Journal of Experimental Botany, Vol. 52, No. 364, pp. 2199-2206,
November 1, 2001
© 2001 Oxford University Press
Original Papers |
How the roots contribute to the ability of Phaseolus vulgaris L. to cope with chilling-induced water stress
1 Dipartimento di Biologia delle Piante Agrarie, Università degli Studi di Pisa, Viale delle Piagge 23, 56124 Pisa, Italy
2 Dipartimento di Scienze Agronomiche e Gestione del Territorio Agroforestale, Università degli Studi di Firenze, Piazzale delle Cascine 18, 50144 Firenze, Italy
3 Dipartimento di Produzione Vegetale, Università degli Studi di Milano, Via Celoria 2, 20133 Milano, Italy
Received 15 March 2001; Accepted 29 June 2001
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Abstract |
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Intact plants and stem-girdled plants of Phaseolus vulgaris grown hydroponically were exposed to 5 °C for up to 4 d; stem girdling was used to inhibit the phloem transport from the leaves to the roots. After initial water stress, stomatal closure and an amelioration of root water transport properties allowed the plants to rehydrate and regain turgor. Chilling augmented the concentration of abscisic acid (ABA) content in leaves, roots and xylem sap. In intact plants stomatal closure and leaf ABA accumulation were preceded by a slight alkalinization of xylem sap, but they occurred earlier than any increase in xylem ABA concentration could be detected. Stem girdling did not affect the influence of chilling on plant water relations and leaf ABA content, but it reduced slightly the alkalinization of xylem sap and, principally, prevented the massive ABA accumulation in root tissues and the associated transport in the xylem that was observed in non-girdled plants. When the plants were defoliated just prior to chilling or after 10 h at 5 °C, root and xylem sap ABA concentration remained unchanged throughout the whole stress period. When the plants were chilled under conditions preventing the occurrence of leaf water deficit (i.e. at 100% relative humidity), there were no significant variations in endogenous ABA levels. The increase in root hydraulic conductance in chilled plants was a response neither to root ABA accretion, nor to some leaf-borne chemical signal transported downwards in the phloem, nor to low temperature per se, as indicated by the results of the experiments with defoliated or girdled plants and with plants chilled at 100% relative humidity. It was concluded that the root system contributed substantially to the bean's ability to cope with chilling-induced water stress, but not in an ABA-dependent manner.
Key words: Abscisic acid, acclimation, stomata, root hydraulic conductance, xylem sap pH.
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Introduction |
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Low, non-freezing temperatures (chilling) damage crop species of tropical or sub-tropical origin, in particular during early growth; generally, the seedlings of these species cannot survive prolonged exposure to chilling conditions. Nonetheless, some degree of chilling tolerance is exhibited by chilling-sensitive species, as indicated by the results of experiments with hardened plants (Perez de Juan et al., 1997
) or with different genotypes of maize (Capell and Dörffling, 1993) and rice (Lee et al., 1993).
The ability to maintain a favourable water status is an important component of plant tolerance to chilling, as one of the first symptoms of chilling injury is shoot dehydration that is caused by the altered balance between root water uptake and leaf transpiration (Sanders and Markhart, 2001).
Abscisic acid (ABA) may play a crucial role in the adaptation of plants to chilling stress. Exogenous ABA was reported to increase chilling tolerance in sensitive plants (Markhart, 1984; Pardossi et al., 1992, and references cited therein). Moreover, some genotypes of maize (Capell and Dörffling, 1993) and rice (Lee et al., 1993) maintained a favourable water status under chilling conditions by means of rapid stomatal closure, which appeared to be dependent on the ability for fast accumulation of ABA in leaf tissues. In previous work (Vernieri et al., 1991; Pardossi et al., 1992), chilled bean (Phaseolus vulgaris L.) seedlings were able to rehydrate and regain leaf turgor after initial water stress; this recovery was associated with stomatal closure and a concomitant increase in ABA levels in both leaf and root tissues.
While the interactions among leaf ABA, stomatal behaviour and shoot water status in chilled plants have been extensively investigated, less attention has been devoted to investigate the involvement of roots in chilling tolerance (Sanders and Markhart, 2001). In this regard, the role of roots may be 2-fold. Firstly, root-sourced chemical signals, namely increases in ABA concentration and/or pH of the xylem sap, may be transported upwards in the transpiration stream to reduce stomatal conductance and leaf growth, as it has been repeatedly observed in plants subjected to root stress conditions, such as drought (Thompson et al., 1997) and high salinity (Hartung and Davies, 1994). Secondly, increased water and nutrient uptake by the roots can improve leaf water and mineral relations in chilled plants (Sanders and Markhart, 2001).
The paper reports a study undertaken to investigate how the roots contribute to the ability of Phaseolus vulgaris to cope with chilling-induced water stress. In particular, it was verified whether stomatal closure and/or ABA accumulation in the leaves of chilled (5 °C) plants was related to changes in ABA concentration and pH of xylem sap, and whether ABA accumulation in chilled roots was a response to low temperature in the root zone, to altered root water relations or to a chemical signal originating in the stressed leaves and transferred to the roots via the phloem. In other experiments, it was investigated whether the recovery from chilling-induced water stress was associated with an amelioration of root water transport properties, and, in that case, whether it was dependent on root ABA. As the effect of low temperature on root physiology may be influenced by soil moisture, bean plants were grown in water culture in order to investigate the roots’ response to temperature per se.
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Materials and methods |
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Plant material and growing conditions
Bare-rooted seedlings of Phaseolus vulgaris (cv. Borlotto Nano) were grown hydroponically in a growth chamber at 25 °C air temperature and 60–65% relative humidity (RH) with a 12 h photoperiod and a photosynthetically active radiation (PAR) of approximately 200 µmol m-2 s-1 from fluorescent tubes. After emergence in wet expanded clay, seedlings were carefully transferred to 10 dm3 plastic tanks (36 plants per tank) filled with half-strength Hoagland's nutrient solution, which was aerated continuously by means of aquarium stones. The osmotic potential of the culture solution was approximately -0.044 and -0.041 MPa at 25 °C and 5 °C, respectively.
Experimental treatments
Stress treatments were started 12–13 d after sowing, when seedlings had nearly expanded primary leaves and total leaf area, shoot and root dry weight were 80–100 cm2, 0.19–0.22 g and 0.07–0.09 mg per plant, respectively. In these plants, the root system consisted of 15–20 main roots, which were 10–20 cm long and had 25–45 laterals with a length of 0.2–0.8 cm. The senescent cotyledons were removed 2–3 d before the onset of cold treatment.
Three experiments were conducted. In experiment 1, both intact and stem-girdled plants were chilled by transferring them to precooled nutrient solution in a growth chamber at 5 °C under continuous light, in the same RH and PAR conditions of the controls. Stem girdling was used to inhibit the phloem transport from the leaves to the roots. Girdling was achieved by a filament of wire looped around stem about 0.5 cm below the cotyledons and heated by means of a 10 V potential for 20 s. The effectiveness of girdling in blocking the phloem transport was demonstrated by applying tritiated ABA (300000 cpm in PBS buffer, pH 7) to the leaves of both control and stem-girdled plants, and then measuring radioactivity in root tissues after 24 h; radioactivity was detected in the control roots, but not at all in those of girdled plants (data not shown). Defoliated plants were also transferred to 5 °C; plants were defoliated with a razor blade just prior to chilling treatment or after 10 h or 30 h of stress.
On two occasions, experiment 1 was repeated by stressing the plants in the dark in a water-saturated atmosphere, which was achieved by enveloping the hydroponic tank with plastic sheet.
In experiment 2, leaf water relations, root ABA content and transpiration-induced root water uptake (Jv) and hydraulic conductance (Lp) were determined in intact plants and stem-girdled plants grown in potometers at 5 °C as in the first experiment.
In experiment 3, root ABA content and hydrostatic pressure-induced Jv and Lp were determined in intact plants, stem-girdled plants and defoliated plants grown in hydroponic tanks at 5 °C at 100% or 65% RH.
Data collection
Stomatal behaviour was assessed by measuring abaxial leaf diffusion resistance (LDR) with an automatic diffusion porometer (MK, Delta-T Devices, Cambridge, UK). Water potential was determined by psychrometry in leaf (3.0x1.5 cm) and root (about 2 cm long) segments with a fresh weight of approximately 50 mg. Osmotic potential was measured on expressed sap of frozen/thawed samples using a freezing-point depression osmometer; turgor pressure was calculated as the difference between water and osmotic potential. Leaf segments were also used for the measurement of relative water content (RWC). Further details on the determination of water relations were reported previously (Pardossi et al., 1992).
Quantitative analysis of free ABA in aqueous extract of leaf and root tissues as well as in the xylem exudate was performed using a radioimmunoassay (RIA) based on DBPA1 monoclonal antibody, as previously described (Pardossi et al., 1992).
Xylem sap was exuded from root stumps with a Scholander pressure chamber using a pressure of 0.5 MPa. The initial 25–30 mm3 of exudate from each stump was discarded to avoid contamination that could result from squeezing the hypocotyl by hand, when the silicon sleeve was attached to the stump for collecting exuding sap (Else et al., 1994). In preliminary experiments, the saps expressed at various pressures from 0.4–0.6 MPa contained similar concentrations of ABA, thus indicating that the actual fluid existing in the xylem prior to removing the shoot was analysed (Dodd et al., 1996).
Root hydraulic characteristics, expressed on a root dry mass basis, were determined in both entire plants and detached whole root systems, using the same nutrient solution fed to the plants in the growth chamber. In all the experiments great care was taken to avoid root injury that could affect water penetration into the roots.
Transpiration-induced root water uptake (Jv) and hydraulic conductance (Lp) were assessed in whole plants with potometers. Plants were sealed in 50 ml plastic vessels (one plant per vessel) through a rubber bung with a graduated pipette attached; Jv was estimated by weighing the nutrient solution used to refill the graduated pipette to the reference point. At different times during chilling, Jv was monitored for 2–3 h in four or five plants for each treatment; afterwards the water potential of roots and culture solution were determined with thermocouple psychrometer and freezing-point osmometer, respectively. Transpiration-induced Lp was calculated as the ratio between Jv and the water potential gradient between roots and the external solution; root water potential was assumed to be the most realistic representation of xylem tension.
Hydrostatic pressure-induced Jv and Lp were determined in detopped root systems with a temperature-controlled pressure chamber filled with approximately 8 dm3 of the growing nutrient solution; the chamber allowed seven root samples to be processed simultaneously. The root system was sealed inside the vessel taking care that the hypocotyl was not submerged in the solution; the cut stem surface protruded through a rubber stopper inserted through the lid of the vessel. The chamber was pressurized from the bottom with compressed air. Pressure was slowly increased to 0.25 MPa and steady-state Jv was measured sequentially at 0.25, 0.30, 0.35, and 0.40 MPa. At each step change of pressure, the nutrient solution inside the vessel was mixed and aerated for a few minutes by adjusting a pressure release valve at the top of the chamber to release a small amount of air which bubbled through the solution. Typically, not less than 4 h were needed to complete the pressurization sequence. Hydrostatic pressure-induced Lp was determined as the slope of the linear relationship between Jv and pressure; only root samples with a significant (P=0.05) linear Jv–pressure relationship were considered for Lp determination.
Statistics
A completely randomized design was adopted. Each experiment was repeated two to four times with similar results; in each occasion, 72 or 144 plants were stressed. Data from representative runs were reported as mean values (±s.d.) of 4–6 replicates; 1 or 2 plants represented one replicate. The significance of the difference between means was assessed using unpaired t-test.
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Results |
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In non-stressed plants maintained at 25 °C under continuous light, water relations, endogenous ABA levels and xylem sap pH did not change significantly throughout the treatment period; therefore, only values at the beginning of the stress treatment are presented here.
In bean plants maintained at 5 °C (experiment 1) stomata remained open, as indicated by low LDR during the first hours (Fig. 1), and plants suffered severe water stress; leaf RWC, water potential, osmotic potential, and turgor pressure declined rapidly, and plants wilted within a few hours. Later, stomata began to close and after 16–18 h LDR was significantly higher with respect to the values at the beginning of stress treatment (Fig. 1). This resulted in shoot rehydration and leaf turgor recovery, which was almost complete after 48 h at 5 °C (Fig. 1). There was no important osmotic adjustment involved in the recovery of leaf turgor, and no significant effects of chilling on root water relations were observed (Fig. 1).
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Endogenous ABA levels remained unchanged in leaves, roots and xylem exudate of intact plants until 18–24 h of stress, thereafter they rose massively reaching values up to 3–5 times the levels of non-stressed plants (Fig. 2
).
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Girdling the stem below the cotyledons did not modify significantly the influence of chilling on plant water relations (Fig. 1
) and leaf ABA content (Fig. 2), but it prevented the large increase in root and xylem sap ABA concentration observed in intact plants. In girdled plants, only a transient, albeit significant, increase in root ABA content was found after 24 h of chilling (Fig. 2). The possibility that this increase in root ABA was due to ABA import from the stem tissues below the girdling point was ruled out by an experiment in which the same variations in root ABA content during chilling were observed in plants whose stems were girdled just below the cotyledons or close to the collar (data not shown). In another experiment, intact plants and girdled plants were chilled by maintaining them in separate hydroponic tanks, in order to verify whether the differences in root ABA content between the two groups of plants could be accounted for by a different release of the hormone from the roots to the surrounding medium. This was not the case, however. In fact, ABA concentration remained unchanged in the nutrient solution in which stem-girdled plants were immersed (data not shown); on the contrary, it increased progressively in the solution of non-girdled plants, with a kinetic similar to that of root ABA.
During chilling the pH of xylem sap increased progressively in both intact and girdled plants (Fig. 2); this alkalinization was detected before stomata started to close. Stem girdling slightly reduced the rise in xylem pH during chilling (Fig. 2).
When bean plants were defoliated just prior to chilling or after 10 h at 5 °C, the ABA concentration of roots and xylem sap did not change significantly throughout the 50 h stress period (Fig. 3). When plants were defoliated after 30 h at 5 °C, root and xylem sap ABA concentration reached values significantly higher than those measured in plants defoliated at an earlier time, but these levels did not increased further after leaf removal (Fig. 3).
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When chilling treatment was performed in a water-saturated atmosphere, i.e. under conditions preventing the occurrence of leaf water deficit, there were no significant variations in water relations, endogenous ABA levels and xylem sap pH throughout the whole stress period in both intact and stem-girdled plants (data not shown).
All the results of experiment 1 are consistent with previous findings (Vernieri et al., 1991; Pardossi et al., 1992).
In experiment 2, the effect of whole-plant chilling on root water transport properties was investigated in intact plants, girdled plants and defoliated plants maintained at 5 °C. In non-stressed plants Jv, Lp and root water potential were 4.0 to 7.0x10-3 kg kg-1 s-1, 15–26x10-3 kg kg-1 s-1 MPa-1, and -0.30 to -0.35 MPa, respectively; these values did not change considerably throughout the treatment period.
As found in experiment 1, the plants suffered a severe water deficit and RWC declined rapidly upon exposure to chilling temperature (Fig. 4). After 12–16 h of stress, transpiration-induced Jv and Lp increased significantly with respect to the values at the beginning of the stress treatment (Fig. 4); the amelioration in root water transport properties together with stomata closure (data not shown) allowed the the plants to rehydrate and regain turgor. Later, Jv and Lp tended to return to the values detected in the first hours of stress (Fig. 4).
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In experiment 3, hydrostatic pressure-induced Jv and Lp were determined in intact plants maintained at either 65% or 100% RH in darkness, in order to prevent the occurrence of leaf water stress, as well as in plants in which stems were girdled or leaves were removed just prior to chilling. High RH, stem girdling and defoliation prevented the huge ABA accumulation in roots observed in intact plants (Fig. 5
). Lp increased during chilling in both intact and girdled plants, and, after 24 h, it was significantly higher compared to the values at the beginning of stress (Fig. 5); on the contrary, in defoliated plants and in those chilled at 100% RH, Lp tended to decline during chilling.
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Discussion |
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Root–shoot communication
Root–shoot communication has been extensively investigated in plants subjected to drought, salinity or flooding conditions; however, as far as is known, there are few reports on plants exposed to low temperatures (Smith and Dale, 1988
; Fracheboud and Stamp, 1993; Lee et al., 1993; Janowiak and Dörffling, 1994) and the involvement of root and xylem ABA in regulating stomatal resistance, water relations and ABA synthesis in the leaves of chilled plants is not clear.
In experiments with maize genotypes differing in cold tolerance, it was found that stomatal resistance in chilled plants correlated significantly with xylem sap ABA concentration and that chilling resulted in increased pH of xylem sap only in the tolerant genotypes (Janowiak and Dörffling, 1994). Similarly, in rice, it was noted that root and xylem sap ABA concentration increased within a few hours of chilling in a tolerant rice cultivar, but not in a more sensitive genotype (Lee et al., 1993). It has also been reported that low temperatures (2–5 °C) increased xylem ABA directly in tomato plants grown hydroponically (Starck et al., 1998), whereas the rise in root and xylem ABA concentration in maize plants grown in the soil at 10 °C was associated with a reduction of root water potential (Janowiak and Dörffling, 1994). It has also been suggested that the increase in xylem ABA concentration observed in root-chilled (10 °C) bean plants could reflect an import of ABA from the shoot (Smith and Dale, 1988). Other authors reported that leaf-borne ABA transported in the phloem might act as a shoot–root stress signal in plants (Jeschke et al., 1997, and references cited therein).
In bean, chilling caused a strong shoot dehydration in seedlings grown in water culture (experiment 1); nevertheless, the plants were soon able to rehydrate and regain leaf turgor through an increase in both LDR and Lp. Stomatal closure was associated with an increase in endogenous leaf ABA content in both intact and stem-girdled plants.
Low temperatures enhanced ABA levels in roots and the associated transport in the xylem; grouping data of experiments 1 and 2, a significant (r2=0.85) linear relationship was calculated between root and xylem concentration of the hormone. Nevertheless, stem girdling, which inhibited the phloem transport from the leaves and did not modify the influence of chilling on leaf water relations and ABA content, completely prevented the large elevation in root and xylem ABA concentration that occurred in intact plants. Also, in intact plants LDR and leaf ABA started to rise slightly later than xylem pH, but before any increase in xylem sap ABA concentration could be detected. The alkalinization of xylem sap was not dependent on root ABA, as it also occurred in girdled plants, albeit less than in intact plants. Therefore, the conclusion must be that, in chilled bean, stomatal closure and ABA accretion in leaves was not mediated by the elevation of ABA concentration.
This work has provided evidence that large ABA accretion in chilled roots was not accounted for by altered root water relations or by low temperature per se, and that a chemical message, or ABA itself, originating in water-stressed leaves and reaching the roots via the phloem was apparently necessary for ABA to accumulate in roots. First, substantial changes in root water relations of chilled plants were never observed. Second, root ABA accumulation was prevented when the phloem transport from the leaves was interrupted by stem girdling. Third, when plants were chilled after leaves were removed or under conditions preventing leaf water stress, ABA accumulated neither in roots nor in the xylem exudate.
Root hydraulic conductance
In bean plants maintained at 5 °C, the recovery from initial water stress was associated with an increase in Lp that was measured in entire, transpiring plants (experiment 2) as well as in detached root systems under pressure (experiment 3).
An amelioration of root water transport properties during exposure to low temperatures was reported in both chilling-tolerant (rape: Bigot and Boucaud, 1996; spinach: Fennel and Markhart, 1998) and sensitive plants (mung bean: Bagnall et al., 1983; soybean: Markhart et al., 1979). The results obtained so far suggested that ABA might be involved in root acclimation to low temperature. The recovery in Lp in mung bean after 5 d of root chilling was preceded by a rise in endogenous ABA content in both leaf and root tissues (Bagnall et al., 1983). Moreover, in a recent work with two maize inbred lines grown under cool soil conditions (Janowiak and Dörffling, 1998), it was found that root ABA levels in the chilling-tolerant genotype increased to a greater extent than in the sensitive one. Lastly, exogenous ABA increased Lp in chilled plants of sunflower (Ludewig et al., 1988) and soybean (Markhart, 1984).
At variance with these results, the increase in Lp in bean after some hours at 5 °C was not related to ABA accumulation in root tissues, since it also took place in stem-girdled plants, which did not show the huge increase in root ABA level that was exhibited by intact plants. Root ABA content rose transiently in stem-girdled plants, but the increase in Jv and Lp of potometer-grown plants preceded that in root ABA. Moreover, Lp did not change in defoliated plants and in plants stressed under conditions preventing leaf dehydration, in both of which endogenous ABA levels remained unchanged during the chilling treatment. Therefore, the amelioration in Lp in chilled bean was a response neither to root ABA accretion, nor to some leaf-borne chemical signal transported downwards in the phloem, nor to low temperature per se.
Rapid root acclimation to chilling temperatures could be due to a modification in the chemical composition of the membranes that water has to cross (Sanders and Markhart, 2001). Very recently, Markhart and coworkers (Fennel and Markhart, 1998; Sanders and Markhart, 2001) suggested that leaf and/or root acclimation to low temperature could be related to a change in the activity of water channel proteins (aquaporins), which regulate water flux across cell membranes (Chrispeels and Maurel, 1994). According to the model proposed by Steudle and Peterson for water movement across roots (Steudle and Peterson, 1998), optimization of water uptake can be rapidly achieved by switching between apoplastic and cell-to-cell water pathways within the roots as well as by the action of water channels.
Work is in progress to investigate how the water moves through the roots of bean under chilling conditions. The first results of experiments carried out using the aquaporin-blocker HgCl2 (Chrispeels and Maurel, 1994) and the apoplastic tracer Light Green (Else et al., 1995) suggest that, in bean, aquaporins control most of the bulk root water flow at optimal temperature, and that the contribution of aquaporins to water transport declined during chilling (as indicated by the smaller inhibition of water flux by Hg in chilled plants than in non-stressed ones), while that of the apoplast increased (as indicated by the increase of apoplastic tracer concentration in root xylem sap) (A Pardossi, unpublished results). These results are consistent with those reported recently (Li et al., 2000), which found that chilling reduced the expression of aquaporin genes in both leaves and roots of rice. It seems possible, therefore, that the amelioration of root hydraulic properties in chilled bean was related to a change in the pathway of water across the roots.
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Conclusions |
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The results reported here and in previous papers (Vernieri et al., 1991
; Pardossi et al., 1992) indicate that the response to chilling in bean is biphasic. During the first hours of exposure to chilling temperatures, a strong leaf water deficit occurs, thereafter stomatal closure and an amelioration of root water transport properties allow the plants to rehydrate and regain turgor. This hydraulic acclimation is of ecological relevance as it contributes substantially to plant survival in cold environments. Leaf-sourced ABA is likely to be involved in the regulation of stomatal response to chilling, while there is no causal relationship between ABA and root hydraulic acclimation.
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Notes |
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4 To whom correspondence should be addressed. Fax: +39 2 70633243. E-mail: Alberto.Pardossi{at}unimi.it
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References |
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Bagnall K, Wolfe J, King RW. 1983. Chill-induced wilting and hydraulic recovery in mung bean plants. Plant, Cell and Environment 6, 457–464.
Bigot J, Boucaud J. 1996. Short-term response of Brassica rapa plants to low root temperature: effects on nitrate uptake and its translocation to the shoot. Physiologia Plantarum 96, 646–654.
Capell B, Drffling K. 1993. Genotype-specific difference in chilling tolerance of maize in relation to chilling-induced changes in water status and abscisic acid accumulation. Physiologia Plantarum 88, 638–646.
Chrispeels MJ, Maurel C. 1994. Aquaporins: the molecular basis of facilitated movement through living plant cell. Plant Physiology 105, 9–15.[ISI][Medline]
Dodd IC, Stikic R, Davies WJ. 1996. Chemical regulation of gas exchange and growth of plants in drying soil in the field. Journal of Experimental Botany 47, 1475–1490.
Else MA, Davies WJ, Whitfor PN, Hall KC, Jackson MB. 1994. Concentrations of abscisic acid and other solutes in xylem sap from root systems of tomato and castor-oil plants are distorted by wounding and variable sap flow rates. Journal of Experimental Botany 45, 317–323.
Else MA, Hall KC, Arnold GM, Davies WJ, Jackson MB. 1995. Export of abscisic acid, 1-aminocyclopropane-1-carboxylic acid, phosphate and nitrate from roots to shoots of flooded tomato plants. Plant Physiology 107, 377–384.[Abstract]
Fennel A, Markhart AH. 1998. Rapid acclimation of root hydraulic conductivity to low temperature. Journal of Experimental Botany 49, 879–884.
Fracheboud Y, Stamp P. 1993. Cold induced ABA in the xylem sap of maize. In: Wilson D, Thomas H, Pithan K, eds. Crop development for the cool and wet regions of Europe. Brussels: European Community, 141–146.
Hartung W, Davies WJ. 1994. Abscisic acid under drought and salt stress. In: Pessarakli M, eds. Handbook of plant and crop stress. New York: Marcel Dekker Inc., 401–411.
Janowiak F, Dörffling K. 1994. Response of maize seedlings to chilling of roots with special emphasis on root-to-shoot communication. In: Sowinski P, Zagdanska B, Anio A, Pithan K, eds. Crop development for the cool and wet regions of Europe. Brussels: European Community, 213–220.
Janowiak F, Dörffling K. 1998. Changes in the abscisic acid (ABA) content and injuries of radicles of maize seedlings under cool soil conditions. In: Dörffling K, Brettschneider B, Tantau H, Pithan K, eds. Crop adaptation to cool climates. Brussels ECSP-EEC-EAEC, 141–146.
Jeschke DW, Peuke AD, Pate JS, Hartung W. 1997. Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. Journal of Experimental Botany 48, 1737–1747.
Lee TM, Lur H-S, Chu C. 1993. Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings. I. Endogenous abscisic acid levels. Plant, Cell and Environment 16, 481–490.
Li LG, Li SF, Tao Y, Kitagawa Y. 2000. Molecular cloning of a novel water channels from rice: its products expression in Xenopus oocytes and involvement in chilling tolerance. Plant Science 154, 43–51.
Ludewig M, Dörffling K, Seifert H. 1988. Abscisic acid and water transport in sunflowers. Planta 175, 325–333.
Markhart III AH. 1984. Amelioration of chilling-induced water stress by abscisic acid-induced changes in root hydraulic conductance. Plant Physiology 74, 81–83.
Markhart III AH, Fiscus EL, Naylor AW, Kramer PJ. 1979. Effect of temperature on water and ion transport in soybean and broccoli systems. Plant Physiology 64, 83–87.
Pardossi A, Vernieri P, Tognoni F. 1992. Involvement of abscisic acid in regulating water status in Phaseolus vulgaris during chilling. Plant Physiology 100, 1243–1250.
Perez de Juan J, Irigoyen JJ, Sanchez-Diaz M. 1997. Chilling of drought-hardened and non-hardened plants of different chilling-sensitive maize lines: changes in water relations and ABA contents. Plant Science 122, 71–79.
Sanders P, Markhart III AH. 2001. Root system functions during chilling temperatures: injury and acclimation. In: Basra AS, ed. Crop responses and adaptations to temperature stress. New York: The Haworth Press Inc., 77–108.
Smith PG, Dale JE. 1988. The effects of root cooling and excision treatments on the growth of primary leaves of Phaseolus vulgaris L.: rapid and reversible increases in abscisic acid content. New Phytologist 110, 293–300.
Starck Z, Choluj D, Gawronska H. 1998. The effect of drought hardening and chilling on ABA content in xylem sap and ABA-delivery rate from root of tomato plant. Acta Physiologiae Plantarum 20, 41–48.
Steudle E, Peterson CA. 1998. How does water get through roots? Journal of Experimental Botany 49, 775–778.
Thompson DS, Wilkinson S, Bacon MA, Davies WJ. 1997. Multiple signals and mechanism that regulate leaf growth and stomatal behaviour during water deficit. Physiologia Plantarum 100, 303–313.
Vernieri P, Pardossi A, Tognoni F. 1991. Influence of chilling and drought on water relations and abscisic acid accumulation in bean. Australian Journal of Plant Physiology 18, 25–35.
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