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CROP PHYSIOLOGY & METABOLISM

Diurnal and Seasonal Photosynthesis in Two Asparagus Cultivars with Contrasting Yield

^a Dep. of Plant and Microbial Sciences, Univ. of Canterbury, Private Bag 4800, Christchurch, New Zealand
^b New Zealand Institute of Crop and Food Research, P.O. Box 4704, Christchurch, New Zealand

* Corresponding author (m.turnbull{at}botn.canterbury.ac.nz)

	ABSTRACT

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To investigate physiological characters underpinning spear yield in asparagus (Asparagus officinalis L.), diurnal and seasonal changes in photosynthetic parameters were measured under field conditions in two cultivars with contrasting yield. Seasonal patterns in photosynthetic parameters were strongly dependent on cladophyll developmental stage in both cultivars. The greatest photosynthetic rates of 8.94 ± 0.54 µmol m^-2 s^-1 for the high-yielding cultivar (ASP-69) and 6.50 ± 0.38 µmol m^-2 s^-1 for the low-yielding cultivar (ASP-03) were observed in fully expanded cladophyll tissue measured in mid-summer (February) when both photon flux density (PFD) and temperature were at a maximum. A significant decline in net photosynthetic rate (A) was measured in April, when plants experienced colder night temperatures and shorter day lengths. A close correlation between A and stomatal conductance (g_s) (r = 0.84) was observed. Timing of cladophyll initiation and duration did not appear to be significant factors contributing to cultivar difference in photosynthesis. Variation in photosynthetic capacity between the two cultivars was related to significant differences in cladophyll thickness and specific leaf weight (SLW). The results substantiate the conclusion that both metabolic and anatomical factors play significant roles in determining differences in photosynthetic capacity between the two asparagus cultivars studied.

Abbreviations: A, net photosynthetic rate • A_max light saturated net photosynthetic rate • A_sat, light and CO₂ saturated net photosynthetic rate • C_a, atmospheric CO₂ concentration • C_i, intercellular CO₂ concentration • g_s, stomatal conductance • J_max potential rate of RuBP regeneration • L_stom, relative stomatal limitation on photosynthesis • R_d, dark respiration rate • SLW, specific leaf weight • V_cmax, maximum rate of carboxylation

	INTRODUCTION

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ALTHOUGH A POSITIVE RELATIONSHIP between plant assimilate production (photosynthetic rate) and crop productivity might be expected, findings of this nature are not common (Gifford and Evans, 1981; Daie, 1985; Evans, 1993; Lawlor, 1995). There are a number of likely reasons for this. First, photoassimilate may be partly invested to maximize leaf area rather than directly invested to photosynthetic capacity. In this case, assimilate production at the whole plant level is increased, but not with an increase in the unit area rate of photosynthesis (Stitt and Schulze, 1994). Second, a portion of assimilates may be wasted, i.e., allocated to other organs and not contribute to crop yield (Pooter and Remkes, 1990; Stitt and Schulze, 1994). The link, therefore, between photosynthetic rate and crop yield is modified by strategies of assimilate partitioning and utilization. Although the relationship between rate of CO₂ assimilation and crop yield has often been found to be decoupled, a positive correlation has been reported in a few cases (Zelitch, 1982; Peng et al., 1991; Masle, 1992; Farquhar and Sharkey, 1994; Pettigrew and Meredith, 1994; Fischer et al., 1998). Under some circumstances the correlation between photosynthetic rate and dry matter production measured under field conditions at different times of the crop growth is indeed strong (Chandra Babu et al., 1985; Pooter and Remkes, 1990; Pettigrew and Meredith, 1994).

Asparagus, unlike most crops, is perennial, and current photosynthesis does not directly contribute to spear yield. Annually, assimilate produced in summer is firstly translocated into storage roots and is subsequently utilized in vegetative growth during the next spring (Robb, 1984; Haynes, 1987; Pressman et al., 1993). It is, therefore, expected that storage roots may act as a physiological buffer between carbon assimilation in the fern phase and its utilization in spear development. From a physiological point of view, the three stages of fern development (carbon assimilation), winter dormancy (carbon storage), and spear development (carbon utilization) provide a model system to investigate carbon assimilation and its partitioning. Recently, Faville et al. (1999) reported a positive correlation between light saturated photosynthesis (A_max) and spear yield among three asparagus cultivars. This finding was later confirmed by Bai and Kelly (1999) who found that spear yield and rate of photosynthesis were significantly correlated among eight asparagus cultivars. These results suggest that genetic variation in photosynthetic capacity among asparagus cultivars may contribute to differences in spear yield.

In this study, we tested the hypothesis that cultivar variations in spear yield in asparagus are associated with carbon assimilation. One objective of this study was, therefore, to investigate diurnal and seasonal patterns of carbon assimilation under field conditions in two selected asparagus cultivars with significantly different yield. This is significant because the annual course of photosynthesis, and not maximum rate, determines annual plant carbon budget. The second aim of this study was to examine the relationship between photosynthetic capacity and parameters potentially limiting to photosynthesis. Specific attention was given to (i) effect of cladophyll age on photosynthetic capacity; (ii) the extent of stomatal and nonstomatal limitation to photosynthesis; (iii) causes of cultivar variation in photosynthetic capacity.

	MATERIALS AND METHODS

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Study Site and Plant Materials
Two asparagus clonal cultivars (ASP-69 and ASP-03) in a preexisting trial located at the Institute of Crop and Food Research, Christchurch, New Zealand, were selected for this study on the basis of differences in spear yield and morphology. A significant difference in spear yield between the two cultivars had been established for the previous 6 yr (W.A. Jermyn, unpublished data). ASP-03 is a low-yielding cultivar with small spears and short ferns. By contrast, ASP-69 is a high-yielding cultivar with large spears and ferns in comparison to ASP-03. Samples for determination of seasonal patterns were collected monthly between 1100 and 1300 h. Three plots for each cultivar were used to conduct this study. The mean maximum and minimum temperatures in January, February, and March averaged 22 and 12.6°C, respectively, and in April and May were 16.7 and 6.7°C, respectively. The total monthly precipitation received increased from January (36.2 mm) to March (56.1 mm) and then decreased in April (36.3 mm) and May (23.6 mm). The mean monthly day–night length declined slightly from January (14.9–9.1 h) to March (12.5–11.5 h) and more in April (10.8–13.2 h) and May (9.6–14.4 h).

CO₂ Assimilation Measurements
The full diurnal courses of A and g_s under ambient light conditions were measured monthly from January to April 1999 with a portable gas analysis system (LI-COR model 6400, Lincoln, NE) equipped with a CO₂ control module. All measurements were made on clear days except in March during which measurements were made on a partially cloudy day. Each measurement was made by enclosing about 20 to 30 cladophylls in a clear-topped cuvette to make the total photosynthetic area approximately 4 cm². Cladophyll cuvette conditions during each measurement were maintained at 40% relative humidity, 25°C cuvette temperature, and 35 Pa CO₂ concentration. Each determination was made when A had stabilized; this process typically took 1 to 2 min. After each measurement, cladophylls used for the A measurement were collected and their total surface area was calculated according to the equation:

where D is cladophyll diameter and L is the length of the cladophyll and n is the number of cladophylls used.

The responses of A to intercellular CO₂ partial pressure (A/C_i response) and to irradiance (A/PFD response) were determined on different clear days with similar conditions between 1030 to 1500 h. An umbrella was used to shade the LI-COR gas analysis system during the measurements to avoid overheating. For A/C_i response determination, external CO₂ concentrations (C_a) were supplied in 10 steps from 5 to 80 Pa. Measurements were made at each C_a point when gas exchange had equilibrated, at which point, the coefficient of variation (CV) for the CO₂ concentration differential between the sample and reference analyzers was below 1%. Cladophyll temperature was maintained at 25°C with thermoelectric coolers, and water vapor pressure deficit (VPD) was generally held between 1.2 and 1.7 kPa. A constant PFD of 2000 µmol m^-2 s^-1 was provided by blue-red light-emitting diodes mounted above the chamber.

Analysis of A/C_i responses involved calculation of parameters potentially limiting to photosynthesis: V_cmax (maximum carboxylation rate of rubisco) and J_max (RuBP regeneration capacity mediated by maximum electron transport rate). This was achieved by Photosynthesis Assistant (Dundee Scientific, UK), which uses the biochemical model describing A by Farquhar et al. (1980). Comparison of photosynthetic characteristics between the two cultivars was assisted by calculation of A_sat (net photosynthetic rate at a CO₂ concentration of 80 Pa and saturating PFD, 2000 µmol m^-2 s^-1), C_i/C_a (the ratio of internal to external CO₂ partial pressure under saturating PFD at ambient C_a), and the relative stomatal limitation calculated according to the equation

where A is the net assimilation rate at the growth C_a (35 Pa), and A_o is the net photosynthetic rate at a C_a resulting in a C_i equal to the growth C_a (Farquhar and Sharkey, 1982). The response of A to PFD was determined in the cuvette at PFDs of 2000, 1500, 1000, 800, 500, 300, 200, 150, 100, 75, 50, 25 and 0 µmol m^-2 s^-1. The CO₂ concentration in the cuvette was held at 35 Pa. Other conditions in the cuvette were similar to those in A/C_i curve determinations. Dark respiration (R_d) was measured directly from light response at zero irradiance. Values of A_max were estimated by Photosynthesis Assistant, which uses a quadratic equation established by Prioul and Chartier (1977).

Chlorophyll Fluorescence
Chlorophyll fluorescence of cladophylls measured with a portable fluorometer (Mini-PAM-2000, Walz, Germany) was used to assess the photochemical efficiency of photosystem II (PSII). Intact cladophylls were dark adapted for 30 min by means of a dark clip holder. Minimal fluorescence F_o of the dark-adapted cladophylls was determined by exciting the cladophylls with weak modulated radiation (LED 655 nm) of 0.15 µmol m^-2 s^-1 at frequency of 0.6 kHz. Thereafter, a saturation pulse of 4500 µmol m^-2 s^-1 was applied through a fibre optic cable for 400 ms to obtain maximum fluorescence F_m. Maximum photochemical efficiency of PSII (F_v/F_m) was calculated by the formula (F_m - F_o)/F_m (Bolhàr-Nordenkampf and Öquist, 1993).

Additional Measurements
Total soluble protein was extracted by grinding approximately 0.5 g of fresh sample in a precooled mortar with 5 mL of 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid (HEPES)KOH extraction buffer (pH 7.5), containing 20 mM MgCl₂, 50 mM HEPES, 5 mM EDTA, 2% (w/v) polyvinyl-polypyrolidone (PVP), 15% (w/v) polyethyleneglycol (PEG), 14 mM ß-mercaptoethanol, and 1% (v/v) Tween 80. Immediately after extraction, the extract was centrifuged for 3 min at 15 000 x g and 4°C. The resulting supernatant was assayed for soluble protein by the method of Bradford (1976) using BSA as a standard protein. Chlorophyll content was determined according to Sestak (1971) by grinding about 0.3 g fresh tissue in liquid nitrogen, double extracting with 2 mL of 80% (v/v) acetone, centrifuging for 5 min at 11 000 x g and 4°C, and measuring absorbance of the supernatant at 647 and 664 nm. Shoot xylem water potential () was measured on second shoot terminal branches at midday with a pressure chamber (PMS Instrument CO, Corvallis, OR). Shoot relative water content was determined in separate branches and calculated by

where FW is fresh weight of tissue, FW_sat is the water saturated weight after absorbing water over night, and DW is the dry weight after 48 h at 70°C. Freeze-dried cladophylls were used for soluble sugar and starch determination by a phenol-sulfuric acid method (Tissue and Wright, 1995).

Statistical Analysis
One way analysis of variance (ANOVA) was used to test for difference between the two cultivars. Effect of cladophyll age on photosynthetic parameters was analyzed by Tukey's test. Differences were considered significant if P < 0.05.

	RESULTS

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Diurnal and Seasonal Changes in A and g_s
In both cultivars investigated, diurnal patterns of A generally paralleled changes in PFD and exhibited a sinusoidal pattern (Fig. 1) . In the rapidly expanding cladophyll tissue measured in January, the two cultivars exhibited similar values of A throughout the day, whereas in the fully expanded cladophyll tissue measured in February, a significant difference in A between the two cultivars was observed throughout the measuring period. Measurements of A in mature cladophyll tissues (March) showed reduction in A in both cultivars in comparison with fully expanded cladophyll tissue. However, a consistent difference between the two cultivars was still evident, particularly in the morning. The diurnal patterns of A in senescent cladophyll tissue measured in April were clearly different from the actively photosynthesizing cladophyll tissue in February. After reaching a peak at approximately 1300 h, both cultivars displayed a consistent decline until the end of the day.

View larger version (23K): [in this window] [in a new window]   Fig. 1. Diurnal and seasonal changes in the rate of net photosynthesis (A) and stomatal conductance (gs) between ASP-69 (•) and ASP-03 (). Results are means of six replicates ± SE. Significant differences between ASP-69 and ASP-03 are indicated as *, P < 0.05; **, P < 0.01; ***, P < 0.001.

Diurnal courses in g_s generally paralleled those in A in both cultivars (Fig. 1). In the rapidly expanding cladophyll tissue (January), values of g_s were similar for the two cultivars. In the fully expanded cladophyll tissue (February), there was a significant difference in g_s between the two cultivars throughout the day. Maximum g_s was 104 ± 6 mmol m^-2 s^-1 for ASP-69 and 83 ± 7 mmol m^-2 s^-1 for ASP-03, respectively. A similar trend was observed in mature cladophyll tissue measured in March, but g_s was lower. In senescent cladophyll tissue (April), there was less difference between the two cultivars, although g_s in ASP-69 was slightly higher than in ASP-03. A close correlation between maximum g_s and A was found in both cultivars (r = 0.84; Fig. 2) .

View larger version (21K): [in this window] [in a new window]   Fig. 2. Relationship between stomatal conductance (gs) and net photosynthetic rate by plotting individual values of maximum net photosynthetic rate from each measuring days against concurrent stomatal conductance values.

View larger version (41K): [in this window] [in a new window]   Fig. 3. Seasonal changes in (a) maximum photochemical efficiency Fv/Fm, (b) total chlorophyll content, (c) chlorophyll a/b ratio and (d) soluble protein content measured between 1100 to 1200 h in cladophylls of ASP-69 (closed bar) and ASP-03 (open bar). Results are means of six replicates ± SE. Significant differences between ASP-69 and ASP-03 are indicated as *, P < 0.05; **, P < 0.01; ***, P < 0.001. Different letters within cultivars indicate statistically different values P < 0.05 as determined by Tukey's test.

Cladophyll diameter in ASP-69 was significantly greater than in ASP-03 (Table 3). The greater size in ASP-69 was associated with a greater SLW of 2.47 ± 0.03 mg cm^-2 in comparison with ASP-03 with 2.18 ± 0.05 mg cm^-2. Soluble sugar content was greater in ASP-69 than in ASP-03, whereas starch content did not differ significantly between the two cultivars in mature cladophylls (Table 3).

	DISCUSSION

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Effect of Cladophyll Age on Photosynthetic Parameters
In temperate conditions, photosynthetic activity in asparagus is maintained for approximately 4 mo from late spring to late summer and then all cladophyll tissue senesces within a few weeks in the fall. Given such a short growth period, it is crucial for the plants to reach maximum photosynthetic capacity quickly and to maintain photosynthesis for as long as possible. Our results indicate that both cultivars had high rates of net photosynthesis in rapidly expanding cladophyll tissue and attained maximum rates of net photosynthesis in fully expanded cladophyll tissue when seasonal radiation and temperature were both at a maximum. These results are in agreement with those of Downton and Törökfalvy (1975) who found that net photosynthesis occurs once the cladophyll begins to assume a needle-like form.

Both cultivars showed a significant decline in A in senescent cladophyll tissue in April, although most of the senescing cladophylls retained their chlorophyll content. The lack of a significant decrease in F_v/F_m in senescent cladophyll tissue in April in comparison to May indicates that photochemical capacity was maintained. In the senescent cladophyll tissue measured in May, the decrease in photosynthesis was accompanied by a significant decline both in F_v/F_m and chlorophyll content, indicating a loss of both reaction centers and light harvesting complexes of PSII (Massacci and Jones, 1990). Furthermore, the rapid decrease in the chlorophyll a/b ratio in May indicates that the PSII reaction center complexes, which contain only chlorophyll a, were degraded more than the light-harvesting chlorophyll protein (Pearrubia and Morebo, 1995). These results suggested that cladophyll senescence has two phases. In the first phase, the decrease in A may be explained by the existence of an increased mesophyll resistance because of biochemical inactivation of photosynthetic enzymes or decreased enzyme pools caused by an extended cold period (Hansen et al., 1996; Schwarz et al., 1997). In the second phase, there is an overall reduction both in reaction centers and light harvest complexes of PSII (Peñarrubia and Morebo, 1995).

In the current study, we did not observe any symptoms of photoinhibition in the two cultivars even though PFD exceeded 1500 µmol m^-2 s^-1 at noon on all the measuring days. Rates of photosynthesis were well maintained and generally aligned with diurnal changes in PFD. Neither cultivar displayed a significant decline in F_v/F_m during the days measured. F_v/F_m always recovered to maximum values at night except in senescing cladophylls. This suggests that both cultivars are fully adapted to present environmental conditions and do not suffer photoinhibition.

Stomatal and Nonstomatal Limitation to Photosynthesis
Both stomatal and nonstomatal (metabolic) factors have been shown to limit photosynthetic capacity, and the impact of the two factors varies among species or genotypes in response to environmental conditions (Hutmacher and Krieg, 1983; Briggs et al., 1986; Teskey et al., 1986). Under dry soil conditions, it is generally believed that stomatal limitation to CO₂ influx into the mesophyll is the primary cause of the photosynthetic depression observed in mature tissue (Quick et al., 1992; Kicheva et al., 1994; Ishida et al., 1999). However, relative reductions in photosynthesis compared with stomatal conductance have been observed in several species under dry soil conditions (Ni and Pallardy, 1992). In addition, decreased stomatal conductance may be the result rather than the cause of decreased photosynthesis (Fiscus et al., 1997). Under other circumstances (elevated CO₂), metabolic limitation may exercise a greater degree of control over photosynthesis than the stomatal conductance at the chloroplast level (Noormets et al., 2001).

In the present study, both cultivars had significantly lower net photosynthesis rates in the senescent cladophyll measured in April in comparison with the mature cladophyll measured in March. The decline in A was accompanied by a decrease in stomatal conductance, whereas C_i/C_a ratio, which directly reflects changes in the relationship between stomatal conductance and the biochemical capacity for CO₂ fixation (Tissue et al., 1995), was similar in these two cultivars. Relative stomatal limitation to photosynthesis (L_stom) was also not significantly different between the two cultivars. These results indicate a close coordination between stomatal conductance and biochemical capacity for CO₂ assimilation in the two cultivars. However, the decline in A without a corresponding decline in C_i/C_a in the early senescent cladophyll suggests that the stomatal response was secondary to changes in mesophyll processes (Noormets et al., 2001).

Causes of Cultivar Variation in Photosynthetic Rate
Parameters derived from A/C_i and A/PFD relationships provide some understanding as to the causes for the different photosynthetic capacities between the two asparagus cultivars. Values of A_sat, A_max, and V_cmax in ASP-69 were significantly greater than in ASP-03. Apart from the physiological differences, differences in cladophyll properties are also likely to play a significant role in determining the rate of photosynthesis in the two cultivars. The rate of photosynthesis can be affected by various anatomical features of the leaves, including mesophyll size and arrangement. In this study, significant cultivar difference existed in cladophyll thickness. The high-yielding cultivar (ASP-69) had thicker cladophylls and greater SLW than in ASP-03. Similar results have also been reported by Faville et al. (1999) and Bai and Kelly (1999). Obviously, an increase in thickness will influence mesophyll volume for a given surface area. Our observations are thus consistent with the idea that the greater biochemical activity in ASP-69 is partly due to greater photosynthetic machinery resulting from thicker cladophyll tissue. The close relationship between cladophyll thickness and photosynthetic capacity among asparagus cultivars raises the possibility of selecting high-yielding cultivars with greater photosynthetic rate without significantly reducing canopy size. This approach needs further investigation. The overall data presented here highlight the conclusion that apart from significant differences in canopy size, photosynthetic capacity per unit leaf area is also a significant factor contributing to differences in assimilate production between the two cultivars, and both physiological and anatomical factors appear to play significant roles in determining differences in photosynthetic capacity.

	ACKNOWLEDGMENTS

 
This study was supported by the New Zealand Foundation for Research Science and Technology under contract CO2X0019. We thank New Zealand Institute of Crop and Food Research for providing the asparagus trial and maintaining the site facilities to conduct this study and we thank Nicole Lauren for her technical assistance.

Received for publication May 25, 2001.

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