JXB Advance Access originally published online on May 11, 2006
Journal of Experimental Botany 2006 57(9):1981-1989; doi:10.1093/jxb/erj145
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© The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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RESEARCH PAPER |
The effect of root pressurization on water relations, shoot growth, and leaf gas exchange of peach (Prunus persica) trees on rootstocks with differing growth potential and hydraulic conductance
Department of Plant Sciences, University of California, Davis, CA 95616, USA
*To whom correspondence should be addressed. E-mail: tmdejong{at}ucdavis.edu
Received 19 September 2005; Accepted 2 February 2006
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Abstract |
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It is well known that rootstocks can have an effect on the vegetative growth and development of the tree; however, there has been no clear explanation about the physiological mechanism involved in this phenomenon. Evidence indicates that the rootstock effects on tree vegetative growth may be related to hydraulic limitations of the rootstock. The objective of these experiments was to investigate the shoot growth, water potential, and gas exchange of peach trees on different rootstocks in response to manipulations of water relations of trees on rootstocks that differ in root hydraulic conductance. Tree water relations were manipulated by applying different amounts of pneumatic pressure on the root system and then relative shoot extension growth rate, tree transpiration rate, leaf water potential, leaf conductance, leaf transpiration, and net CO2 exchange rate responses were measured. Root pressurization increased leaf water potential, relative shoot extension growth rate, leaf conductance, leaf transpiration, and net CO2 exchange rates of trees on both vigorous and dwarfing rootstocks. There was a significant positive linear correlation between applied pneumatic pressure and tree transpiration rate and leaf water potential. Leaf conductance, transpiration rate, and net CO2 exchange rate as well as relative shoot extension growth rates were also positively correlated with the applied pneumatic pressure on the root system. These relationships were consistent across both vigorous and size-controlling rootstocks, indicating that rootstock hydraulic limitation may be directly involved in the vegetative growth control of peach trees.
Key words: Peach, Prunus, root pressurization, rootstock, vegetative growth, water relations
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Introduction |
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There are several physiological mechanisms that have been proposed to explain the decline in tree growth over time within a species (Ryan and Yoder, 1997). The hydraulic limitation mechanism hypothesis suggests that tree growth is limited by the conductance or resistance of water movement through the soil–plant continuum. The soil–plant hydraulic conductance theoretically determines an operating range for leaf water potential and transpiration rates to preserve the function of the hydraulic system (Tyree and Sperry, 1988). This concept has been experimentally demonstrated by Kolb and Sperry (1999) and Hacke et al. (2000). Stomata are regulated to maintain a leaf water potential and transpiration rate within the hydraulic limits of the soil–plant system. Soil–plant hydraulic conductance is positively correlated with stomatal conductance within a species (Saliendra et al., 1995) and among species (Meinzer et al., 1995). Furthermore, experimental manipulations that negatively affect the plant hydraulic system can have negative effects on stomatal conductance (Sperry et al., 1993; Saliendra et al., 1995), limiting transpiration rate (Sperry and Pokman, 1993) and carbon assimilation (Hubbard et al., 2001). This relationship is apparently facilitated by a water potential-mediated regulation of stomatal conductance (Saliendra et al., 1995; Fuchs and Livingston, 1996; Comstock and Mencuccini, 1998). Relative hydraulic conductance decreases with size (Yang and Tyree, 1993) and age (Mencuccini and Grace, 1996) within a species. More importantly, stomatal conductance and carbon assimilation also tend to decrease with tree age as hydraulic conductance decreases (Yoder et al., 1994; Hubbard et al., 1999). Correspondingly, Tyree et al. (1998) reported a good correlation between the hydraulic conductance and growth potentials of different tropical tree species, supporting the hypothesis that hydraulic conductance may constrain the long-term growth potential of trees.
Specific rootstocks can significantly influence the vegetative growth of fruit trees (Rogers and Beakbane, 1957; Lockard and Schneider, 1981; Webster, 1995). Evidence indicates that rootstocks can have an effect on tree vegetative growth by influencing the hormonal balance (Kamboj et al., 1999), mineral nutrition (Jones, 1971), and/or water relations (Olien and Lakso, 1986). It has been argued that the differences in rootstock effects on one or more of these processes account for the observed differences in vegetative growth of trees. Although there have been some improvements in understanding of rootstock effects on tree growth, there is no widely accepted explanation of the underlying physiological mechanism behind this phenomenon (Webster, 2004). Recent research conducted on peach trees with rootstocks that impart different tree growth potentials has shown significant differences in stem water potential (Basile et al., 2003) and leaf carbon assimilation (Solari et al., 2006a) associated with rootstock-induced differences in growth potential. The latter study also evaluated shoot growth responses to manipulations of stem water potential under field conditions. There was a direct positive relationship between stem water potential and shoot growth among peach trees on different rootstocks. Furthermore, differences in rootstock hydraulic conductance were positively related to the relative growth potential that these peach rootstocks imparted to trees growing in field conditions (Solari et al., 2006b). Similar results have been reported for apple rootstocks (Olien and Lakso, 1986; Cohen and Naor, 2002) but the differences in hydraulic conductance have been attributed to the graft unions rather than the rootstocks themselves (Atkinson et al., 2003). It appears therefore that the dwarfing effect of specific peach rootstocks on tree growth may be related to hydraulic limitation of the rootstocks involved. However, no study has related changes in hydraulic conductance to vegetative growth potential among peach trees on different rootstocks.
The root pressurization method provides an indirect means of testing the relationship between hydraulic conductance and vegetative growth potential among peach trees on different rootstocks. A pneumatic pressure applied in a chamber raises the hydrostatic pressure across the whole system (Passioura and Munns, 1984). This increases the total water potential throughout the soil–plant system assuming that no substantial increase in water flow occurs through the plant (Passioura and Munns, 1984). However, there is no pneumatic pressure effect on the root water relations because the pressure is equally transmitted throughout the air and liquid phases in the chamber so the difference between the two phases remains constant (Passioura and Munns, 1984). By contrast, the pneumatic pressure has a significant effect on shoot water relations, altering the turgor pressure component (Passioura and Munns, 1984). The present study used the root pressurization method to test the hypothesis that rootstock hydraulic limitations can account for the differences in vegetative growth potential in peach trees. The objective was to investigate the shoot growth, water potential, and leaf gas exchange responses of peach trees on different rootstocks under changing pneumatic pressure conditions of the root system. This was achieved by temporarily subjecting the rootstocks to differing amounts of pneumatic pressure, thus overcoming the differences in root hydraulic conductance between rootstocks.
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Materials and methods |
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One-year-old peach trees (Prunus persica L. Batsch, cv. O'Henry) grafted on two rootstocks were grown at the Controlled Environment Facility, University of California, Davis. The rootstocks used for this experiment were previously documented to impart a low (Prunus salicina Lindl.xPrunus persica L. Batsch hybrid, cv. K146–43) and high (Prunus persica L. BatschxPrunus davidiana hybrid, cv. Nemaguard) vegetative growth potential (Weibel et al., 2003). The environmental conditions in the controlled environment room were set at 14 h of light at 1000 µmol photons m–2 s–1 PPFD, 25/20 °C air temperature, and 50/80% relative humidity during the light and dark periods, respectively. The three trees of each rootstock were pruned to
0.2 m above the graft union, weighed, and planted in 40 l steel pressure chambers (wine fermentors; Webb et al., 1966) in February 2004. The soil medium consisted of 50% by volume of Turface fritted clay (Profile Products LLC, Buffalo Grove, USA) and 50% by volume of Pro-Mix BX peat moss (Premier Tech Ltd, Quebec, Canada) amended with 0.5 kg per tree of 18-6-12 Multicote fertilizer (N-P-K; Schultz Co., Bridgeton, USA). The trees were irrigated once a day to maintain the soil medium near maximum water-holding capacity. Each pressurization experiment involved two trees and six pressures, and pressurization experiments were repeated three times over a period of 1 month. The experiments were conducted on a total of three trees per rootstock and each rootstock was exposed to pressurization treatments twice. The pressure chambers consisted of steel cylindrical containers with flanges to attach a round steel plate with a welded coupler in the centre. The trunk of the dormant tree went through the coupler, two steel washers, and a threaded steel clamping device at the time of planting. The steel plate was bolted to the container flanges separated by a rubber gasket to ensure a pressure seal. Pressure chambers with trees grafted on the same rootstock were interconnected in series to a compressed air cylinder through an IR4000 series high-pressure regulator (Parker Hannifin Corp, Veriflow Division, Richmond, USA). On each measurement day a pressure seal was formed around the tree trunk by inserting a silicone rubber grommet between the washers and compressing it with the threaded steel clamping device. Pressure gauges, relief valves, check valves, and caps were also installed at this time. Different levels of pneumatic pressure (none, 0.2, 0.3, 0.4, 0.5, and 0.6 MPa) were applied on the root system over several days and physiological responses were measured at each pressure. The root system was initially pressurized using an air compressor and then a compressed air cylinder was opened to maintain the pneumatic pressure constant at each level for 6 h.
Experimental measurements were made during May. Shoot extension was measured on one shoot of each tree with a linear voltage displacement transducer (Transtek Co., Hartford, USA) during a root pressurization period. The shoot tip was attached to a fine copper wire with clear adhesive tape. The free end of the wire went through two eye screws and then was connected to the core of a linear voltage displacement transducer. The first and second eye screws were true to the shoot tip and the linear voltage displacement transducer, respectively, so that the shoot extension was equal to the displacement of the core. The relative shoot extension rate (RSER) was calculated as:
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Tree transpiration rate was gravimetrically measured with an ES100L digital scale (Ohaus Corp., Pine Brook, USA) during the last hour of a root pressurization period. Leaf water potential was also measured at this time on two fully mature, well-exposed leaves for each tree using the pressure chamber method (Scholander et al., 1965). The excised leaves of the selected shoots were pressurized with a 3005-model pressure chamber (Soil Moisture Equipment, Santa Barbara, USA). Leaf water potential was also measured at the end of the dark period and assumed to be in equilibrium with the soil water potential.
Leaf gas exchange measurements were conducted on five fully mature and well-exposed leaves with an LI-6400 infrared gas analyser (Li-Cor Inc., Lincoln, USA) during the last hour of a root pressurization period. Reference concentration of CO2 inside the leaf chamber was controlled at 400 µmol CO2 m–2 s–1. The PPFD, reference air temperature, and relative humidity inside the leaf chamber were set at 1000 µmol photons m–2 s–1 PPFD, 25 °C, and 50%, respectively. The soil respiration rate was measured by sampling the air inside the chamber during the last hour of a root pressurization period. CO2 concentration in the samples was determined with a Horiba infrared gas analyser (Horiba Instruments Inc., Irvine, USA).
Hydraulic measurements were made on each tree in June, subsequent to the pressurization experiments. The high pressure flow method was used to measure the hydraulic resistance (inverse of conductance) of the peach trees (Tyree et al., 1993, 1994). The high pressure flow method involves quasi-steady- and/or transient-state measurements. The hydraulic resistance from quasi-steady (Rquasi-steady state) and transient (Rtransient state) state measurements were calculated as:
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The biomass of the tree was separated into leaves, stems, trunk, root shank, and extension roots at the end of the hydraulic measurements. The total leaf area was measured with an LI-3100 area meter (Li-Cor Inc.). The fresh biomass was dried in a forced-air oven at 60 °C for at least 2 weeks to determine dry weight. Tree absolute growth rate (AGR) was calculated as:
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The tree relative growth rate was expressed as kg kg–1 d–1. The net assimilation rate (NAR) was calculated as:
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Statistical analyses of the data were made with SAS statistical software (SAS Institute, Cary, USA). Analysis of variance was used to test the rootstock effect on dry matter production, distribution, and growth of the trees. Analysis of variance was also used to test the rootstock effect on the scion, rootstock, and tree hydraulic conductance. The mean separation between the rootstocks was carried out with a 0.05 level of significance by the Tukey pair-wise comparison test. Non-linear regression analysis was used to test the rootstock effect on the relative shoot extension rate pattern. Multiple linear regression analysis was used to evaluate the relationships between applied pneumatic pressure, water potential, shoot growth, soil respiration, and leaf gas exchange variables of trees on different rootstocks.
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Results |
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The leaf water potential and tree transpiration rate were positively correlated with the applied pneumatic pressure on the root system (P <0.0001 and 0.0001). Trees grafted on Nemaguard had higher mean leaf water potentials (P <0.0001) and tree transpiration rates (P <0.0001) than trees on K146-43 (Fig. 1). There were no significant interaction effects between rootstock and applied pneumatic pressure on leaf water potential but there were on tree transpiration rate (P=0.0024). Leaf water potential at the end of the dark period (assumed to reflect soil water potential) was not significantly different among trees on different rootstocks (data not shown).
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The leaf conductance, transpiration and net CO2 exchange rates were also positively correlated with the applied pneumatic pressure on the root system (P=0.0001, 0.0001, and 0.004, respectively). Trees grafted on Nemaguard had a higher mean leaf conductance (P=0.0473), net CO2 exchange (P=0.0578), and transpiration rates (P=0.0212) than trees on K146-43 (Fig. 2). There was no significant interaction effect between rootstock and applied pneumatic pressure on these measurements.
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Trees grafted on Nemaguard had higher mean relative shoot extension rates (P <0.0001) than trees on K146-43 (Fig. 3). The relative shoot extension rates were also positively correlated with the applied pneumatic pressure on the root system (P <0.0001). However there was no significant interaction effect between the rootstock and applied pneumatic pressure on relative shoot extension rates (Fig. 4).
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Scion and rootstock hydraulic conductance per unit leaf area were significantly different among trees on different rootstocks (P=0.0015 and 0.003, respectively; Fig. 5). Trees on K146-43 had the highest mean scion hydraulic conductance per unit leaf area, whereas trees on Nemaguard had the highest mean rootstock hydraulic conductance per unit leaf area. Overall, trees on Nemaguard had a higher mean tree hydraulic conductance unit leaf area (P=0.0462) than trees on K146-43 (Fig. 5).
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The tree dry weight was not significantly different among trees on different rootstocks at the time of planting (Table 1). However, trees grafted on Nemaguard had a higher mean final tree dry weight than trees grafted on K146-43 (P=0.0037). The significant differences in final tree dry weights were only related to significant differences in final scion dry weights (P=0.0013) and, consequently, Nemaguard had the highest mean final scion to rootstock dry weight ratio (P=0.0018; Table 1).
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Trees on Nemaguard had higher mean absolute and relative growth rates (P=0.0018 and 0.0148, respectively) than trees on K146-43 (Table 2). Trees grafted on Nemaguard also had the highest mean net assimilation rate and leaf area ratio (P=0.0378 and 0.0163, respectively; Table 2). Conversely, trees grafted on K146-43 had a higher mean soil/root respiration rate than trees on Nemaguard (P=0.0320; Fig. 6).
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Discussion |
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As expected, root pressurization had a significant influence on the tree water relations. Leaf water potential was directly proportional to applied pneumatic pressure on the root system (Fig. 1). The rootstocks also had a significant effect on leaf water potential confirming previous studies (Basile et al., 2003; Solari et al., 2006a). However, the leaf water potential response to root pressurization was independent of the rootstock. The leaf water potential rise was not equivalent to the applied pneumatic pressure on the root system contrary to what was reported by Passioura and Munns (1984). For instance, a 0.6 MPa increase in applied pressure to the Nemaguard trees might have been expected to result in an increase in leaf water potential from –0.9 to –0.3 MPa if transpiration and hydraulic conductance remained unchanged. But since transpiration also increased by
50% there was an apparent increase in the water potential gradient within the plant and a measured leaf water potential of about –0.6 MPa after pressurization. Thus a transient increase in leaf water potential following root pressurization was reduced by an increase in the transpiration rate of the trees (Fig. 1), and this corresponded to a measured increase in leaf conductance (Fig. 2). Tree transpiration rate was directly proportional to the applied pneumatic pressure on the root system but the slope of the relationship differed between rootstocks (Fig. 1). The different rootstock effects on tree transpiration rate response to root pressurization may suggest differences in hydraulic conductance among trees on the two rootstocks. Previous studies have also used the root pressurization technique to drive changes in plant water status (Saliendra et al., 1995; Fuchs and Livingston, 1996; Comstock and Mencuccini, 1998). These studies demonstrated that leaf water potential acts as a feedback mechanism that can regulate stomatal conductance. The present study supports those reports and also shows that leaf transpiration and net CO2 exchange rates increased linearly with the applied pneumatic pressure on the root system (Fig. 2). Solari et al. (2006a) presented similar results in the field when the water potential of peach trees on the same rootstocks was manipulated by partially covering the tree canopies. After covering the canopy there was an increase in stem water potential, leaf conductance, transpiration, and net CO2 exchange rates. These results clearly indicate the physical aspects of the control of water movement through the soil–plant system. These physical principles have been used to explain patterns of water use with respect to soil and atmosphere environments and differences in species and cultivars (Sperry, 2000), and now this paper demonstrates the same principles with regard to the differences in rootstocks of compound fruit trees. The root pressurization also had a significant influence on the pattern of shoot growth. The applied pneumatic pressure initially caused a dramatic increase in relative shoot extension rate (Fig. 3). This initial extension surge cannot be entirely attributed to an elastic expansion since this process was not entirely reversible after the pneumatic pressure was released on the root system. Thereafter, the relative shoot extension rate decreased, probably related to adjustments in cell wall properties (Green et al., 1971). The decrease in relative shoot extension rate was the same for trees on both rootstocks. The shoot extension rate eventually returned to a steady-state condition (Fig. 3). Passioura and Munns (2000) reported similar growth patterns when pneumatic pressure was applied on other plant species that exhibited elastic and inelastic responses in leaf extension during root pressurization. Similar responses have also been observed in response to sudden environmental changes in light (Christ, 1978), relative humidity (Shackel et al., 1987; Serpe and Matthews, 2000), and soil water potential (Acevedo et al., 1971; Serpe and Matthews, 1992).
However, the relative ‘steady-state’ shoot extension rates of the pressurized trees in the present study clearly differed from the non-pressurized trees (Fig. 4). These resultant relative shoot extension rates were directly proportional to the applied pneumatic pressure on the root system. More importantly, the rootstocks did not have significant differential effects on this relationship despite their inherent differences in relative shoot extension growth rates (Solari et al., 2006a). The differences in relative shoot extension rate between pressurized and non-pressurized trees presumably involved a persistent adjustment in growth-inducing water potential gradients (Nonami and Boyer, 1993; Nonami et al., 1997) expressed as turgor pressure (Serpe and Matthews, 1992; Hsiao et al., 1998) contrary to the proposed complete self-stabilization growth concept (Green and Cummins, 1974; Passioura and Fry, 1992; Zhu and Boyer, 1992).
The present study confirms the influence that specific peach rootstocks have on the hydraulic conductance of the tree. The rootstocks had a significant effect on tree hydraulic conductance (Fig. 5). These differences in tree hydraulic conductance were associated with significant differences in rootstock hydraulic conductance. This result is consistent with previous studies on the same peach rootstocks (Solari et al., 2006b). However, the scion in this study also showed significant differences in hydraulic conductance partially counteracting the effect of the rootstock. It is difficult to explain the differences in scion conductance since they were the same genotype, except to note that the hydraulic conductance of the scion and root of the trees on Nemaguard were relatively balanced, while the conductances of the two were clearly unbalanced in the trees on K146-43. It may be that the scion response to decreased relative conductance in the rootstock was to increase its relative conductance.
The differences in tree hydraulic conductance among rootstocks were overcome by applying differing amounts of pneumatic pressure on the root system. This process simulated changes in tree hydraulic conductance considering the biophysics of water movement. The root pressurization improved the tree water status which had a positive effect on shoot growth in agreement with Berman and DeJong (1997) and carbon assimilation similar to previous field studies (Solari et al., 2006a). In the long term, the rootstock-related differences in tree water status had a pronounced effect on dry matter distribution (Table 1), similar to what has been reported previously (Steinberg et al., 1989), and the overall vegetative growth of the tree. These effects on the tree dry matter production, distribution, and growth are consistent with the physiological responses to root pressurization and indicate that the hydraulic limitation mechanism can account for differences in vegetative growth potential in peach trees (Tables 1, 2). Additionally, the fact that the two rootstocks had the same root dry weight, while having substantially different apparent root/soil respiration rates, suggests that the rootstocks differed in specific root respiration rates (Fig. 6). This, in turn, may also have affected the total tree relative growth and net assimilation rates (Table 2). More comparative research needs to be done to clarify the potential role of differences in root respiration rates among these vigorous and size-controlling peach rootstocks. In the meantime, this study clearly documents that there is a direct relationship between tree hydraulic conductance and peach relative shoot extension growth rate; and this, as well as previous research (Solari et al., 2006b), indicates that rootstock hydraulic conductance differs among the peach rootstocks examined. Thus there is clear evidence that rootstock hydraulic conductance is at least one physiological mechanism involved in the size-controlling potential of selected peach rootstocks.
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Acknowledgements |
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We would like to thank Drs Albert Fischer, Bruce Lampinen, Kenneth Shackel, and Mark Matthews for the use of their equipment and laboratories. We are grateful to Mr Manuel Solari for his invaluable assistance during measurements and Mr Dennis Lewis and William Slater at the UC Davis Controlled Environment Facility for their assistance with the controlled environment room.
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