JXB Advance Access originally published online on May 7, 2004
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Journal of Experimental Botany, Vol. 55, No. 401, pp. 1371-1382, June 1, 2004
© 2004 Oxford University Press
RESEARCH PAPER |
Hydraulic conductance and rootstock effects in grafted vines of kiwifruit
Received 19 December 2003; Accepted 26 February 2004
Horticulture and Food Research Institute of New Zealand, Te Puke Research Center, RD 2 Te Puke, New Zealand
* To whom correspondence should be addressed. Fax: +64 7 573 3871. E-mail: mclearwater{at}hortresearch.co.nz
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Abstract |
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Whole-plant hydraulic conductance, shoot growth, and leaf photosynthetic properties were measured on kiwifruit vines with four clonal rootstocks to examine the relationship between plant hydraulic conductance and leaf stomatal conductance (gs) and to test the hypothesis that reduced hydraulic conductance can provide an explanation for reductions in plant vigour caused by rootstocks. The rootstocks were selected from four species of Actinidia and grafted with Actinidia chinensis var. chinensis ‘Hort16A’ (yellow kiwifruit) as the scion. Total leaf area of the scion on the least vigorous Actinidia rootstock, A. kolomikta, was 25% of the most vigorous, A. hemsleyana. Based on shoot growth and leaf area, the selections of A. kolomikta and A. polygama are low-vigour rootstocks, and A. macrosperma and A. hemsleyana are high-vigour rootstocks for A. chinensis. Whole-plant hydraulic conductance, the ratio of xylem sap flux to xylem water potential, was lower in the low-vigour rootstocks, reflecting their smaller size. However, leaf-area-specific conductance (Kl) and gs were both higher in the low-vigour rootstocks, the opposite of the expected pattern. Differences in Kl were found in the compartment from the roots to the scion stem, with no difference between rootstocks in the conductance of stems or leaves of the scion. There was no evidence that the graft union caused a significant reduction in hydraulic conductance of vines with low-vigour rootstocks. Leaf photosynthetic capacity did not vary between rootstocks, but photosynthesis and carbon isotope discrimination (
13C) under ambient conditions were higher in the low-vigour rootstocks because gs was higher. gs and 13C were positively correlated with Kl, although the mechanism for this relationship was not based on stomatal regulation of a similar xylem water potential because water potential varied between rootstocks. For Actinidia rootstocks, changes in Kl do not provide a direct explanation for changes in vigour of the scion. However, depending on the rootstock in question, changes in hydraulic conductance, biomass partitioning, and crown structure are involved in the response. Key words: Actinidia, hydraulic conductance, kiwifruit, photosynthesis, rootstock effects, stomatal conductance, water relations.
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Introduction |
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Clonal rootstocks are widely used to control the vegetative vigour of fruit trees and improve fruit yield and quality (Webster, 1995; Castle, 1995). The mechanisms for these commercially useful rootstock effects are complex and poorly understood, but a common hypothesis is that rootstocks that reduce scion vigour have low hydraulic conductance (Syvertsen and Graham, 1985; Atkinson and Else, 2001). Low root conductivity may reduce water transport to the shoots, ultimately decreasing stomatal conductance (gs), photosynthesis, and shoot growth for a given investment in root biomass. In this study, the hydraulic architecture and leaf physiology of grafted kiwifruit (Actinidia) plants were compared with a range of new rootstocks that vary in the degree of vegetative vigour they impart to the scion. The aim was to learn more about the physiological mechanism for the control of kiwifruit scion vigour by the rootstock, and in particular to examine the relationship between the hydraulic architecture of the vine and leaf stomatal conductance and photosynthesis.
Previous explanations for rootstock effects on fruit trees have included the influence of the rootstock on water and mineral transport to the shoots (Jones, 1976; Olien and Lakso, 1986), growth regulator signals (Beakbane, 1956; Jones, 1986; Soumelidou et al., 1994b; Kamboj et al., 1999; Sorce et al., 2002), and the direct influence of the graft union on phloem and xylem transport (Simons, 1986; Soumelidou et al., 1994a, b; Atkinson et al., 2003). Particular attention has been focused on the hydraulic conductivity of the roots and graft union and their influence on water transport. Citrus rootstocks that promote vigour in the scion have high root conductivity, higher rates of leaf gas exchange, increased leaf N and P concentration and higher shoot to root ratios when grown as ungrafted plants (Syvertsen, 1981; Syvertsen and Graham, 1985). Leaf water potential (
l) and gs are lower in scions grafted onto dwarfing apple rootstocks when they are subjected to drying soil (Olien and Lakso, 1986; Higgs and Jones, 1990). The ability of apple rootstocks to control scion vigour has therefore been related to the way they respond to drought (Atkinson et al., 2000). Two recent studies of dwarfing apple rootstocks have both highlighted reductions in hydraulic conductance caused by low-vigour rootstocks. Cohen and Naor (2002) found that, in an orchard situation with plant spacing adjusted to maintain a similar leaf area index, dwarfing rootstocks reduced total water use without altering total conductance relative to sapwood area (no effect on sapwood area specific conductance, Ks). Reductions in scion vigour instead corresponded with reduced conductance from the soil to stem relative to the leaf area supplied (reduced leaf-area-specific conductance, Kl). By contrast, Atkinson et al. (2003) destructively measured properties of the graft union of apple trees and concluded that the hydraulic conductance of the graft union provided a mechanistic explanation of the rootstock effect. Ks and Kl of the graft union and rootstock and scion stems were lower on dwarfing rootstocks, and Atkinson et al. (2003) therefore concluded that the rootstock induced anatomical changes in the graft and scion. These changes may restrict water and mineral transport to the scion and possibly cause the accumulation of basipetally transported auxin. When considered overall, the variety of rootstock effects across many crops and the complexity of interactions between the roots and shoot mean that it is not likely that there is a single, simple explanation for rootstock effects on scion vigour. However, in many examples, long-distance transport mechanisms are likely to be involved. In general, low transport efficiency of the rootstock or rootstock and scion together are equated with low scion vigour.
Kiwifruit is a relatively new commercial crop with few rootstock cultivars available. The control of excess vegetative vigour is a major expense for kiwifruit growers (Miller et al., 2001). In addition, yields are often limited by spring flower production. The selection of ‘Kaimai’, a clonal rootstock cultivar from the species Actinidia hemsleyana Dunn, has already demonstrated the potential for new Actinidia rootstocks. When used as a rootstock for Actinidia deliciosa var. deliciosa ‘Hayward’ (green kiwifruit), ‘Kaimai’ doubles the number of flowers on each shoot by enhancing the synchrony of spring budbreak and reducing floral abortion before anthesis (Wang et al., 1994b). ‘Kaimai’ does not, however, reduce scion vigour. Flower-promoting kiwifruit rootstocks, including ‘Kaimai’, tended to have a higher total cross-sectional area of xylem vessels in the stele, implying higher root axial conductivity (Wang et al., 1994a). The roots of flower-promoting rootstocks also contain more starch and mucilage-containing crystalline idioblast cells, leading Wang et al. (1994a) to speculate that reserve mobilization and plant water status in spring had important effects on scion flower production. Several other groups have demonstrated significant rootstock effects on shoot growth and flower production in Actinidia (Viti et al., 1990; Cruz et al., 1997), but there are currently no practical rootstocks available for controlling scion vigour. There is also no information on the physiological mechanism by which an Actinidia rootstock might reduce scion vigour. The indication from the apple and citrus research described above is that such a rootstock will have low root conductance and reduce water transport to the shoot.
The hypothesis was that Kl would be lower in grafted Actinidia plants with rootstocks that caused a reduction in scion vigour. Preliminary measurements with four clonal rootstocks grafted with the same scion showed that the rootstocks did have significant effects on scion water relations and gs, and there were clear reductions in vigour in two of the four rootstocks. Studies of tree hydraulic architecture have recently emphasized the existence of a common relationship between Kl and stomatal regulation of transpiration (Meinzer et al., 2001; Hubbard et al., 2001). The stomata are thought to respond to hydraulic and chemical signals in a way that integrates the hydraulic conductance of the soil to leaf pathway, thus maintaining a constant l and maximizing photosynthesis while minimizing the risk of hydraulic failure through cavitation (Bond and Kavanagh, 1999; Sperry, 2000). The response of gs to Kl may help explain the effects of these Actinidia rootstocks on scion vigour.
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Materials and methods |
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Plant material
Cuttings for four rootstock clones were taken in 1995 and rooted in a nursery. The four rootstocks were part of a larger trial of eight genotypes selected to encompass a range of Actinidia species and growth forms. Actinidia hemsleyana Dunn ‘Kaimai’ (formerly known as ‘TR2') is a registered rootstock cultivar known to promote flowering and vigour in green kiwifruit (Wang et al., 1994b). The other three clones, of unknown potential as rootstocks, were selected from three different species held in the Actinidia germplasm collection at the HortResearch Te Puke Research Orchard. The species were Actinidia macrosperma C.F. Liang, Actinidia polygama (Sieb. et Zucc.) Maxim., and Actinidia kolomikta (Maxim. et Rupr.) Maxim. Hereafter, each clonal selection will be referred to by its species name. As ungrafted plants the A. hemsleyana, A. macrosperma, and A. polygama clones grow as vigorous, deciduous vines at the Te Puke site. The A. kolomikta clone, a deciduous species from colder continental climates in north-east Asia, grows slowly and is difficult to establish as a mature vine at the Te Puke site. The scion used on all rootstocks was Actinidia chinensis Planch. var. chinensis ‘Hort16A’, a commercial cultivar of yellow fleshed kiwifruit (Ferguson and Retamales, 1999).
Scion wood was whip and tongue grafted onto the rootstocks in 1996 at a height of 0.5 m. The grafted plants were planted in the orchard in August 1997 with 5.6 m between plants and 4.6 m between rows. The experimental design was a randomized complete block, with one grafted plant of each rootstock randomly arranged within six replicate blocks. Similar grafted vines were used as buffer rows around the entire experiment and male vines for pollination were interspersed among and around the blocks. The scions were trained on to a pergola structure 1.85 m high, with a single stem from the graft to pergola height and two leaders trained north and south in the row direction and managed according to normal commercial practice (Fig. 1), except that no growth regulators were used to promote bud burst or fruit growth. During winter the vines were pruned to remove excess growth and long one-year-old shoots tied down to form the fruiting crown for the next season. Vines on weaker rootstocks had fewer long shoots, so higher proportions of older shoots with short one-year-old laterals were therefore retained as the fruiting crown. After flowering the fruit were thinned to remove misshapen fruits and to maintain a minimum ratio of approximately two leaves per fruit on the weaker rootstocks. The vines were sprinkler irrigated beneath the canopy every 3–4 d during the summer to prevent significant soil water deficits developing. The measurements reported in this study were taken over two years from November 2000 until January 2003, a period that spans most of three growing seasons. The majority of measurements were made in the season that began in spring 2001 and ended with harvest in May 2002.
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Leaf area, plant size, and yield
Leaf area index (LAI) was calculated from gap fraction data extracted from monthly digital hemispherical canopy photographs taken with a Nikon Coolpix 990 camera and an FC-E8 fish-eye adapter, beginning in October 2001. The proximity of shelter trees to the western edge of the experimental plots meant that two photographs were taken per plant, one under the western edge of the crown and one under the centre, and only the eastern side of each photograph used for analysis. Black and white photographs were taken under overcast conditions with the compression level set to fine. To avoid bias by canopy density, exposure was determined by pointing the camera at the sky (no canopy) and observing the exposure level with the camera in automatic mode and exposure compensation set to –1.0, then fixing this observed exposure in manual mode for photographs under the canopy. Publicly available software (Gap Light Analyser 2.0, Simon Fraser University, British Columbia) was used to extract the gap fraction for each 10° zenith and 15° azimuth sector. Mean transmission was calculated for 10° zenith angle intervals from 10° to 60°, after discarding any sectors that fell outside the crown of the plant. Leaf angle was measured directly on the scion using a compass-protractor and LAI was then calculated from the transmission data based on the assumption of an ellipsoidal leaf angle distribution and a mean leaf angle of 25.4° (Norman and Campbell, 1989; Campbell, 1990). Photographic LAI estimates were verified against direct measurements of LAI made by counting or harvesting leaves. For pergola-grown kiwifruit canopies the relationship between LAI estimated from the photographed gap fraction and that measured directly had a slope of 1.0±0.05 and an R2 >0.9 (M Clearwater, unpublished data).
Six emerging shoots were labelled during budburst on three replicate vines of each rootstock (72 shoots in total). Three shoots per plant were from buds emerging on parent shoots longer than 0.3 m, and three from parent shoots less than 0.3 m. Starting on 14 September 2001, and at approximately weekly intervals until 1 November, the width of each leaf on the shoot was measured using a ruler as soon as the leaf was large enough to handle (approximately 10 mm wide). Area per leaf was calculated from a regression developed by periodically harvesting leaves of a range of sizes from other shoots and relating leaf area to leaf width, and leaf area per shoot by summing the individual leaf areas. During measurements, the shoot apical bud was classified as alive or dead. Normal shoot development of kiwifruit includes a proportion of shoots with apical buds that cease growth and abort, resulting in a ‘terminated’ shoot.
Projected crown area (Acrown) for each plant was estimated at the end of the 2002 and 2003 seasons from measurements of the width of the crown perpendicular to the row direction at 0.5 m intervals, and calculating crown area as the sum of the measured widths multiplied by 0.5 m. Total crown leaf area (Aleaf) was calculated as crown area multiplied by LAI for the relevant month. Each year in early May the fruit from each vine was harvested and the weight of each fruit recorded. In July, when the vines were dormant, stem diameter was measured at marked points 0.15 m above and below the graft union. After accounting for average bark thickness the Huber value was calculated as the ratio of sapwood area above the graft to leaf area.
Photosynthesis
During the first measurement season leaf samples were taken every 6 weeks for specific leaf area (SLA) and 
13C determination, beginning in November 2000. Five fully expanded, sun-exposed leaves were selected from shoots that began growth in spring. After removing the petioles, lamina area was measured using a leaf area meter (LI3100, Li-Cor, Nebraska). The leaves were then dried at 65 °C for 24 h, dry weight was recorded and the samples finely ground in a ring grinder. Subsamples of leaf tissue were sent to the University of Waikato Stable Isotope Unit where the 13C/12C ratio was measured in a mass spectrometer (Tracermass, Europa Scientific Ltd, Crewe, UK) and discrimination expressed relative to that of the PeeDee belemnite standard (p 13C). Discrimination relative to CO2 in the air was calculated as 13C=(a–p)/(1+p), where a is the of the source air (Farquhar et al., 1982), which was assumed to be –8
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The photosynthetic response of leaves to light and CO2 was recorded between December 2001 and January 2002 using a portable photosynthesis system equipped with an LED light source (LI6400 and 6400-02B, Li-Cor, Nebraska). Five light-response and 8–12 CO2-response curves were recorded for each rootstock. Each curve was recorded on a newly selected, fully expanded, sun-exposed leaf on a shoot that began growth in spring, with leaves selected from at least three different plants per rootstock. For light-response curves leaf temperature was between 20 °C and 25 °C, and the vapour pressure deficit (Dl) between 0.5 and 1.0 kPa. For the CO2-response curves leaf temperature was controlled at 20 °C, Dl between 1.0 and 2.0 kPa, and light intensity held at 1500 µmol m–2 s–1. Light-response curves were fitted with a non-rectangular hyperbola (Ogren and Evans, 1993), and the parameters Amax (light-saturated rate of photosynthesis), 
(apparent quantum efficiency), Rd (dark respiration), and 
(convexity) estimated by non-linear regression (Photosyn Assistant, Dundee Scientific, Dundee, UK). Plots of photosynthesis as a function of intercellular CO2 concentration (ci) were fitted with the mechanistic model of (von Caemmerer and Farquhar (1981) and the parameters Jmax and Vcmax estimated by non-linear regression (Photosyn Assistant, Dundee Scientific, Dundee, UK). For comparison with the 13C discrimination measurements of the previous summer, the leaves used for CO2-response measurements were retained, dried at 60 °C for 24 h and five from each rootstock sent for 13C analysis as described above.
Photosynthesis and stomatal conductance of leaves under ambient conditions was recorded during January 2002. For these measurements, the light source was removed from the photosynthesis system, chamber temperature set to ambient air temperature (15–25 °C) and reference CO2 concentration controlled to give values in the leaf chamber between 350 and 370 µmol mol–1. On ten sunny or partially cloudy days photosynthesis was recorded between 10.00 h and 15.00 h on randomly selected, sun-exposed leaves on the same type of shoots and the same plants as those used for response curves. Usually six measurements were made on a plant before moving to the next rootstock and scion within the randomized block, then the procedure was repeated periodically through the day. During measurements, leaf temperature varied between 20 °C and 30 °C, Dl between 0.8 kPa and 2.5 kPa, and irradiance between 20 µmol m–2 s–1 and 2200 µmol m–2 s–1, with the variation in irradiance resulting from variation in leaf orientation and cloud cover. To compare ambient photosynthesis between rootstocks under light-saturated conditions, the data were filtered to exclude measurements when irradiance at the leaf surface was <1500 µmol m–2 s–1, and mean photosynthesis (A), gs, and leaf internal CO2 concentration (ci) compared using analysis of variance (ANOVA) with vine nested within rootstock. For this comparison there were between 112 and 142 individual measurements spread over three plants per rootstock treatment. Mean irradiance for each rootstock was also compared to confirm that there was no bias in leaf irradiance during measurements.
Hydraulic conductance
Whole-plant hydraulic conductance was calculated periodically from February 2002 to January 2003 from measurements of whole vine sap flux and xylem water potential (the evaporative flux method; Tsuda and Tyree, 2000). Measurements were made at approximately monthly intervals through parts of two summers because of initial difficulty encountered measuring sap flow. The earliest measurements were on 8 November, when the leaf area index was approximately 80% of its maximum, and the last measurements were on 2 May, at the time of harvest and before significant leaf drop. Sap velocity was measured continuously every half hour using the heat pulse velocity method (Green et al., 2003), with thermocouples spaced at 5, 10, 15, and 20 mm depth within the sapwood. Two Teflon probe sets were installed in the scion of one plant of each rootstock treatment and connected to a CR10 datalogger and AM25T multiplexor (Campbell Scientific, Logan, UT). Replication was achieved by installing the equipment in a new randomized block three times during the experiment. Probes were installed at least 0.2 m above the graft union and below the pergola height. Bark thickness and stem diameter were recorded each time a probe was installed or removed. Attempts to use the heat pulse compensation method were unsuccessful because of the high velocity of sap flow in the small diameter but very porous kiwifruit stems. Cross-over times were too short to detect during periods of high evaporative flux. Heat pulse velocity was instead measured using the Tmax method, with the probes and datalogger configured to record the time until the maximum temperature rise downstream of the heater probe (Green et al., 2003). Heat pulse velocity was converted to sap velocity and volumetric sap flux for the plant (Eplant, kg s–1) by dividing total stem sapwood area (Asapw) into an annulus for each thermocouple and summing annulus area multiplied by sap velocity for each annulus. Sap velocity was usually highest close to the cambium and declined moderately towards the centre of the stem, but the entire radius was conducting. Transpiration was also expressed per unit leaf area (Eleaf) by dividing Eplant by Aleaf.
For estimates of hydraulic conductance, xylem water potentials were measured using a pressure chamber on relatively sunny days on the same vines as used for sap velocity measurements. The flow pathway was partitioned into three compartments by measuring water potential at three different positions within the plant (Fig. 1), xylem water potential as close as possible to the main stem (stem), xylem water potential midway between the centre and edge of the crown (shoot), and leaf water potential also in the mid-crown area (leaf). stem and shoot were measured with the pressure chamber using leaves that had been prevented from transpiring by covering with aluminium foil the previous night or early in the morning of the same day. leaf was measured on a leaf from the same or a nearby shoot to that used for shoot, except that the leaf was transpiring normally. Pressure chamber measurements on non-transpiring leaves reflect the water potential of the xylem in the stem to which the leaf is attached, whereas measurements on transpiring leaves reflect a bulk average of xylem and tissue water potential within the leaf itself (Meinzer et al., 2001). Measurements were taken every 1–2 h, while the vines were still exposed to sun, usually between 10.00 h and 17.00 h. Two measurements were made per position, one on each side of the vine, and further measurements were made if the first two did not agree. Dawn water potentials (soil) were made on covered leaves on some days, but with the irrigation, summer rainfall of the region, and positive nocturnal root pressures, there were no significant differences between rootstocks and soil water potential was assumed to be zero.
The water potential values were averaged for each time and position and matched with the corresponding average sap flux measurement for the vine during the same half hour. Hydraulic conductance (K, kg MPa–1 s–1) for each portion of the pathway from soil to leaf was calculated as:
K=Eplant/–(1)
where was the difference in water potential across each portion of the pathway (stem for K from soil to stem, shoot–stem for K from stem to shoot, leaf–shoot for K of the leaves, and leaf for K of the whole pathway from soil to leaf; Fig. 1). Leaf-area-specific conductance (Kl), scion sapwood area specific conductance (Ks) and crown area specific conductance (Kg) were calculated from K as:
Kl=K/Aleaf(2)
Ks=K/Asapw(3)
Kg=K/Acrown(4)
(Tsuda and Tyree, 2000; Cohen and Naor, 2002). All conductance values were expressed in units of kg MPa–1 m–2 s–1. Where necessary, an additional subscript was used to denote the relevant portion of the flow pathway for a particular conductance estimate, for example, Kl,soil-stem for leaf-specific conductance from soil to the stem or Kl,plant for leaf-specific conductance for the whole pathway. If it is assumed that transpiration per unit leaf area is the product of stomatal conductance times an effective vapour pressure deficit at the leaf surface, then from equations 1 and 2:
Kl=gsDl/(–Pmw)(5)
(Hubbard et al., 2001). Atmospheric pressure (P) and the molecular weight of water (mw) are included to account for the expression of Dl in kPa and gs in mol m–2 s–1. Equation 5 shows that, for a linear relationship between Kl and gs, the quotient of Dl and should remain constant.
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Results |
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Plant size and leaf area
The crown area and leaf area index of the A. chinensis scion varied strongly in response to the rootstock on which it was grafted (Table 1; Fig. 2). Scions growing on the lowest vigour A. kolomikta stock occupied half the area, had half the leaf area index, and therefore had one-quarter of the total leaf area of scions on the most vigorous A. hemsleyana rootstock (Table 1). A. polygama and A. macrosperma rootstocks produced plants of intermediate size and leaf area index. Overall, A. kolomikta and A. polygama can be considered low-vigour rootstocks, and A. macrosperma and A. hemsleyana high-vigour rootstocks for this A. chinensis scion. Reductions in leaf area were not accompanied by equivalent reductions in flower numbers. Although a higher proportion of fruitlets were thinned from the low-vigour vines after anthesis (data not shown), these vines still carried higher crop loads relative to total leaf area (Table 1).
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Differences in crown size and leaf area were related to differences in the rate of early shoot development and the proportion of terminating shoots (Fig. 3). When vigorous, non-terminating shoots were considered, there was little difference in the rate of shoot leaf area development between rootstocks (Fig. 3A). However, less vigorous shoots that eventually terminated developed more slowly and the final total leaf area on each shoot was lower on the two low-vigour rootstocks (Fig. 3B). Of the 18 monitored shoots for each rootstock, 16 shoots (89%) had terminated on both the A. kolomikta and A. polygama stocks, while 8 and 5 shoots (44% and 28%, respectively) had terminated on the A. macrosperma and A. hemsleyana rootstocks by the end of measurements on November 1. The scion on the low-vigour rootstocks therefore had a higher proportion of terminating shoots, and their terminating shoots grew more slowly and had less leaf area per shoot. The leaf area index thus increased more slowly at the beginning of the season (Fig. 2). The low number of non-terminating shoots that extend beyond the existing crown also explains the low crown area on the low-vigour stocks (Table 1).
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While the low-vigour stocks supported a reduced leaf area, the sapwood area of the scion main stem was not reduced when compared with the vigorous stocks (Table 1). The ratio of scion sapwood area to leaf area (the Huber value) was therefore three times higher with the low-vigour rootstocks (Table 1). By contrast with the usual taper in diameter from rootstock to scion, the A. polygama rootstock produced a relatively narrow rootstock stem, but a wider scion stem, and the highest ratio of scion sapwood area to rootstock sapwood area (Table 1).
Photosynthesis and stomatal conductance
The scions on the two low-vigour rootstocks had significantly lower SLA early in the season (Fig. 4A). 13C measured on the same leaf sample also showed consistent differences between rootstocks (Fig. 4B). A. polygama contrasted strongly with the other rootstocks by imparting the highest and least seasonally variable discrimination to the scion. 13C was lower with the three other rootstocks, but increased as the season progressed. In these three rootstocks discrimination was consistently ranked according to the leaf area and vigour of the scion: 13C A. hemsleyana (most vigorous)<A. macrosperma<A. kolomikta (least vigorous) (Fig. 4B).
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During the middle of the growing season no significant difference in the photosynthetic response to light or CO2 could be detected between rootstocks. Fitted parameters for the light response averaged (±SE) over the four rootstocks were Amax 19.5±0.8,
0.057±0.003, Rd 1.2±0.2, 0.40±0.03. For the CO2 response the average parameters were Vcmax 37±1 and Jmax 112±4. While there were no clear differences in photosynthetic capacity, there were pronounced differences between rootstocks in the stomatal conductance and photosynthesis of scion leaves during photosynthesis on clear, sunny days. Under ambient conditions with high irradiance, gs, A, and ci were higher on the two low-vigour stocks (Table 2). The leaves on the A. polygama stock were noticeable in having the highest gs and ci of all the stocks. Measurement of 13C on a sample of leaves used for the CO2 response curves confirmed the same pattern of discrimination as observed during the previous season (compare Table 2 and Fig. 4B).
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Hydraulic conductance
Xylem water potential measured on fine days did not correspond to the vigour imparted by the rootstock. The scion on A. kolomikta, a low-vigour stock, had the most negative water potentials, while the scion on A. polygama, also a low-vigour stock, had the least negative water potentials (Fig. 5). The same pattern was observed regardless of the position in the crown, but differences were more pronounced the closer that measurements were made to the rootstock and the
stem position. Approximately 50% of the total pressure drop from roots to the leaves occurred between the soil and the scion stem, less than 10% between the scion main stem and the leaves, and the remaining 40% in the leaves (Fig. 5).
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The hydraulic conductance (Kplant) of the rootstock and scion reflected the overall size of the plants. There were no consistent seasonal or daily changes in Kplant, nor was there any clear hysteresis in plots of transpiration against
. The values presented here are, therefore, the overall averages for the measurement period. Larger plants (A. hemsleyana and A. macrosperma) had higher conductance up to the leader (Ksoil-stem), the shoots (Kstem-shoot) and the leaves (Kleaf; Table 3). However, when conductance was expressed relative to the leaf area supplied (leaf-specific hydraulic conductance, Kl), whole-plant conductance (Kl,plant) was higher in the low-vigour rootstocks because of differences in the compartment from soil to scion stem (Kl,soil-stem; Table 3). Kl,soil-stem of the A. polygama rootstock/scion combination was 56% higher than that of A. kolomikta, which in turn was 37% higher than that of A. macrosperma and A. hemsleyana. However, there were no significant differences between rootstocks in Kl,stem-shoot and Kl,leaf. When conductance was expressed relative to scion sapwood area above the graft (specific conductance, Ks,plant), conductance was lowest in the low-vigour rootstocks (Table 4). This result reflects the large sapwood area of the stems of the low-vigour vines relative to the sap flux through these vines (Table 1). Conductance expressed relative to projected area occupied by the crown (Kg) was lowest with the A. kolomikta rootstock, particularly up to the main stem (Kg,soil-stem; Table 4). Overall the low-vigour rootstocks had lower hydraulic conductance relative to ground area occupied by their scion.
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For all measures of conductance, the conductance from the main stem to shoots in the mid-canopy was an order of magnitude higher than conductance from soil to the stem and conductance of the leaves (Tables 3, 4). This means that most of the resistance to flow was located between the soil and scion main stem, and within the leaf.
Ambient leaf photosynthetic parameters were correlated with differences in hydraulic properties caused by the rootstocks (Fig. 6). ci measured using gas-exchange equipment was correlated with 13C, indicating that the observed differences in A and gs under ambient conditions provide an explanation for the carbon isotope signature of the scion (Fig. 6A). Both gs and 13C were strongly correlated with Kl,soil-stem (Fig. 6B, C). gs was not significantly correlated with Kl,stem-shoot or Kl,leaf. In low-vigour rootstocks high gs was associated with high Kl,soil-stem, particularly in the A. polygama rootstock that had the highest gs and Kl,soil-stem (Fig. 6B). Leaf level stomatal behaviour therefore appeared to be coupled to leaf-specific hydraulic conductance, with variation in conductance caused by differences between rootstocks in the pathway from the roots to the scion main stem.
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Discussion |
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Kl plant was higher in Actinidia plants with rootstocks that reduced scion vigour, and lower in plants with increased vigour, the opposite of the expected pattern. This result contrasts with the two recent studies of apple rootstocks that measured low Kl in plants with dwarfing rootstocks (Cohen and Naor, 2002; Atkinson et al., 2003). The gs of sunlit leaves was also higher in the low-vigour plants and there was a positive linear relationship between gs and Kl,soil-stem. As a result there were consistent differences between rootstocks in the photosynthesis and carbon isotope composition of scion leaves.
Co-ordination between gs and Kl
The links between stomatal function, hydraulic capacity, and regulation of the transpiration rate have been widely demonstrated in other species (Meinzer, 2002). The stomata of many species respond to sudden changes in Kl caused by defoliation (Pataki et al., 1998), shading (Whitehead et al., 1996), or partial cutting of the xylem (Sperry et al., 1993). Under ideal conditions, gs declines with decreasing Kl, resulting in near homeostatic regulation of leaf water potential at a constant value (Hubbard et al., 2001). It is thought that the mechanism for this regulation is a feedback response of the stomata to some aspect of leaf water status (an hydraulic signal), resulting in changes in gs that minimize fluctuations in leaf (Bond and Kavanagh, 1999; Hubbard et al., 2001). In the present study the mechanism was not a feedback response to bulk Eleaf or leaf because these variables differed between the rootstocks. leaf differed significantly between rootstocks and was not correlated with gs. The stomata may instead have been responding to some other aspect of leaf water status, or to an unknown chemical signal exchanged between the rootstock and scion. Regardless of the mechanism involved, the changes in leaf photosynthesis and carbon isotope composition and their relationship with Kl suggest a consistent, long-term stomatal response to a change in vine hydraulic architecture caused by the rootstock. If the mechanism does involve a chemical signal then it may also be relatively conserved between genotypes. The rootstocks used in this study were from four different species belonging to two sections of the genus Actinidia (Leiocarpae and Strigosae) with widely different geographical distributions within eastern Asia. The scion was a clone from a fifth species and a separate section (Stellatae) (Ferguson, 1990). Further experiments with these rootstocks will include comparisons of xylem sap composition and the possible nature of xylem transported signals passed from the rootstock to the scion.
Hydraulic architecture and the rootstock effect
In the low-vigour A. kolomikta and A. polygama rootstocks, total leaf area was reduced by approximately 70% compared with the vigorous stocks, but hydraulic conductance (Kplant) by only 55%. Hydraulic conductance per unit leaf area (Kl,plant) was therefore increased. Atkinson et al. (2003) proposed that low graft union conductance provided a mechanistic explanation for the effect of dwarfing rootstocks in apple. In the present study, a destructive harvest was not possible and the conductance of the graft union could not be measured in isolation. Calculations of Ks,plant for the scion main stem show significant differences because rootstock effects on stem diameter were not in proportion with changes in Kplant (lower Kplant but increased sapwood area with the low-vigour stocks). However, the sapwood of these Actinidia species, as with other lianas, is highly porous with large diameter vessels (Dichio et al., 1999; Clearwater and Clark, 2003). The conductance of the stem from the leader to the mid-canopy was an order of magnitude higher than the conductance of the leaves or roots (Tables 3, 4), and the main stem also probably contributes only a small proportion to overall resistance and any differences in Kplant between rootstocks. The same pattern is found in ungrafted plants of other species, with the largest resistance often found in the roots (Sperry et al., 2002). Therefore, low Ks in the low-vigour rootstocks is not reliable evidence that changes in the anatomy or conductance of the main stem were important components of the rootstock effects. Furthermore, if a change in hydraulic conductance of the graft union or main stem was the primary mechanism for Actinidia rootstock effects, equal or reduced Kl,plant would be expected in the low-vigour rootstocks, as observed for the dwarfing apple rootstocks (Cohen and Naor, 2002; Atkinson et al., 2003). Alternative explanations must therefore be sought for the effect of these rootstocks on scion behaviour.
The high Kl,soil-stem and gs of the scion growing on the A. polygama rootstock suggest an increase in root hydraulic capacity relative to shoot leaf area. Leaf-specific conductance differed in the soil to stem portion (Kl,soil-stem) of the pathway, rather than in the stems and leaves (Kl,stem-shoot and Kl,leaf) of the scion. The most significant resistance in the pathway from soil to main stem is likely to be the roots (Sperry et al., 2002). Less negative stem also indicates that the root conductance of the A. polygama rootstock was high compared with the rate of transpiration, despite the increase in gs. Root conductance should be a function of root biomass and root conductance per unit biomass. Species with high root conductance tend to be faster growing and produce roots with a higher surface area or length per unit dry mass (Tyree et al., 1998; Comas et al., 2002). There are also trade-offs between root morphology, anatomy, and root longevity, with faster turnover expected in high-conductance species (Eissenstat, 1997). It is therefore possible that the grafting of A. chinensis onto the A. polygama stock resulted in an increased proportion of total carbon gain being allocated to the roots. Root respiration, root turnover, or partitioning to total root biomass may be higher with the A. polygama rootstock relative to the supported leaf area. Further measurements are needed to determine if there is a causal relationship between carbon partitioning to roots and reductions in vigour of the scion.
Of the four rootstocks, A. kolomikta caused the most extreme reduction in scion leaf area index and plant size, and had the most negative water potentials. The results for this rootstock illustrate the need to consider changes in crown architecture when interpreting leaf level responses to changes in plant hydraulic architecture (Meinzer et al., 1993). The Ohm’s law analogy used in this study simplifies the crown into two resistors connected in series (the stems and leaves), when in fact it represents a complex series parallel network. A change in the distribution of flow through this network affects the interpretation of estimates of hydraulic conductance. To illustrate this effect, consider Equation 5 and the linear relationship between Kl,soil-stem and gs (Fig. 6B). For stem to be significantly more negative with A. kolomikta then Dl must also have increased, otherwise there would not have been a linear relationship between Kl,soil-stem and gs across the different rootstocks. With A. kolomikta the LAI was low, a higher proportion of leaves must have been exposed to direct sunlight, Eleaf was higher, and it was therefore concluded that the effective average driving force for transpiration across all leaves (Dl) was increased. Boundary layer conductance may also be lower with a more open crown, thus further increasing transpiration. Although calculated Kl,plant was higher with A. kolomikta, these vines may still have been limited by the hydraulic capacity of their roots. The low Kg plant value for A. kolomikta (Table 4) illustrates this potential limitation, with hydraulic capacity reduced relative to crown projected-area. Cohen and Naor (2002) also found that Kg was lower in apple trees with dwarfing rootstocks. In both examples, plant size and leaf area per plant were reduced in low-vigour plants, but they had a high potential evaporative demand and occupied more space relative to their hydraulic capacity. The cause of low root conductance and open crown structure with the A. kolomikta rootstock is not known, but it is possible that the phenology of this rootstock contrasts more strongly with that of the scion than the other rootstocks. A. kolomikta is naturally distributed in more northern latitudes and higher altitudes in north-east Asia than the scion and other rootstocks (Liang, 1983). Ongoing measurements are now testing whether shoot growth in spring is limited by root function and plant water status.
The vigour of the A. macrosperma and A. hemsleyana stocks was associated with faster scion shoot and leaf development in spring and a higher proportion of non-terminating extension shoots. The resulting high leaf area was supported by high hydraulic conductance (Kplant). Huber values were low and Ks,plant values were high, indicating roots and stem with high hydraulic conductance and high sap flux relative to stem diameter. Kl,plant was reduced in these stocks, but because of the high LAI the proportion of self-shaded leaves was probably higher, and Kg,plant was equivalent or higher than the low-vigour rootstocks. Compared with other species, Kl,plant for these vines are comparable with those for annual crops and some other temperate deciduous woody plants (Tsuda and Tyree, 1997, 2000), and high compared with some temperate evergreen trees (Phillips et al., 2002). There were also consistent differences between the two high-vigour stocks. Scions on A. hemsleyana had a higher LAI than on A. macrosperma, and overall plant size and K were higher. Final leaf area and crown size was lower with the A. macrosperma stock, but shoot growth in spring was still relatively rapid. Fast initial canopy development, but a reduction in overall vigour, is of practical interest because of the expense of controlling summer vegetative growth in commercial Actinidia orchards. However, overall hydraulic conductance on a leaf area or crown area basis was similar with the two vigorous Actinidia stocks, indicating that with vigorous rootstock–scion combinations leaf area development was well co-ordinated with root and stem hydraulic capacity.
There were no clear differences in leaf photosynthetic capacity between rootstocks during midsummer, although there were clear reductions in SLA and the rate of leaf expansion during spring in the low-vigour stocks. The similarity in photosynthetic capacity between stocks shows that changes in leaf properties on their own are unlikely to provide a direct explanation for rootstock effects in kiwifruit. Primarily because of higher gs, the rate of ambient photosynthesis by sunlit leaves was higher with both the low-vigour stocks. This result contrasts with some of the effects of rootstocks on photosynthesis in other fruit crops. In citrus, root conductance and leaf gas exchange by rootstock seedlings were positively correlated with the vigour imparted to the scion (Syvertsen and Graham, 1985). In apple it has been suggested that some of the effect of dwarfing rootstocks is through hydraulic effects on water transport and, ultimately, the rate of photosynthesis (Cohen and Naor, 2002). In this study the rate of photosynthesis of sunlit leaves was lower in the high-vigour rootstocks, but whole-plant carbon gain was probably higher because of the higher LAI and crown area.
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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Partitioning of hydraulic resistance between the roots, stems, and leaves of grafted Actinidia plants showed that the largest resistances (lowest conductance) to flow were found in the roots and leaves. As there were no significant differences in Kl of the upper stems and leaves, overall differences in hydraulic architecture between the grafted plants were dominated by the effect of the rootstocks. Kl,soil-stem was increased with the low-vigour rootstocks, suggesting that low root or stem hydraulic conductance is not a primary mechanism for vigour reduction with these Actinidia rootstocks. The differences in stomatal conductance of the scion reflected differences in hydraulic architecture between rootstock. The differences in the hydraulic architecture of these plants did indicate, however, that the observed rootstock effects are at least linked to changes in crown structure and biomass partitioning to the roots.
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Steve Green provided help and advice with sap flow measurements, David Logan helped with drawing, and Murray Judd and Bill Snelgar provided valuable comments on an early version of this paper. This work was funded by the NZ Foundation for Research, Science and Technology (Contract C06X0202)
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Atkinson CJ, Else MA. 2001. Understanding how rootstocks dwarf fruit trees. The Compact Fruit Tree 34, 46–49.
Atkinson CJ, Else MA, Taylor L, Dover CJ. 2003. Root and stem hydraulic conductivity as determinants of growth potential in grafted trees of apple (Malus pumila Mill.). Journal of Experimental Botany 54, 1221–1229.
Atkinson CJ, Policarpo M, Webster AD, Kingswell G. 2000. Drought tolerance of clonal Malus determined from measurements of stomatal conductance and leaf water potential. Tree Physiology 20, 557–563.[Abstract]
Beakbane AB. 1956. Possible mechanism of rootstock effect. Annals of Applied Biology 44, 517–521.[CrossRef]
Bond BJ, Kavanagh KL. 1999. Stomatal behavior of four woody species in relation to leaf-specific hydraulic conductance and threshold water potential. Tree Physiology 19, 503–510.[Abstract]
Campbell GS. 1990. Derivation of an angle density function for canopies with ellipsoidal leaf angle distributions. Agricultural and Forest Meteorology 49, 173–176.[CrossRef][Web of Science]
Castle WS. 1995. Rootstock as a fruit quality factor in citrus and deciduous tree crops. New Zealand Journal of Crop and Horticultural Science 23, 383–394.[Web of Science]
Clearwater MJ, Clark CJ. 2003. In vivo magnetic resonance imaging of xylem vessel contents in woody lianas. Plant, Cell and Environment 26, 1205–1214.[CrossRef]
Cohen S, Naor A. 2002. The effect of three rootstocks on water use, canopy conductance, and hydraulic parameters of apple trees and predicting canopy from hydraulic conductance. Plant, Cell and Environment 25, 17–28.[CrossRef]
Comas LH, Bouma TJ, Eissenstat DM. 2002. Linking root traits to potential growth rate in six temperate tree species. Oecologia 132, 34–43.[CrossRef][Web of Science]
Cruz CJ, Lawes GS, Woolley DJ, Ganesh S. 1997. Evaluation of rootstock and ‘Hayward’ scion effects on field performance of kiwifruit vines using a multivariate analysis technique. New Zealand Journal of Crop and Horticultural Science 25, 273–282.[Web of Science]
Dichio B, Baldassarre R, Nuzzo V, Biasi R, Xiloyannis C. 1999. Hydraulic conductivity and xylem structure in young kiwifruit vines. Acta Horticulturae 498, 159–164.
Eissenstat DM. 1997. Trade-offs in root form and function. In: Jackson LE, ed. Ecology in agriculture. San Diego: Academic Press, 173–199.
Farquhar GD, Ball MC, Von Caemmerer S, Roksandic Z. 1982. Effect of salinity and humidity on the 13C value of halophytes: evidence for diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions. Oecologia 52, 121–124.[CrossRef][Web of Science]
Ferguson AR. 1990. The genus Actinidia. In: Warrington IJ, Weston GC, eds. Kiwifruit: science and management. Auckland: New Zealand Society for Horticultural Science and Ray Richards Publisher, 15–35.
Ferguson AR, Retamales J. 1999. Kiwifruit cultivars: breeding and selection. Acta Horticulturae 498, 43–51.
Green SR, Clothier BE, Jardine B. 2003. Theory and practical application of heat pulse to measure sap flow. Agronomy Journal 95, 1371–1379.
Higgs KH, Jones HG. 1990. Response of apple rootstocks to irrigation in south-east England. Journal of Horticultural Science 65, 129–141.[Web of Science]
Hubbard RM, Ryan MG, Stiller V, Sperry JS. 2001. Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell and Environment 24, 113–121.
Jones OP. 1976. Effect of dwarfing interstocks on xylem sap composition in apple trees: effect on nitrogen, potassium, phosphorus, calcium, and magnesium content. Annals of Botany 40, 1231–1235.
Jones OP. 1986. Endogenous growth regulators and rootstock/scion interactions in apple and cherry trees. Acta Horticulturae 177, 179–184.
Kamboj JS, Blake PS, Quinlan JD, Baker DA. 1999. Identification and quantitation by GC-MS of zeatin and zeatin riboside in xylem sap from rootstock and scion of grafted apple trees. Plant Growth Regulation 28, 199–205.[CrossRef][Web of Science]
Liang CF. 1983. On the distribution of Actinidias. Guihaia 3, 229–248.
Meinzer FC. 2002. Co-ordination of vapour and liquid phase water transport properties in plants. Plant, Cell and Environment 25, 265–274.[CrossRef][Medline]
Meinzer FC, Clearwater MJ, Goldstein G. 2001. Water transport in trees: current perspectives, new insights and some controversies. Environmental and Experimental Botany 45, 239–262.[CrossRef][Web of Science][Medline]
Meinzer FC, Goldstein G, Grantz DA. 1993. Carbon isotope discrimination and gas exchange in coffee during adjustment to different soil moisture regimes. Stable isotopes and plant carbon-water relations. Academic Press, 327–345.
Miller SA, Broom FD, Thorp TG, Barnett AM. 2001. Effects of leader pruning on vine architecture, productivity and fruit quality in kiwifruit (Actinidia deliciosa cv. Hayward). Scientia Horticulturaee 91, 189–199.[CrossRef]
Norman JM, Campbell GS. 1989. Canopy structure. In: Pearcy RW et al., eds. Plant physiological ecology. Field methods and instrumentation. London: Chapman and Hall, 301–325.
Ogren E, Evans JR. 1993. Photosynthetic light-response curves. 1. The influence of CO2 partial-pressure and leaf inversion. Planta 189, 182–190.[Web of Science]
Olien WC, Lakso AN. 1986. Effect of rootstock on apple (Malus domestica) tree water relations. Physiologia Plantarum 67, 421–430.[CrossRef]
Pataki DE, Oren R, Phillips N. 1998. Responses of sap flux and stomatal conductance of Pinus taeda L. trees to stepwise reductions in leaf area. Journal of Experimental Botany 49, 871–878.
Phillips N, Bond BJ, McDowell NG, Ryan MG. 2002. Canopy and hydraulic conductance in young, mature and old Douglas-fir trees. Tree Physiology 22, 205–211.[Abstract]
Simons RK. 1986. Graft-union characteristics as related to dwarfing in apple (Malus domestica Borkh.). Acta Horticulturae 160, 57–66.
Sorce C, Massai R, Picciarelli P, Lorenzi R. 2002. Hormonal relationships in xylem sap of grafted and ungrafted Prunus rootstocks. Scientia Horticulturae 93, 333–342.[CrossRef]
Soumelidou K, Battey NH, John P, Barnett JR. 1994a. The anatomy of the developing bud union and its relationship to dwarfing in apple. Annals of Botany 74, 605–611.
Soumelidou K, Morris DA, Battey NH, Barnett JR, John P. 1994b. Auxin transport capacity in relation to the dwarfing effect of apple rootstocks. Journal of Horticultural Science 69, 719–725.[Web of Science]
Sperry JS. 2000. Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13–23.[CrossRef][Web of Science]
Sperry JS, Alder NN, Eastlack SE. 1993. The effect of reduced hydraulic conductance on stomatal conductance and xylem cavitation. Journal of Experimental Botany 44, 1075–1082.
Sperry JS, Hacke UG, Oren R, Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant, Cell and Environment 25, 251–263.[CrossRef][Medline]
Syvertsen JP. 1981. Hydraulic conductivity of four commercial citrus rootstocks. Journal of the American Society for Horticultural Science 106, 378–381.[Web of Science]
Syvertsen JP, Graham JH. 1985. Hydraulic conductivity of roots, mineral nutrition, and leaf gas exchange of citrus rootstocks. Journal of the American Society for Horticultural Science 110, 865–869.[Web of Science]
Tsuda M, Tyree MT. 1997. Whole-plant hydraulic resistance and vulnerability segmentation in Acer saccharinum. Tree Physiology 17, 351–357.[Abstract]
Tsuda M, Tyree MT. 2000. Plant hydraulic conductance measured by the high pressure flow meter in crop plants. Journal of Experimental Botany 51, 823–828.
Tyree MT, Velez V, Dalling JW. 1998. Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia 114, 293–298.[CrossRef][Web of Science]
Viti R, Xiloyannis C, Trinci M, Ragone AF. 1990. Effect of calcareous soil on vegetative growth of ownrooted and grafted kiwifruit trees. Acta Horticulturae 282, 209–216.
von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta 153, 376–387.[CrossRef][Web of Science]
Wang ZY, Gould KS, Patterson KJ. 1994a. Comparative root anatomy of 5 actinidia species in relation to rootstock effects on kiwifruit flowering. Annals of Botany 73, 403–413.
Wang ZY, Patterson KJ, Gould KS, Lowe RG. 1994b. Rootstock effects on budburst and flowering in kiwifruit. Scientia Horticulturae 57, 187–199.[CrossRef]
Webster AD. 1995. Rootstock and interstock effects on deciduous fruit tree vigour, precocity, and yield productivity. New Zealand Journal of Crop and Horticultural Science 23, 373–382.[Web of Science]
Whitehead D, Livingston NJ, Kelliher FM, Hogan KP, Pepin S, McSeveny TM, Byers JN. 1996. Response of transpiration and photosynthesis to a transient change in illuminated foliage area for a Pinus radiata D. Don tree. Plant, Cell and Environment 19, 949–957.[CrossRef]
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