to the nitrate-free medium used to grow their plant material. The cultured tobacco cells used by Maurel et al. ( Maurel et al., 1997) to prepare membranes were exposed to high concentrations of nitrate in Murashige and Skoog medium, but were obviously habituated to conditions where water fluxes across the PM would have been low; these too showed little or no response to Hg, suggesting the absence of sensitive water channels.
|
|
|
Studies of root Lpr in Lotus japonicus |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
Lotus japonicus can be used to study both diurnal and nutritional responses of Lpr. A well-marked diurnal cycle of Lpr can be observed when root systems are enclosed in pressure chambers and water driven through them at rates comparable to those found in transpiring plants (T Henzler, DT Cooke, DT Clarkson, unpublished results). The same cycle was found in plants transpiring in ambient conditions and where transpiration was greatly reduced (Table 3
). The effect of withdrawing nitrate from the culture medium (Fig. 4) was to decrease root Lpr by 80% over 4 d; there was a recovery in when was resupplied. The initial delay in the response is probably explained by the fact that the roots had been supplied with 5 mM and the root tissues contained more than 60 mM . For some time, the vacuolar store of would have supported both export to the shoot and efflux into the root apoplasm ( Van der Leij et al., 1998). After 24 h the vacuolar in Lotus roots would have been largely dissipated (A Massonneau, unpublished data).
|
|
When mRNA from L. japonicus roots was probed with cDNAs to AtPIP1 and AtPIP2, strongly hybridizing transcripts were found (Clarkson et al., 1996
; RN Waterhouse and AJ Smyth, unpublished results) whose abundance varied diurnally (Fig. 5). Transcript abundances increased to a maximum in the first part of the photoperiod, then declined to a minimum value at the beginning of darkness. The transcript abundance increased at the end of the night, thus anticipating dawn and the daytime increase in transpiration. Figure 5 also shows Northern blots of transcripts of the root-expressed cytosolic form of L. japonicus glutamine synthetase and a homologue of the barley high affinity nitrate transporter HvNRT2 ( Trueman et al., 1996); these show little diurnal cycling. As might be expected from the results in Table 3, current rates of transpiration had no effect on the abundance of the PIP1-homologous mRNA (Fig. 6).
|
|
Nitrate-deprivation decreased strongly the abundance of PIP1-homologous mRNAs in half of the experiments, but had weaker effects in others. At present there is no explanation for this variable response which contrasts so markedly with the reproducible diurnal pattern.
Western blots of proteins isolated from the PM of L. japonicus reveal a single highly adundant band which cross reacts with anti-AtPIP1a antiserum. The antibody was raised against 42 N-terminal amino acid residues which distinguish PIP1-type aquaporins from others ( Clarkson et al., 1996);. The apparent MW of this band, 27–29 kDa, is characteristic of aquaporins.
|
Water channels and variable root Lpr |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
In Lotus japonicus there is strong evidence that the PM contains one or more aquaporins which are homologous to the PIP1 and PIP2 types of A. thaliana. It has been proved that AtPIP1b in that species s an Hg-sensitive water channel; if the expression of the PIP1b gene is down-regulated by antisense in A. thaliana, the water permeability of the PM is lowered to between 20–30% of that in wild type roots. Water permeability was inhibited by >90% by treatment of protoplast membranes with HgCl2 ( Kaldenhoff et al., 1998
). The evidence from wheat roots (Carvajal et al., 1996) and from Chara ( Henzler and Steudle, 1995) also indicates that root Lpr and Lp of the PM, respectively, are extremely sensitive to brief Hg exposures. However, sensitivity of water permeation to HgCl2 may not be a reliable guide to the involvement of aquaporins in water fluxes. There is at least one major class of aquaporin which lacks mercury sensitivity (for example, RD28, Daniels et al., 1994). Clearly, in a membrane where such an aquaporin is the dominant water channel, there would be no Hg-sensitivity. It was found that water permeability of PM vesicles prepared from cultured tobacco cells was not Hg sensitive ( Maurel et al., 1997). Moreover, these authors observed that the temperature dependence and activation energy of water transport in these preparations were not significantly different from values to be expected by simple diffusion of water across the lipid bilayer. From this they concluded that no case could be made for water channels having an important role in PM water permeability in their preparations. In A. thaliana, it has been pointed out that if there are Hg-insensitive aquaporins present in root PMs from -fed plants, they, and the diffusive permeability of the PM to water account for no more than 15% of the total permeability ( Kaldenhoff et al., 1998). It has also been shown that Hg has no effect on the diffusive water permeation of tobacco PM ( Maurel et al., 1997). This study’s results with -grown roots of wheat are more in agreement with those of Kaldenhoff et al. ( Kaldenhoff et al., 1998). The loss of Hg-sensitivity of root Lpr after N- or P-deprivation suggests that either the activity or the density of water channels in the root cell PMs is diminished during nutrient deficiency. This idea has also been advanced to explain changes in the hydraulic properties of roots of Zea mays with various levels and types of N nutrition ( Barthes et al., 1995, 1996; Hoarau et al., 1996).
It should be borne in mind that changes in the contribution of the apoplasmic pathway to the overall water conduction by the root may contribute to the observed fluctuation in root Lpr ( Zimmermann and Steudle, 1998). In particular, water flowing through apoplasmic leaks in younger parts of the root, or at the points of lateral root insertion, may increase root Lpr at higher flow rates. Nevertheless, it is suggested that the opening and closing of water channels will modify the relative rates of flow in the cell-to-cell and apoplasmic pathways ( Zimmermann and Steudle, 1998).
During P-deficiency observations on cytosolic Pi levels by 31P-NMR show that it is strongly buffered by vacuolar reserves ( Lee and Ratcliffe, 1993). Similar homeostasis in cytosolic has been observed in the first few days of N-deprivation in barley ( van der Leij et al., 1998). If there is little change in the concentration of these anions on the cytosolic side of the PM during the early stage of nutrient-deprivation, it is possible that the responses seen are due to changes in the composition of the solution in the apoplasm, i.e. at the extracellular face of the PM. It is by no means clear how such a response might be brought about; there might be some regulatory interaction, perhaps by phosphorylation ( Johansson et al., 1996), between ion movement through the anion transporters and either the activity or turnover of water channel proteins. In short, it may be that ion currents through these anion transporters is the message to which the system responds. Against this idea must be set the observations of Barthes et al. ( Barthes et al., 1996) that the increased Lpr in roots of Z. mays, seen when they are moved from an N-deficient medium to one containing nitrate, depended on nitrate reduction. One must conclude that the signal, in this instance, came from the cytoplasm where nitrate reduction occurs. A signal derived from nitrate or ammonium assimilation cannot explain, however, the strikingly similar effects of P-, S-
and N-deficiencies on Lpr. Perhaps there are, indeed, parallel pathways leading to the effect on Lpr.
|
Downstream effects of changing Lpr |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
Much evidence is against the view that the stress-induced changes in Lpr grossly or permanently perturb plant water relations. Some of the earliest observations showed that stomata closed without there being any reduction in leaf water status (Chapin et al., 1988
). These results call to mind similar effects on stomata in plants where soil begins to dry; where some form of chemical signalling between roots and leaves has been advanced to explain these effects (Davies and Zhang, 1991;Davies et al., 1994; Passioura, 1988; Schurr and Schultze, 1996). Both abscisic acid (Davies and Zhang, 1991) and unknown components of the xylem sap ( Munns and King, 1988; Munns et al., 1993) have been shown to increase in concentration in the transpiration stream of plants with roots in drying soil. The stomata close without there being a perturbation in leaf water potential. The signal for the increased release of stomata-closing substances from the root may be some change in root water potential or root turgor pressure. In the case of N-deficiency there are changes in the flux of two plant growth regulators from roots to leaves, namely abscisic acid, the concentration of which has been reported to go up in some species ( Krauss, 1978;Clarkson and Touraine, 1994), but not in others ( Peuke et al., 1994) and cytokinin, the concentration of which goes down ( Beck and Wagner, 1994). At present there is no basis upon which these changes in flux might be related to decreased Lpr. It is well known, however, that ABA can increase Lpr if applied exogenously to roots ( Hose and Hartung, 1999).
As mentioned earlier, another frequent response to N- and P-deprivation is increased allocation of dry matter to root growth. This response is also seen during drought stress in Lolium perenne ( Jupp and Newman, 1987), Zea mays ( Schmidhalter et al., 1998), Glycine max ( Huck et al., 1983) among many other species of economic interest. In experiments with A. thaliana, lines carrying antisense constructs to PIP1b were found to have their root systems, both relatively and absolutely enlarged ( Kaldenhoff et al., 1998); there was no evidence of alteration in transpiration rate or shoot growth. The Lpr of the roots of Arabidopsis, and of the protoplasts derived from them, was diminished to about the same extent as found for N- and P-deprivation in wheat roots. In all lines, this decline was associated with more extensive root systems; in some cases five times as extensive as those of wild-type plants without there having been a major reduction in shoot size (R Kaldenhoff, personal communication). It seems likely that the net assimilation rate of the leaves was increased in the antisensed lines to cope with the additional demands created by the growth and maintenance of such a large root system. It has been argued that the carbon costs of extensive root systems are negligible when set against nutritional gains or increased competitiveness ( Thomas, 1994).
The intrinsic size of the root system of wheat genotypes may be genetically linked to drought and salinity tolerance; this was indicated by QTL analysis of a mapping population of doubled haploid lines arising for a cross of cv. Chinese springxSQ1 (Chinoy et al., 1998). Lines tolerant of these stresses may also have more efficient nitrogen acquisition than those with relatively smaller, or shorter root systems (DT Clarkson and S Quarrie, unpublished results). The enlargement of the root system in 24 independently transformed lines of A. thaliana carrying antisense to PIP1b suggests a relatively simple manipulation for increasing stress tolerance if other species of economic interest are found to behave similarly. The Arabidopsis plants in earlier experiments ( Kaldenhoff et al., 1998) behaved as if they had detected hydric or nutrient stress without developing any adverse symptoms.
|
Acknowledgments |
|---|
We gratefully acknowledge the collaboration of our colleagues Toni Schaeffner, Burkhardt Stumpf and Ian Prosser and most helpful discussions with Ralf Kaldenhoff. We are especially grateful to Tony Clark of the Biochemistry Department, University of Bristol for his expertise in stopped-flow spectrophotometry. The research was supported by grants from the Biotechnology and Biological Sciences Research Council (BBSRC), Plant Molecular Biology II Programme, the European Union, Biotechnology Framework IV, and the British Council/DAAD. Long Ashton Research Station receives grant-aided support from the BBSRC.
|
Notes |
|---|
4 To whom correspondence should be addressed. Fax: +44 1275 39421. E-mail: david.clarkson@bbsrc.ac.uk
|
References |
|---|
|
TopAbstractIntroductionNutrient deficiencies and water...Nutrient deficiencies and root...Root Lpr and transpirationBehaviour of wheat roots...Studies of root Lpr...Water channels and variable...Downstream effects of changing...References |
|---|
Azaizeh H, Gunse B, Steudle E. 1992. Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings. Plant Physiology 99, 886–894.
Barthes L, Bousser A, Hoarau J, Deléens E. 1995. Reassessment of the relationship between nitrogen supply and xylem exudation in detopped maize seedlings. Plant Physiology and Biochemistry 33, 173–183.
Barthes L, Deléens E, Bousser A, Hoarau J, Prioul J.-L. 1996. Xylem exudation is related to nitrate assimilation pathway in detopped maize seedlings: use of nitrate reductase and glutamine synthetase inhibitors as tools. Journal of Experimental Botany 47, 485–495.
Beck E, Wagner BM. 1994. Quantification of the daily cytokinin transport from root to the shoot of Urtica dioica L. Botanica Acta 107, 342–348.[Web of Science]
Carvajal M, Cooke DT, Clarkson DT. 1996. Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199, 372–381.[Web of Science]
Chapin FS. 1990. Effects of nutrient deficiency on plant growth: evidence for a centralized stress-response system. In: Davies WJ, Jeffcoat B, eds. Importance of root to shoot communication in the response to environmental stress, Monograph 21. Bristol: British Society for Plant Growth Regulation, 135–148
Chapin FS, 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, 352–366.
Chinoy C, Farmer P, Saker L, Steed A, Clarkson DT, Quarrie, SA. 1998. QTL analysis of N uptake and utilization in spring wheat. Journal of Experimental Botany 49 (supplement), 76.
Clarkson DT, Touraine B. 1994. Morphological response of plants to nitrate-deprivation: a role for abscisic acid? In: Roy J, Garnier E, eds. A whole plant perspective on carbon-nitrogen interactions. The Hague: SPB Academic Publishing, 187–196.
Clarkson DT. Waterhouse RN. Schäffner AR, Carvajal M, Cooke DT. 1996. Water channels and root hydraulic conductivity. Plant Physiology and Biochemistry, Special Issue Abstracts of FESPP Congress, Florence, 162–163.
Daniels MJ, Mirkov TE, Chrispeels M. 1994. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homologue of the tonoplast water channel protein TIP. Plant Physiology 106, 1325–1333.[Abstract]
Davies WJ, Tardieu F Trejo CL. 1994 How do chemical signals work in plants that grow in drying soil? Plant Physiology 104, 309–314.[Web of Science][Medline]
Davies WJ, Zhang J. 1991. Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 42, 55–76.[Web of Science]
Desai MC. 1937. Effect of certain nutrient deficiencies on stomatal behaviour. Plant Physiology 12, 253–283.
Drew MC, Saker LR. 1975. Nutrient supply and the growth of the seminal root system in barley. II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. Journal of Experimental Botany 26, 79–90.
Drew MC, Saker LR. 1978. Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake, in response to a localized supply of phosphate. Journal of Experimental Botany 29, 435–451.
Fiscus EL. 1975. The interaction between osmotic-and pressure-induced water flow in plant roots. Plant Physiology 80, 752–759.
Gilbert SM, Clarkson DT, Cambridge M, Lambers H, Hawkesford MJ. 1997. SO2-4 deprivation has an early effect on the content of ribulose-1,5-bisphosphate carboxylase/oxygenase in young leaves of wheat. Plant Physiology 115, 1231–1239.[Abstract]
Henzler T, Steudle E. 1995. Reversible closing of water channels in Chara internodes provided evidence for a composite transport model of the plasma membrane. Journal of Experimental Botany 46, 199–209
Hoarau J, Barthes L, Bousser A, Deléens E, Prioul JL. 1996. Effect of nitrate on water transfer across roots of nitrogen pre-starved maize seedlings. Planta 200, 405–415.
Hose E, Hartung W. 1999. The efect of abscisic acid on water transport through maize roots. Journal of Experimental Botany 50 (supplement), 40.
Huck MG, Ishimara K, Peterson CM, Ushijima T. 1983. Soybean adaptation to water stress at selected stages of growth. Plant Physiology 73, 422–427.
Jackson RB, Caldwell MM. 1989. The timing and degree of root proliferation in fertile-soil microsites for three cold-desert perennials. Oecologia 81, 149–153.
Johansson I, Larsson C, Ek B, Kjellbom P. 1996. The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca and apoplastic water potential. The Plant Cell 8, 1181–1191.[Abstract]
Jupp AP, Newman EI. 1987. Morphological and anatomical effects of severe drought on the roots of Lolium perenne L. New Phytologist 105, 393–402.
Kaldenhoff R, Grote K, Zhu J-J, Zimmermann U. 1998. Significance of plasmalemma aquaporins for water transport in Arabidopsis thaliana. The Plant Journal 14, 121–128.[Web of Science][Medline]
Kammerloher W, Fischer U, Piechottka GP, Schaeffner AR. 1994. Water channels in plant plasma membrane cloned by immunoselection from a mamalian expression system. The Plant Journal 6, 187–199.[Web of Science][Medline]
Karmoker JL, Clarkson DT, Saker LR, Rooney JM, Purves JV. 1991. Sulphate deprivation depresses the transport of nitrogen to the xylem and hydraulic conductivity of barley (Hordeum vulgare L.) roots. Planta 185, 269–278.
Krauss A. 1978. Tuberization and abscisic acid content of Solanum tuberosum as affected by nitrogen nutrition. Potato Research 21, 183–193.
Lambers H, Posthumus F, Stulen I, Lanting L, Van de Dijk SJ, Hofstra R. 1981a. Energy metabolism of Plantago lanceolata as dependent on the supply of mineral nutrients. Physiologia Plantarum 51, 85–92.
Lambers H, Posthumus F, Stulen I, Lanting L, van de Dijk SJ, Hofstra R. 1981b. Energy metabolism of Plantago major major as dependent on the supply of nutrients. Physiologia Plantarum 51, 245–252.
Larsson C, Widell S, Kjellbom P. 1987. Purification of high purity plasma membranes. Methods in Enzymology 148, 558–568.
Lee RB, Ratcliffe RG. 1983. Subcellular distribution of inorganic phosphate, and levels of nucleoside triphosphate, in mature maize roots at low external phosphate concentrations: measurements with 31P-NMR. Journal of Experimental Botany 44, 587–597.
McDonald AJS, Lohammar T, Ericsson A. 1986. Growth response to step decrease in nutrient availability in small birch (Betula pendula Roth). Plant, Cell and Environment 9, 427–432.
Maggio A, Joly RJ. 1995. Effects of mercuric chloride on the hydraulic conductivity of tomato root systems. Evidence for a channel-mediated pathway. Plant Physiology 109, 331–335.[Abstract]
Maurel C, Tacnet F, Güclü J, Guern J, Ripoche P. 1997. Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proceedings of The National Academy of Sciences, USA 94, 7103–7108.
Mees GC, Weatherley PE. 1957. The mechanism of water absorption by roots. Proceedings of The Royal Society of London, Series B 147, 367–380.
Munns R, King RW. 1988. Abscisic acid is not the only stomatal inhibitor in the transpiration stream of wheat plants. Plant Physiology 88, 703–708.
Munns R, Passioura JB, Milborrow BV, James AR, Close TJ. 1993. Stored xylem sap from wheat and barley in drying soil contains a transpiration inhibitor with a large molecular size. Plant, Cell and Environment 16, 867–872.
Niemietz CA, Tyerman SD. 1997. Characterization of water channels in wheat root membrane vesicles. Plant Physiology 115, 561–567.[Abstract]
Parsons LR, Kramer PJ. 1974. Diurnal cycling in the root resistence to water flow. Plant Physiology 30, 19–23.
Passioura JB. 1988. Root signals control leaf expansion in wheat seedlings growing in drying soil. Australian Journal of Plant Physiology 15, 687–693.
Passioura JB, Tanner CB. 1985. Oscillations in apparent hydraulic conductance in cotton roots. Australian Journal of Plant Physiology 12, 455–461.[Web of Science]
Peuke AD, Jeschke WD, Hartung W. 1994. The uptake and flow of C, N and ions between roots and shoots in Ricinus communis. II. The flows of cations, chloride and abscisic acid. New Phytologist 140, 625–636.
Radin JW. 1990. Responses of transpiration and hydraulic conductance to root temperature in nitrogen- and phosphorus-deficient cotton seedlings. Plant Physiology 92, 855–857.
Radin JW, Ackerson RC. 1981. Water relations of cotton plants under nitrogen deficiency. III. Stomatal conductance, photosynthesis and abscisic acid accumulation during drought. Plant Physiology 67, 115–119.
Radin JW, Eidenbock MP. 1984. Hydraulic conductance as a factor limiting leaf expansion in phosphorus-deficient cotton plants. Plant Physiology 75, 372–377.
Radin JW, Matthews MA. 1989. Water transport properties of cortical cells in roots of nitrogen- and phosphorus-deficient cotton seedlings. Plant Physiology 89, 264–268.
Robinson D. 1994. Tansley Review No 73. The response of plants to non-uniform supplies of nutrients. New Phytologist 127, 635–674.[Web of Science]
Robinson D. 1996. Variation, co-ordination and compensation in root systems in relation to soil variability. In: Anderson HM, Barlow PW, Clarkson DT, Jackson MB, Shewry PR, eds. Plant roots–from cell to systems. Dordrecht: Kluwer, 57–66.
Schmidhalter U, Evéquoz M, Camp K-H, Studer C. 1998. Sequence of drought response in maize seedlings in drying soil. Physiologia Plantarum 104, 159–168.
Schurr U, Schultze E-D. 1996. Effects of drought on nutrient and ABA transport in Ricinus communis. Plant, Cell and Environment 19, 665–674.
Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Vanden Berg PJ, Belcher A, Warrilow AGS. 1998. Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter. The Plant Journal 12, 875–884.
Steudle E. 1994. Water transport across roots. Plant and Soil 167, 79–90.
Steudle E, Peterson CA. 1998. How does water get through roots? Journal of Experimental Botany 49, 775–788.
Thomas H. 1994. Resource rejection by higher plants. In Montieth JL, Scott RK, Unsworth, MH, eds. Resource capture by crops. Nottingham: University of Nottingham Press, 375–385.
Trueman LJ, Richardson A, Forde BG. 1996. Molecular cloning of higher plant homologues of the high affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene 175, 223–231.[Web of Science][Medline]
Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JAC. 1999. Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. Journal of Experimental Botany 50 Special Issue, 1055–1071.[Abstract]
Van der Leij M, Smith SJ, Miller AJ. 1998. Remobilisation of vacuolar stored nitrate in barley root cells. Planta 205, 64–72.[Web of Science]
Wallace A, Frolich A. 1965. Phosphorus deficiency symptoms in tobacco versus transpirational water loss. Nature 208, 123–124.
Waterhouse RN, Smyth AJ, Massonneau A, Prosser IM, Clarkson DT. 1996. Molecular characterisation of asparagine synthetase from Lotus japonicus. Dynamics of asparagine synthesis in N-sufficient conditions. Plant Molecular Biology 30, 883–897.[Web of Science][Medline]
Zhu QL, Steudle E. 1991. Water transport across maize roots. Simultaneous measurements of flows at the cell and root level by double pressure probe techniques. Plant Physiology 95, 305–315.
Zimmermann HM, Steudle E. 1998. Apoplastic transport across young maize roots: effect of the exodermis Planta 206, 7–19.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  Y. Li, Y. Gao, X. Xu, Q. Shen, and S. Guo Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration J. Exp. Bot., May 1, 2009; 60(8): 2351 - 2360. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Bramley, N. C. Turner, D. W. Turner, and S. D. Tyerman Roles of Morphology, Anatomy, and Aquaporins in Determining Contrasting Hydraulic Behavior of Roots Plant Physiology, May 1, 2009; 150(1): 348 - 364. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Gorska, Q. Ye, N. M. Holbrook, and M. A. Zwieniecki Nitrate Control of Root Hydraulic Properties in Plants: Translating Local Information to Whole Plant Response Plant Physiology, October 1, 2008; 148(2): 1159 - 1167. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Levin, J. H. Lemcoff, S. Cohen, and Y. Kapulnik Low air humidity increases leaf-specific hydraulic conductance of Arabidopsis thaliana (L.) Heynh (Brassicaceae) J. Exp. Bot., October 10, 2007; (2007) erm220v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Kanai, K. Ohkura, J. J. Adu-Gyamfi, P. K. Mohapatra, N. T. Nguyen, H. Saneoka, and K. Fujita Depression of sink activity precedes the inhibition of biomass production in tomato plants subjected to potassium deficiency stress J. Exp. Bot., August 1, 2007; 58(11): 2917 - 2928. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Gloser, M. A. Zwieniecki, C. M. Orians, and N. M. Holbrook Dynamic changes in root hydraulic properties in response to nitrate availability J. Exp. Bot., July 1, 2007; 58(10): 2409 - 2415. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. NAIDOO Factors Contributing to Dwarfing in the Mangrove Avicennia marina Ann. Bot., June 1, 2006; 97(6): 1095 - 1101. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Keller Deficit Irrigation and Vine Mineral Nutrition Am. J. Enol. Vitic., September 1, 2005; 56(3): 267 - 283. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Schraut, H. Heilmeier, and W. Hartung Radial transport of water and abscisic acid (ABA) in roots of Zea mays under conditions of nutrient deficiency J. Exp. Bot., March 1, 2005; 56(413): 879 - 886. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Loque, U. Ludewig, L. Yuan, and N. von Wiren Tonoplast Intrinsic Proteins AtTIP2;1 and AtTIP2;3 Facilitate NH3 Transport into the Vacuole Plant Physiology, February 1, 2005; 137(2): 671 - 680. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Fujita, M. Okada, K. Lei, J. Ito, K. Ohkura, J. J. Adu-Gyamfi, and P. K. Mohapatra Effect of P-deficiency on photoassimilate partitioning and rhythmic changes in fruit and stem diameter of tomato (Lycopersicon esculentum) during fruit growth J. Exp. Bot., November 1, 2003; 54(392): 2519 - 2528. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Loudet, S. Chaillou, A. Krapp, and F. Daniel-Vedele Quantitative Trait Loci Analysis of Water and Anion Contents in Interaction With Nitrogen Availability in Arabidopsis thaliana Genetics, February 1, 2003; 163(2): 711 - 722. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. JAVOT and C. MAUREL The Role of Aquaporins in Root Water Uptake Ann. Bot., September 1, 2002; 90(3): 301 - 313. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. FRICKE Biophysical Limitation of Cell Elongation in Cereal Leaves Ann. Bot., August 1, 2002; 90(2): 157 - 167. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. P. Comstock Hydraulic and chemical signalling in the control of stomatal conductance and transpiration J. Exp. Bot., February 1, 2002; 53(367): 195 - 200. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Kamaluddin and J. J. Zwiazek Metabolic inhibition of root water flow in red-osier dogwood (Cornus stolonifera) seedlings J. Exp. Bot., April 15, 2001; 52(357): 739 - 745. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Tazawa, E. Sutou, and M. Shibasaka Onion Root Water Transport Sensitive to Water Channel and K+ Channel Inhibitors Plant Cell Physiol., January 1, 2001; 42(1): 28 - 36. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Steudle Water uptake by roots: effects of water deficit J. Exp. Bot., September 1, 2000; 51(350): 1531 - 1542. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||