Journal of Experimental Botany, Vol. 52, No. 359, pp. 1323-1330,
June 1, 2001
© 2001 Oxford University Press
Original Papers |
Limitations to photosynthesis of lettuce grown under tropical conditions: alleviation by root-zone cooling
1 Natural Sciences Academic Group, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore 637616
2 Department of Botany, The University of Queensland, St Lucia 4072, Australia
Received 4 December 2000; Accepted 7 February 2001
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Abstract |
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Aerial parts of lettuce plants were grown under natural tropical fluctuating ambient temperatures, but with their roots exposed to two different root-zone temperatures (RZTs): a constant 20 °C-RZT and a fluctuating ambient (A-) RZT from 23–40 °C. Plants grown at A-RZT showed lower photosynthetic CO2 assimilation (A), stomatal conductance (gs), midday leaf relative water content (RWC), and chlorophyll fluorescence ratio Fv/Fm than 20 °C-RZT plants on both sunny and cloudy days. Substantial midday depression of A and gs occurred on both sunny and cloudy days in both RZT treatments, although Fv/Fm did not vary diurnally on cloudy days. Reciprocal temperature transfer experiments investigated the occurrence and possible causes of stomatal and non-stomatal limitations of photosynthesis. For both temperature transfers, light-saturated stomatal conductance (gs sat) and photosynthetic CO2 assimilation (Asat) were highly correlated with each other and with midday RWC, suggesting that A was limited by water stress-mediated stomatal closure. However, prolonged growth at A-RZT reduced light- and CO2-saturated photosynthetic O2 evolution (Pmax), indicating non-stomatal limitation of photosynthesis. Tight temporal coupling of leaf nitrogen content and Pmax during both temperature transfers suggested that decreased nutrient status caused this non-stomatal limitation of photosynthesis.
Key words: Lactuca sativa L., root-zone temperature, photosynthetic CO2 assimilation, stomatal conductance, relative water content.
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Introduction |
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The tropical climate of Singapore, which is non-seasonal, hot and humid, is not suitable for growing temperate crops. However, lettuce has been successfully grown in an aeroponics system by exposing the roots to cool temperatures (15–25 °C) while shoots were maintained at hot ambient temperatures (Lee and Cheong, 1996
; He and Lee, 1998a, b). Both the formation of compact heads and the growth and development of root and shoot were affected by root-zone temperature (RZT) (He and Lee, 1998a, b). However, the effect of RZT on photosynthesis of temperate lettuce under tropical conditions has not been investigated.
Limitations of photosynthesis by supra-optimal RZT are usually ascribed to stomatal closure (Behboudian et al., 1994; Du and Tachibana, 1994a) depleting carbon dioxide in the intercellular spaces and at the chloroplast level. Such closure may result from water stress, as supra-optimal RZT can alter the balance between water uptake by the root system and water loss from the shoot. Although the roots of aeroponically grown plants are frequently sprayed with nutrient mist, poor root system development at high RZT (He and Lee, 1998a, b) may cause transient water deficits.
Severe water deficits (relative water content <70%) may also reduce photosynthesis by non-stomatal mechanisms, as diagnosed by decreases in the chlorophyll fluorescence ratio Fv/Fm, or decreased light- and CO2-saturated photosynthetic O2 evolution (Pmax) (Kaiser, 1987). Such non-stomatal effects are exacerbated by additional stresses such as high temperature and high irradiance (Björkman and Powles, 1984) or nutrient deficiency (Verhoeven et al., 1997). Plants grown at high root temperatures often show decreased nutrient concentrations (Du and Tachibana, 1994b).
The aims of this study were to determine whether photosynthesis of plants grown at high RZTs was limited by stomatal or non-stomatal factors, and to determine whether water deficit or nutrient stress could account for these limitations. Leaf relative water content and nitrogen content were measured as they closely correlate with photosynthetic capacity (Kaiser, 1987; Field and Mooney, 1986). Since photosynthesis of plants grown for prolonged periods at supra-optimal RZT may be co-limited by both water and nutrient stresses, reciprocal RZT transfer experiments investigated the timing and impact of these stresses on stomatal and non-stomatal limitation of photosynthesis. The effect of diurnal variations in PPFD on photosynthesis of plants at different RZTs was first assessed on days of differing PPFD. Understanding the causes of photosynthetic limitation in plants at different RZTs will assist in management procedures aimed at reducing the root cooling requirements of temperate crops in the tropics.
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Materials and methods |
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Plant materials and cultural methods
Butterhead lettuce (Lactuca sativa L. cv. Palma) seeds were germinated on moist Whatman filter papers (No. 3) in Petri dishes. After 3 d, seedlings were transplanted onto polyurethane cubes soaked with water and placed in trays in the greenhouse. After two more days to allow seedling establishment, they were transplanted to aeroponics troughs (Lee, 1993
) in a greenhouse at Nanyang Technological University, Singapore. The top of each trough was insulated by sheets of polystyrofoam on which the plants were anchored. Full-strength Netherlands Standard Composition (Douglas, 1982) nutrient solution (conductivity=2.2 mS) was used. Details of the root temperature control system have been previously published (Lee, 1993).
Reciprocal transfer between RZTs
RZT transfer experiments were conducted 3 weeks after transplanting and all measurements were made over the ensuing 10 d. Half the plants were maintained at their original RZT (either 20 °C-RZT or A-RZT), and the other half were transferred to the other RZT at 07.00 h. There were thus four RZT treatments: 20 °C-RZT, A-RZT, 20 °C
A-RZT and A20 °C-RZT. The RZT transfer experiment was performed twice at different times of the year with similar results; results are presented from only one experiment. All leaf measurements used the fourth leaf from the base.
Measurement of environmental variables and photosynthetic parameters in vivo
Three weeks after transplanting, diurnal changes in A and gs were measured in the greenhouse for three clear sunny and three cloudy days between 07.00 h and 19.00 h with a portable open system gas analyser (CIRAS-1, PP-system, Hitchin, Herts, UK). A leaf area of 2.5 cm2 was used to determine A and gs under prevailing solar radiation. PPFD and ambient and leaf temperatures were also measured concurrently with the quantum sensor and thermistors on the CIRAS-1.
In the RZT transition experiments, light-saturated photosynthetic CO2 assimilation (Asat) and stomatal conductance (gs sat) of attached leaves were measured simultaneously between 10.30–11.00 h in the greenhouse with a PPFD of 1350 µmol m–2 s–1 supplied from a metal halide lamp (Wotan 12 V 100 W bulb). Light response curves of both CO2 fixation and O2 evolution (measured in the laboratory at 25 °C at saturating CO2 conditions) had previously established that a PPFD of 1350 µmol m-2 s-1 was saturating for lettuce leaf photosynthesis (data not shown), as in other studies (Caporn, 1989).
Measurement of photosynthetic oxygen evolution on detached leaves
To determine photosynthetic capacity (Pmax) in the absence of stomatal limitation, five leaves were harvested from five different plants between 11.00–11.10 h and brought back to the laboratory. Leaves were then kept in a tray of distilled water under a PPFD of 1350 µmol m-2 s-1 for 30 min. Rates of maximum photosynthetic O2 exchange were determined with a leaf disc O2 electrode (Hansatech, King's Lynn, UK) under a PPFD of 1350 µmol m-2 s-1 at 25 °C at saturating CO2 conditions (1% CO2 from a 1 M carbonate/bicarbonate buffer, pH 9) as described earlier (Ball et al., 1987).
Measurement of chlorophyll fluorescence
All measurements of chlorophyll fluorescence were made with a portable fluorometer (PAM-2000, Walz, Effeltrich, Germany) on attached leaves, immediately following the gas-exchange measurements. A personal computer equipped with DA-2000 software (Walz) was used for data acquisition. To measure Fv/Fm ratio, DLC-8 aluminum leaf clips (2 cm diameter, Walz) were used to pre-darken (15 min) leaves prior to measurement and to enable vertical positioning of the PAM fibre optics with respect to the leaf surface. Leaves from both 20 °C-RZT and A-RZT plants were tested for dark adaptation by using different dark periods from 5–30 min (5 min intervals). The recovery of Fv/Fm in light-grown leaves after exposure to darkness for various periods showed that a 15 min dark adaptation was adequate (data not shown). After dark adaptation for 15 min, leaves were initially exposed to a weak measuring beam to estimate minimal fluorescence (Fo), then a 0.8 s saturation pulse (3000 µmol m-2 s-1) to obtain maximal fluorescence (Fm). Preliminary experiments measured Fm with both 3000 and 6000 µmol m-2 s-1 pulses, and found no effect of the intensity of the pulse (data not shown). Therefore, a saturating pulse of white light of 3000 µmol m-2 s-1 was used.
Measurement of leaf relative water contents
Ten leaf discs of 1 cm diameter were cut and immediately weighed with an analytical balance for the field fresh weight. The leaf discs were then floated on distilled water in the dark for 24 h to determine their turgid weight. Dry weights were obtained after wrapping the leaf discs in aluminium foil and oven-drying at 80 °C for 48 h. RWC was determined as: (fresh weight-oven dry weight)/(turgid weight-oven dry weight)x100.
Measurement of leaf nitrogen content
Dried leaf samples were weighed and placed in a digestion tube with Kjeldahl tablet and 5 ml of concentrated sulphuric acid (H2SO4) (Allen, 1989). The mixture was heated at 250 °C until it turned clear, then total N content was determined using a Kjeltec Auto 1030 Analyser.
Statistical analysis
Differences between RZT treatments were discriminated using Dunnett's procedure at P<0.05. The significance of correlations between plant and environmental variables was tested in JMP In (SAS Institute Inc., Cary, NC, USA).
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Results |
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Photosynthesis, stomatal conductance and water relations during a sunny and a cloudy day
On a clear and hot day, ambient greenhouse PPFD and temperature reached maxima of 1800 µmol m-2 s-1 and 38 °C, respectively (Fig. 1a
, b). Leaf temperatures of 20 °C-RZT plants during the middle of the day were 2–4 °C lower than A-RZT plants (Fig. 1b). Maximum leaf temperatures of 20 °C-RZT and A-RZT plants were 40.6 °C and 42.8 °C, respectively, at 13.00 h. Although A, gs and Fv/Fm were lower in A-RZT plants, the diurnal patterns of these variables were similar at both RZTs, with substantial midday depression occurring (Fig. 1c, d, e). There was no diurnal change in Fo at either RZT (data not shown). Mid-morning maxima and subsequent declines of A and gs occurred c. 2 h earlier in A-RZT plants. In plants at both RZTs, A correlated very well with gs (cf. Fig. 1c, d).
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) and A-RZT (•) on a representative sunny (a–e) and a representative cloudy (f–j) day. Each point is the mean±standard error of five measurements on leaf 4 from five different plants.Following three consecutive bright sunny days, diurnal changes in environmental and plant variables were also measured on a cloudy day (Fig. 1f
–j). Ambient greenhouse PPFD and temperature reached afternoon maxima of 230 µmol m-2 s-1 and 35 °C, respectively (Fig. 1f, g). Leaf temperatures of 20 °C-RZT plants were no more than 2 °C lower than A-RZT plants. Although gs showed a similar diurnal pattern to that seen on sunny days (Fig. 1i), A remained relatively stable from 10.00–16.00 h (Fig. 1h). No diurnal variation of Fv/Fm was seen (Fig. 1j). Again, A, gs and Fv/Fm were lower in A-RZT plants.
The extent of midday depression of A and gs on three sunny (maximum PPFD c. 1800 µmol m-2 s-1) and three cloudy (maximum PPFD<250 µmol m-2 s-1) days is summarized (Table 1 ). On sunny days, midday depression of A and gs were similar in magnitude, and 20–30% greater in A-RZT plants. On cloudy days, the midday depression of A (30%) was much less than the depression of gs (70%). RZT had no effect on the magnitude of midday depression of A and gs on cloudy days.
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Leaf RWC of A-RZT plants was lower than 20 °C-RZT plants on any measurement occasion (Table 2
). Pre-dawn RWC was 3–6% and 29% higher than midday RWC in 20 °C-RZT and A-RZT plants, respectively. The lower pre-dawn RWC of A-RZT plants than 20 °C-RZT plants suggested some residual water stress. However, floating A-RZT plants on a beaker of nutrient solution in a water-saturated atmosphere in the laboratory also gave a similar RWC (data not shown). In both determinations, the leaf discs changed colour when floated on distilled water to determine their turgid weight, suggesting water infiltration of air spaces. Attempts at removing this water by vacuum prior to the measurement of turgid weight were unsuccessful (the vacuum also removed cellular water from the discs resulting in turgid weights which were less than the fresh weights). Leaves of A-RZT plants have a greater volume of air spaces than 20 °C-RZT plants (Flanigan, 1999) and thus the relative increase in turgid weight will be greater. The difference in pre-dawn RWC between RZT treatments therefore reflects differences in leaf anatomy, rather than the development of water stress in the A-RZT plants. Measurement of cellular turgor using the pressure probe will be necessary to confirm this.
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Experiments of reciprocal transfer between RZTs
Midday leaf RWC did not fluctuate with prevailing PPFD (Fig. 2a, b). Average RWC of 20 °C-RZT and A-RZT plants were 90% and 53%, respectively (Fig. 2b). In 20 °CA-RZT plants, RWC decreased from the first day of RZT transfer (P<0.05) and continued to decrease throughout the experiment. RWC of A20 °C-RZT plants did not change for 3 d after RZT transfer, although RWC had increased to 87% after 10 d (Fig. 2b). Both sets of transferred plants showed a similar RWC 5 d after transfer.
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) and those grown at A-RZT transferred to 20 °C-RZT (
). All measurements were made between 12.30–13.00 h. Each point is the mean±standard error of five measurements.Leaf N content was 32% lower in A-RZT plants than 20 °C-RZT plants (Fig. 2c
). While leaf N content remained stable in plants maintained at the one RZT, transfer of plants between RZTs altered N content after 6 d. At the end of the experiment, A20 °C-RZT plants and 20 °CA-RZT plants had a similar leaf N content (Fig. 2c).
To prevent changes in PPFD obscuring any acclimation of plants to altered RZT during the 10 d period, all photosynthetic measurements (gs, A, Pmax) were performed under light-saturating (PPFD=1350 µmol m-2 s-1) conditions. Plants were maintained in the greenhouse at different RZTs while gs sat and Asat were measured. Plants maintained at the one RZT showed constant gs sat and Asat of attached leaves, with both parameters being c. 70% lower in A-RZT plants (Fig. 3a, b). When plants were transferred from 20 °C-RZT to A-RZT, gs sat and Asat significantly (P<0.05) decreased from the first day of RZT transfer. gs sat and Asat of A20 °C-RZT plants was similar to A-RZT plants during the first 3 d post-transfer, and then gradually increased. Parity of Asat and gs sat in transferred plants was reached 5 d after transfer.
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Light- and CO2-saturated photosynthetic O2 evolution (Pmax) of detached leaves from plants remaining at one RZT was also constant during the 10 d period, with Pmax of A-RZT plants 37% lower than 20 °C-RZT plants (Fig. 3c
). Pmax did not significantly (P<0.05) decrease during the first 4 d post-transfer in 20 °CA-RZT plants, although it declined by 22% after 10 d. This decrease was much less than the decreases in Asat measured on attached leaves in the greenhouse (Fig. 3b). In A20 °C-RZT plants, Pmax gradually increased from 3 d post-transfer and was statistically equivalent to 20 °C-RZT plants 10 d after the RZT transfer. Parity of Pmax in transferred plants was reached 8 d after transfer.
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Discussion |
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Although the shoot environment of all plants was identical, cooling the roots to 20 °C-RZT allowed higher assimilation rates by reducing both photoinhibition and stomatal closure.
On cloudy days, there was no dynamic high PFFD-induced photoinhibition at either RZT. However, chronic photoinhibition of A-RZT plants was indicated by their lower Fv/Fm (Fig. 1j) and decreased chlorophyll content (data not shown) compared to 20 °C-RZT plants. Such chlorophyll loss seems to be a photoprotective strategy to reduce light absorption (Verhoeven et al., 1997) rather than high light-induced chlorophyll oxidation, since no increase in Fo (characteristic of photodamage) (Osmond, 1994) was detected.
On sunny days, high PPFD–induced dynamic photoinhibition was entirely attributable to decreased Fm. The relative changes in Fv/Fm were less than the relative changes in A (Fig. 1c, e) suggesting that although photoinhibition contributed to the midday depression of A, there was an additional effect of stomatal closure.
Studying the dynamic responses of A and gs to environmental perturbations may help separate the interrelationships between A and gs (Jones, 1998). Irrespective of RZT, diurnal studies showed highly significant (P<0.05) correlations between A and gs on both cloudy and sunny days. However, there was a clear example where the diurnal responses of A and gs were de-coupled. Between 10.00 h and 16.00 h on cloudy days, plants at both RZTs showed substantial midday stomatal closure which was unaccompanied by reductions in A (cf. Fig. 1h, i), indicating that stomatal behaviour was independent of A at low PPFD.
Pronounced midday stomatal closure occurred in 20 °C-RZT plants (Fig. 1d, i) despite midday leaf RWC being 90% (Fig. 2b). This would seem to exclude leaf water deficit as an explanation, although localized water deficit related to high transpiration rates could still occur. The importance of temperature and VPD on the relative magnitude of midday stomatal closure varied with RZT. In 20 °C-RZT plants, the greater magnitude of midday stomatal closure on cloudy days than sunny days (Table 1) seems inconsistent with the lower temperature and VPD on cloudy days. In A-RZT plants, the higher leaf temperatures (Fig. 1b) and greater midday stomatal closure (Table 1) on sunny days suggested that temperature (or some co-variate such as higher VPD or increased ABA delivery to the stomata) had an additional effect on midday stomatal closure. Separating the effects of temperature and VPD on midday stomatal closure would require controlled environment facilities to examine the effects of one variable while keeping the other constant (Roessler and Monson, 1985).
The greater midday stomatal closure of A-RZT plants on sunny days is characteristic of droughted plants (Tenhunen et al., 1981). That shoot water deficits occurred in A-RZT plants is indicated by their very low midday leaf RWC (Fig. 2b), even though root water contents remained greater than 94% (data not shown) due to frequent misting of the root system with nutrient solution. Leaf RWC recovered overnight (Table 2), suggesting that transient water deficits occurred during the day in A-RZT plants due to a diurnal imbalance of transpiration and root water uptake. Temperature-induced alterations in root morphology (He and Lee, 1998a) are likely to decrease root hydraulic conductivity (Lp) (Dodd et al., 2000), resulting in the development of water stress under high transpiration rates in the middle of the day. The transfer experiment showed that RZT-induced differences in midday RWC were readily reversible over a 10 d period (Fig. 2b); presumably due to reduced root hydraulic conductivity (Lp) in 20 °CA-RZT plants (Dodd et al., 2000) and the initiation of new roots in A20 °C-RZT plants (LP Tan, J He and SK Lee, unpublished observations). The contributions of RZT-induced anatomical and physiological alterations in Lp would merit future investigation in this aeroponics system, especially given the apparent dependence of lettuce shoot physiology on RWC (Fig. 4).
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The highly significant (P<0.05) correlations between gs sat and RWC in both temperature transfers (Fig. 4a
) suggested that stomatal closure was directly caused by reduced RWC. In contrast, lettuce grown in soil columns where the upper layer was allowed to dry showed up to a 90% decline in gs while RWC changed by only 5% (Gallardo et al., 1996), suggesting additional effects of a root-derived chemical signal such as ABA (Davies and Zhang, 1991).
The close correlation between gs sat and Asat in plants transferred between RZTs suggests a stomatal limitation of photosynthesis. Stomatal closure decreases intercellular CO2 concentration (Ci) which then limits A. However, non-uniform stomatal closure under drought could overestimate Ci, thus suggesting non-stomatal limitation of photosynthesis when none existed (Farquhar et al., 1987). The possibility of non-uniform stomatal closure in 20 °CA-RZT plants cannot be excluded, as it occurred in droughted Phaseolus vulgaris plants subjected to a similar (although slower developing) water deficit (Sharkey and Seeman, 1989). Without knowing whether stomatal closure was uniform (which would validate measurement of Ci), an indirect method of determining non-stomatal limitation of photosynthesis (measuring photosynthesis under saturating CO2; Fig. 3c) was preferred.
Previous investigators have generally attributed negative effects of high RZT on A to stomatal closure (Behboudian et al., 1994). While this was certainly the initial response of 20 °CA-RZT plants, a shift to non-stomatal regulation of photosynthesis occurred as time progressed. This was evident in 20 °CA-RZT plants as a divergence from the Asat versus RWC relationship at RWC<70% (Fig. 4b). More conclusive evidence of non-stomatal limitation of photosynthesis in these plants was the decline in Pmax measured under saturating CO2 (Fig. 3c). An absence of severe water deficits in previous investigations may account for the lack of reports of non-stomatal effects of high RZT.
The relationship between RWC and Pmax in 20 °CA-RZT plants (Fig. 4c) accorded with that found in slowly dehydrated detached leaves of mesophytic plants (Kaiser, 1987). However, the lower Pmax of A20 °C-RZT plants compared to 20 °CA-RZT plants at RWC>70% (Fig. 4c), provided evidence of non-stomatal limitation of A that was not mediated by water deficit. It seems likely that nutrient deficiencies due to poor root development could be responsible for the declines in Pmax in A-RZT plants. Parallel analyses of leaf nitrogen content showed tight temporal coupling of leaf N content (Fig. 2c) and Pmax (Fig. 3c) throughout the reciprocal temperature transfers. A full evaluation of the role of N deficiency in mediating the decline in photosynthesis of A-RZT plants would require comparison with the photosynthetic responses of plants grown at 20 °C-RZT subjected to N deprivation.
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Conclusions |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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Plants transferred from 20 °C-RZT to A-RZT showed considerable stomatal limitation of photosynthesis as leaf RWC declined, with non-stomatal limitation occurring only when leaf nitrogen content decreased. In contrast, plants grown for prolonged periods at A-RZT showed non-stomatal limitation of photosynthesis which remained in A
20 °C-RZT plants even as leaf water relations improved. Future studies should focus on how A-RZT limits water and nutrient uptake. Temperature transfer experiments may have practical significance to tropical aeroponics production if plants can be established at one RZT and cropped at another, as a shorter period of time at cool RZTs would reduce cooling costs. However, this experiment suggests that unless lettuce plants are cooled to 20 °C-RZT after early crop establishment, yield penalties will result from the rapid limitation of photosynthesis.
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Acknowledgments |
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This project was supported by the Academic Research Fund, Ministry of Education, Singapore.
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Notes |
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3 To whom correspondence should be addressed. Fax: +65 896 9432. jhe{at}nie.edu.sg
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Abbreviations |
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A, photosynthetic CO2 assimilation; Asat, light-saturated photosynthetic assimilation; A-RZT, ambient root-zone temperature; A
20 °C-RZT, plants grown initially at A-RZT then transferred to 20 °C-RZT; Ci, internal CO2 concentration; Fo, minimal fluorescence yield of a dark-adapted sample; Fm and Fv, maximal and variable fluorescence yield obtained from a dark-adapted sample upon application of a saturating light pulse; Fv/Fm, dark-adapted ratio of variable to maximal fluorescence (the maximal photosystem II quantum yield without actinic light); gs, stomatal conductance; gs sat, stomatal conductance measured at a light intensity saturating for photosynthetic assimilation; Lp, root hydraulic conductivity; Pmax, light- and CO2-saturated photosynthetic O2 evolution; PPFD, photosynthetic photon flux density; RZT, root-zone temperature; RWC, relative water content; 20 °C-RZT, root-zone temperature of 20±2 °C; 20 °CA-RZT, plants grown initially at 20 °C-RZT then transferred to A-RZT; VPD, vapour pressure deficit. |
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