Photosynthetic Responses of Swiss Chard, Kale, and Spinach Cultivars to Irradiance and Carbon Dioxide Concentration

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  • 1 Department of Horticultural Science, University of Minnesota, 305 Alderman Hall, 1970 Folwell Avenue, St. Paul, MN 55108

The impact of irradiance (0–1200 μmol·m−2·s−1) and carbon dioxide concentration (CO2; 50–1200 ppm) on kale (Brassica oleracea and B. napus pabularia; three cultivars), Swiss chard (chard, Beta vulgaris; four cultivars), and spinach (Spinacea oleracea; three cultivars) photosynthetic rate (Pn; per area basis) was determined to facilitate maximizing yield in controlled environment production. Spinach, chard, and kale maximum Pn were 23.8, 20.3, and 18.2 μmol CO2·m−2·s−1 fixed, respectively, across varieties (400 ppm CO2). Spinach and kale had the highest and lowest light compensation points [LCPs (73 and 13 μmol·m−2·s−1, respectively)] across varieties. The light saturation points (LSPs) for chard and kale were similar at 884–978 μmol·m−2·s−1, but for spinach, the LSP was higher at 1238 μmol·m−2·s−1. Dark respiration was lowest on kale and highest on spinach (−0.83 and −5.00 μmol CO2·m−2·s−1, respectively). The spinach CO2 compensation point (CCP) was lower (56 ppm) than the chard or kale CCP (64–65 ppm). Among varieties, ‘Red Russian’ kale Pn saturated at the lowest CO2 concentration (858 ppm), and ‘Bright Lights’ chard saturated at the highest (1266 ppm; 300 μmol·m−2·s−1). Spinach Pn was more responsive to increasing irradiance than to CO2. Kale Pn was more responsive to increasing CO2 than to irradiance, and chard Pn was equally responsive to increasing CO2 or irradiance. Implications and limitations of this work when “upscaling” to whole-plant responses are discussed.

Abstract

The impact of irradiance (0–1200 μmol·m−2·s−1) and carbon dioxide concentration (CO2; 50–1200 ppm) on kale (Brassica oleracea and B. napus pabularia; three cultivars), Swiss chard (chard, Beta vulgaris; four cultivars), and spinach (Spinacea oleracea; three cultivars) photosynthetic rate (Pn; per area basis) was determined to facilitate maximizing yield in controlled environment production. Spinach, chard, and kale maximum Pn were 23.8, 20.3, and 18.2 μmol CO2·m−2·s−1 fixed, respectively, across varieties (400 ppm CO2). Spinach and kale had the highest and lowest light compensation points [LCPs (73 and 13 μmol·m−2·s−1, respectively)] across varieties. The light saturation points (LSPs) for chard and kale were similar at 884–978 μmol·m−2·s−1, but for spinach, the LSP was higher at 1238 μmol·m−2·s−1. Dark respiration was lowest on kale and highest on spinach (−0.83 and −5.00 μmol CO2·m−2·s−1, respectively). The spinach CO2 compensation point (CCP) was lower (56 ppm) than the chard or kale CCP (64–65 ppm). Among varieties, ‘Red Russian’ kale Pn saturated at the lowest CO2 concentration (858 ppm), and ‘Bright Lights’ chard saturated at the highest (1266 ppm; 300 μmol·m−2·s−1). Spinach Pn was more responsive to increasing irradiance than to CO2. Kale Pn was more responsive to increasing CO2 than to irradiance, and chard Pn was equally responsive to increasing CO2 or irradiance. Implications and limitations of this work when “upscaling” to whole-plant responses are discussed.

Leafy green vegetable options are increasing as communities become more ethnically or racially diverse or both, as the health and nutritional benefits of greens consumption are reported (Bertoia et al., 2015; Hu and Rimm, 2015), and as interest in year-round locally produced foods increases (Feldmann and Hamm, 2015). Three increasingly popular leafy vegetables are kale (Brassica oleracea and B. napus pabularia), spinach (Spinacea oleracea), and Swiss chard (chard, Beta vulgaris).

Kale, spinach, and chard leaves are harvested and sold on a fresh-weight basis. The ability of plants to increase fresh weight, or mass, is associated with photosynthesis where plant mass generally increases as photosynthesis increases (Björkman, 1981; Chagvardieff et al., 1994; Dorais, 2003). The primary inputs into the photosynthetic process are light (irradiance), CO2, and water (Björkman, 1981). Therefore, maximizing photosynthesis in leafy greens to maximize yield would require that irradiance, CO2, or water not be limited (Fu et al., 2017; Gaudreau et al., 1994; Gent, 2016).

In northern climates, year-round leafy green production requires protected cultivation during the late fall, winter, and early spring when temperatures drop below freezing. Irradiance and CO2 in protected cultivation often vary, intentionally and unintentionally, depending on covering type, plant spacing, degree of ventilation, whether air is circulated, and whether supplemental lighting or CO2 are supplied (Kretchen and Howlett, 1970). Little work has been conducted on the effects of irradiance and CO2 on the Pn of leafy greens other than lettuce (Lactuca sativa; Dorais, 2003; Fu et al., 2017; Gaudreau et al., 1994) and recent work by Gent (2016) on spinach. An understanding of how irradiance and CO2 impact the Pn of such greens would facilitate maximizing the Pn to maximize yield in protected cultivation. The objective of the research presented here was to determine the Pn responses of spinach, kale, and chard to irradiance and CO2 and to inform producers of the advantages or disadvantages of reduced or increased irradiance or CO2 on yield. We also desired to determine whether leafy green varieties differed in the Pn responses to irradiance and CO2 and whether some varieties were more suited to supplemental, or reduced, irradiance and CO2 levels.

We acknowledge that translating instantaneous Pn measurements on a per-unit-area basis to whole-plant photosynthesis has limitations (see Discussion). Yet, an initial comparative study exploring the variation in the instantaneous Pn on a per-unit-area basis is valuable in that it provides some insight into the degree of variation among species and varieties. These data also provide some guidance on irradiance and CO2 levels that maximize the Pn on the uppermost leaves, especially when plants are young and interior leaf shading is limited.

Materials and Methods

Chard, [‘Rhubarb’, ‘Fordhook Giant’, ‘Bright Yellow’, and ‘Bright Lights’ (red)], kale [‘Toscano’, ‘Winterbor’, and ‘Red Russian’ (B. napus pabularia)], and spinach (‘Melody’, ‘Harmony’, and ‘Bloomsdale LS’) seeds were sown in 10.5-cm-diameter plastic pots (5 seeds/pot) in premoistened LC-8 soilless growing media (Sun Gro Horticulture, Bellevue, WA) and placed in a greenhouse (24 ± 2 °C day and 16 ± 2 °C night temperatures; St. Paul, MN). Kale and chard seeds were obtained from Johnny’s Selected Seeds (Winslow, ME), and spinach seeds were obtained from W. Atlee Burpee & Co. (Warminster, PA). Seeds germinated in 4–7 d.

Greenhouse daylight (0800–1400 hr) was supplemented with 75 μmol·m−2·s−1 high-pressure sodium lighting when daylight (at plant level) was below 200 μmol·m−2·s−1. After 7 d, the three most uniform (similar size) seedlings were left to grow, whereas the others were removed. As kale and chard flower after they unfold a specific leaf number, after a cool temperature exposure, or both, daylength was extended with 75 μmol·m−2·s−1 from 1600–2200 hr as flowering was not a concern [16 h photoperiod; mean daily light integral (DLI) = 12.4 mol·m−2·d−1] to simulate a typical production environment to maximize yield (J. Erwin, personal observation). In contrast, as long days can promote flowering on spinach early in development, spinach seedlings were grown under short days (8 h photoperiod; opaque cloth pulled over plants from 1400–0800 hr daily; mean DLI = 10.7 mol·m−2·d−1) to inhibit flowering. After 30 d, plants were transplanted into 7.6-l plastic pots. Throughout, plants were watered as needed with irrigation water containing 250 ppm N from 15N–0P–15K fertilizer (Peter’s Dark Weather Feed; The Scotts Co., Marysville, OH). All plants were watered at the same time to ensure similar media nutritional status (confirmed with soil tests) among species and varieties.

Photosynthetic rate determination.

After kale plants unfolded seven true leaves (>45° angle from the stem), chard plants unfolded four leaves, and spinach plants unfolded eight leaves (≈4 weeks across species), the impact of irradiance and CO2 on instantaneous Pn on a per-unit-leaf-area basis was determined on the second leaf below the uppermost fully expanded unfolded leaf on five plants of each species and variety. The Pn was measured using a LI-COR LI6400XT portable photosynthesis meter (LI-COR, Inc., Lincoln, NE) using a cuvette (6 cm2) with a built-in variable LED light source. The Pn at 0, 100, 200, 400, 600, 800, 1000, and 1200 μmol·m−2·s−1 irradiance was determined. The Pn at 50, 200, 400, 600, 800, 1000, and 1200 ppm CO2 was also determined. The Pn was recorded 5 min after a change in irradiance or CO2 after the Pn had stabilized. Throughout, cuvette temperature was maintained at 24 °C, and the atmospheric flow rate was 400 μL·min−1. Cuvette CO2 was 400 ppm (outdoor ambient) when determining the Pn responses to irradiance, and irradiance was 300 μmol·m−2·s−1 (typical irradiance in a northern U.S. greenhouse during the winter; personal observation) when measuring the Pn responses to CO2.

Photosynthetic parameter determination.

The Pn data from each leaf of each species and variety at varying irradiance or CO2 were fit to the nonlinear Mitscherlich and the nonrectangular hyperbola functions as both are widely used to estimate the Pn responses to irradiance and CO2 (Aleric and Kirkman, 2005; Goudrian, 1979; Johnson et al., 2010; Laitat and Boussard, 1995; Marino et al., 2010; Peek et al., 2002; Potvin et al., 1990). The Mitscherlich equations (Eqs. [1] and [2]) fit data best here and provided realistic nonlinear parameter values (Table 1; personal observation). More complex biochemical models estimating the leaf Pn [such as used by Farquhar et al. (1980)] were not used, as we quantified the Pn responses to CO2 at irradiance levels typical in northern greenhouses here and not saturating levels typically used with biochemical models.
DE1
Table 1.

Statistics associated with goodness of fit of raw data to the nonlinear Mitscherlich function used to describe responses of kale (Brassica oleracea and B. napus pabularia; three cultivars), spinach (Spinacea oleracea; three cultivars), and Swiss chard (Beta vulgaris; four cultivars) to irradiance and carbon dioxide concentration. The r2, mean square error (MSE), and “k” values (Mitscherlich function) fit to data are shown.

Table 1.
Eq. [1] shows Pn responses [Pn (I)] to irradiance (I). Pn responses to increasing irradiance were asymptotic here; “Pmax” in Eq. [1] estimates the asymptote. LSP was the irradiance at 95% of Pmax. “I0” was the LCP (irradiance when estimated Pn = 0 μmol·m−2·s−1 CO2 fixed), and “k” was a constant that represented the ratio of the quantum yield (q) to the Pn at the LCP (Marino et al., 2010). Rd (dark respiration) was calculated as the estimated Pn (I) when irradiance was 0 μmol·m−2·s−1.
DE2

Eq. [2] shows Pn responses [(Pn (C)] to CO2. Pn responses to increasing CO2 were asymptotic; “Pmax” in Eq. [2] estimates the asymptote. “C0” is the estimated CCP (CO2 when Pn = 0 μmol·m−2·s−1 CO2 fixed), and “k” is a constant. The CO2 concentration at 95% of Pmax approximated the CO2 saturation point (CSP; CO2 when Pn was saturated).

Experimental design and data analysis.

Analysis of variance (ANOVA) was conducted on photosynthetic parameters derived from Eqs. [1] and [2] fit to Pn data from each leaf on each plant as dependent variables. The experiment was analyzed as a two-stage nested design using Type I sum of squares, which allows the use of Tukey’s honestly significant difference (HSD) for mean separation with species as the first factor and cultivar the second. Estimated k values, r2, and mean square errors (MSEs) derived from the ANOVA are shown in Table 1. Tukey’s HSD (α < 0.05) was employed for mean separation except in Table 4 where least significant difference (LSD; α < 0.05) was employed as Tukey’s HSD cannot be employed with a repeated measures test. A Tukey’s test conducted when sphericity is violated (often the case with collected repeated measures tests) will have a vastly inflated Type I error rate; SPSS (see below) presumably does not include Tukey’s test as an option under repeated measures analysis to prevent this error. The best test to compare multiple comparisons in a repeated measures design is Bonferroni’s; for our data, Bonferroni’s gave the same results as LSD. Aside from this case, Tukey’s HSD was used when possible as it is more statistically rigorous than LSD. Throughout, the SPSS statistical software package (IBM SPSS Statistics, Version 23; IBM Corp., Armonk, NY) was used for statistical analysis.

Results

Photosynthetic responses to irradiance.

Pmax (identified by providing saturating irradiance levels at 400 ppm CO2) differed among species, varieties within a species, and across all varieties (Table 2). Spinach had the highest Pmax at 23.8 μmol CO2·m−2·s−1 fixed, whereas for kale it was 20.3 μmol CO2·m−2·s−1 fixed and for chard it was 18.2 μmol CO2·m−2·s−1 fixed (across varieties; Fig. 1; Table 2). Among kale varieties, ‘Red Russian’ and ‘Toscano’ had a higher Pmax (21.0–22.3 μmol CO2·m−2·s−1) than ‘Winterbor’ (17.4 μmol CO2·m−2·s−1; Table 2). Among spinach varieties, ‘Melody’ had a higher Pmax (26.6 μmol CO2·m−2·s−1) than ‘Harmony’ or ‘Bloomsdale LS’ (22.3–22.4 μmol CO2·m−2·s−1; Table 2). Among chard varieties, ‘Fordhook Giant’ had a higher Pmax (21.9 μmol CO2·m−2·s−1) than ‘Bright Lights’ or ‘Yellow’ (16.3–16.6 μmol CO2·m−2·s−1; Table 2). Across all species and varieties, ‘Melody’ spinach had the highest Pmax, and ‘Yellow’ and ‘Bright Lights’ chard had the lowest Pmax (Table 2).

Table 2.

Variation in predicted maximum photosynthetic rate (Pmax), the light compensation point (irradiance at Pn = 0), the light saturation point (irradiance at 95% of Pmax), predicted dark respiration rate (CO2 evolution in dark at 24 °C), and quantum efficiency among three varieties of kale (Brassica oleracea and B. napus pabularia), three varieties of spinach (Spinacea oleracea), and four varieties of Swiss chard (Beta vulgaris) as determined using a fitted Mitscherlich model for each plant of each species and variety. Capital letters denote mean separation [Tukey’s hsd(0.05)] across species, and small letters denote mean separation across varieties.

Table 2.
Fig. 1.
Fig. 1.

Effect of increasing irradiance (A) or carbon dioxide (CO2) concentration (B) on spinach (Spinacea oleracea), kale (Brassica oleracea and B. napus pabularia), and Swiss chard (Beta vulgaris) photosynthetic rate across cultivars. Bars represent the ± mean square error as identified through analysis of variance (α < 0.05).

Citation: HortScience horts 52, 5; 10.21273/HORTSCI11799-17

Spinach had the highest LCP (73 μmol·m−2·s−1), the LCP of chard was 25 μmol·m−2·s−1, and kale had the lowest LCP at 13 μmol·m−2·s−1 (Table 2). Kale and spinach variety LCP did not differ, but chard variety LCP differed from 16 (Bright Lights) to 41 μmol·m−2·s−1 (Rhubarb; Table 2). Chard and kale LSP (884–978 μmol·m−2·s−1) did not differ, but spinach LSP was higher (1238 μmol·m−2·s−1; Table 2). LSP did not differ among varieties within any species studied here (Table 2).

Photosynthetic responses to CO2 concentration.

Pmax (identified by providing saturating CO2 concentrations at 300 μmol·m−2·s−1) differed among some species, among varieties within some species, and across all varieties (Table 3). Chard and kale Pmax did not differ (17.2–17.6 μmol CO2·m−2·s−1 fixed), but spinach Pmax was higher at 19.8 μmol CO2·m−2·s−1 fixed (across varieties; Fig. 1; Table 3). Pmax did not differ among spinach varieties. Among kale varieties, ‘Winterbor’ had a lower Pmax than ‘Red Russian’ (Table 3). Chard Pmax varied from 16.6 μmol CO2·m−2·s−1 for ‘Rhubarb’ to 19.2 μmol CO2·m−2·s−1 for ‘Bright Lights’ (Table 3). Across varieties, ‘Winterbor’ kale had the lowest Pmax (14.7 μmol CO2·m−2·s−1), and ‘Red Russian’ and ‘Toscano’ kale had the highest Pmax (17.8 and 19.0 μmol CO2·m−2·s−1, respectively; Table 3).

Table 3.

Variation in the predicted maximum photosynthetic rate (Pmax; μmol CO2·m−2·s−1), the CCP (CO2 concentration when Pn = 0), and the CSP (the CO2 concentration at 95% Pmax) among three cultivars of kale (Brassica oleracea and B. napus pabularia), three cultivars of spinach (Spinacea oleracea), and four cultivars of Swiss chard (Beta vulgaris) as determined using fitted Mitscherlich functions fit to each cultivar and pooled under each species. Capital letters denote mean separation [Tukey’s hsd(0.05)] across species, and small letters denote mean separation across cultivars.

Table 3.
Table 4.

Predicted instantaneous photosynthetic rates (Pn per unit area; μmol CO2·m−2·s−1) at low irradiance (typical cloudy day in winter; 200 μmol·m−2·s−1), ambient irradiance (typical 300 μmol·m−2·s−1), and at 95% of predicted Pmax (Pn saturated) of kale (Brassica oleracea and B. napus pabularia), Swiss chard (Beta vulgaris), and spinach (Spinacea oleracea) varieties. Predicted Pn at low CO2 levels (200 ppm; depleted enclosed environment), at ambient CO2 levels (400 ppm, current outdoor), and at 95% of predicted Pmax of kale, Swiss chard, and spinach varieties. Percentage in parenthesis is the percent increase in Pn when increasing from the rate one line up and to the left, to the level above the number in parentheses. Letters denote mean separation [Tukey’s hsd (α < 0.05)] within a variety to increasing irradiance or increasing carbon dioxide concentration.

Table 4.

Spinach CCP was lower (56 ppm) than chard or kale CCPs (64–65 ppm) across varieties (Table 3). CCP did not differ among spinach or chard varieties, but differed among kale varieties where ‘Red Russian’ had the lowest CCP (59 ppm) and ‘Winterbor’ the highest (72 ppm; Table 3). CSP did not vary among species or among varieties within a species, but differed when all varieties were compared; ‘Red Russian’ kale had the lowest CSP (858 ppm), and ‘Bright Lights’ chard had the highest CSP (1266 ppm; Table 3).

Dark respiration.

Calculated Rd (24 °C) differed among species. Kale Rd was the lowest (−0.83 μmol CO2·m−2·s−1), chard Rd was −1.64 μmol CO2·m−2·s−1, and spinach Rd was the highest (−5.00 μmol CO2·m−2·s−1; across varieties; Table 2). Rd did not differ among kale and spinach varieties, but differed among chard varieties where ‘Rhubarb’ and ‘Bright Lights’ chard Rd was −2.60 and −10.06 μmol CO2·m−2·s−1, respectively (Table 2).

Discussion

Limitations of generalizing instantaneous Pn data on a per-unit-area basis to whole-plant Pn.

Data here provide a framework for determining irradiance and CO2 impacts on kale, spinach, and chard Pn to facilitate production in controlled environment facilities to maximize yield. Pn is often associated with dry weight gain, fresh weight gain, and yield in vegetables (Heuvelink and Dorais, 2003). There are limitations when extrapolating changes in instantaneous Pn measurements on a per-unit-area basis to whole-plant Pn and conclusions drawn from that data. For instance, instantaneous Pn responses can differ from whole-plant responses when a) multiple inputs are changed at once, b) after plants acclimate to altered irradiance, CO2, or both, and c) when leaf aging and whole-plant leaf area/shading are taken into account.

One environmental parameter (irradiance or CO2) was changed while the other was held constant in our research here. Increasing irradiance and CO2 simultaneously may produce different conclusions, likely increasing LSP, CSP, or both more than reported here. For instance, Chagvardieff et al. (1994) observed increasing CO2 and irradiance simultaneously increased lettuce dry weight 69% more than dry weight gains observed from increasing CO2 and irradiance separately, i.e., there was a synergy between these factors. Also, other environmental parameters can interact with irradiance, CO2, or both to impact Pn. Changes in humidity (Kaiser et al., 2015) or temperature (Dahal et al., 2012) can result in markedly different responses in Pn to irradiance, CO2, or both. Nonenvironmental cultural factors can also impact Pn and assumptions made here. For instance, high irradiance promotion of Pn was most obvious when lettuce was grown under low nitrogen levels only (7 mmol·L−1; Fu et al., 2017).

Photosynthetic rate can acclimate to altered irradiance or CO2 over time (Björkman, 1981; Lambers et al., 2008; Pons, 2012). Therefore, caution should be exercised when extrapolating instantaneous Pn responses to whole-plant Pn over time. Pn at high irradiance or CO2 may be overpredicted, and Pn at low irradiance or CO2 may be underpredicted over time (Bunce and Ziska, 2000). The basis for Pn acclimation to altered irradiance or CO2 is not clear. Acclimation of Pn to high irradiance or CO2 was more correlated with soluble saccharides than with day to day variation in CO2 or irradiance alone (Bunce and Sicher, 2003). In contrast, variation among Arabidopsis varieties in Pn over time to irradiance was associated with differences in Rubsico activation and stomatal conductance (gS) (Kaiser et al., 2016).

Also, the transferability of our conclusions to whole-plant responses is associated with the size (or age) of a plant and leaf area. High irradiance can result in reduced leaf life or smaller leaf area which can result in an overestimating whole-plant Pn if reduced leaf area, more rapid leaf senescence, or both is not taken into account (Austin, 1989). Also, although Pn on the uppermost leaf may be saturated, whole-plant Pn is likely not saturated as lower leaves are shaded in a canopy as a plant grows and unfolds leaves. Such shading results in Pn rates lower than the Pmax on lower leaves even when irradiance on the uppermost leaves is at the LSP. Irradiance in a canopy decreases exponentially from the top to the bottom of a plant following the general equation I = Ioe−kL [I = irradiance below the canopy; Io = irradiance at the top of the canopy; k = the extinction coefficient (generally >0.5 for nonvertically oriented leaves); and L = leaf area index (Lambers et al., 2008)]. Therefore, increasing irradiance at the top of the plant above the LSP will likely increase whole-plant Pn if the leaf area index is high.

Although these limitations when translating instantaneous Pn data to crop responses exist, we believe Pn responses are still informative. Specifically, instantaneous Pn data on a per-unit-area basis provide insight into variation in responses among species and varieties that is of value and provide some insight into which species or varieties may be more responsive to increases in irradiance or CO2 concentration.

Responses to irradiance.

Kale and chard Pn saturated at lower (600–800 μmol·m−2·s−1) irradiance levels than spinach (1000–1200 μmol·m−2·s−1; 400 ppm CO2; Fig. 1; Table 2). Pmax reported here are consistent with previous data on spinach (Boese and Huner, 1990; Yamori et al., 2005) and kale [Brassica; Dahal et al. (2012) (napus) and Ruhil et al. (2015)] at slightly lower CO2 concentrations than used here. Given irradiance in northern climates in greenhouses rarely exceeds LSPs reported here (personal observation), supplemental lighting (up to the LSPs, at a minimum) would increase Pn and presumably yield. Supplemental lighting in northern greenhouse vegetable production facilities is commonplace as growers observe increased yield when providing supplemental light. In greenhouse lettuce production, daylight is often supplemented with 50–100 μmol·m−2·s−1 (DLI = 12–13 mol·m−2·d−1) during the winter to realize 140% to 270% increases in yield compared with plants with no supplemental lighting in Canada (Gaudreau et al., 1994). Similarly, Brassicaceae microgreen (seedling) fresh weight and nutritional value increased when irradiance was increased from 0 to 320–440 μmol·m−2·s−1, but not when irradiance was further increased from 440 to 545 μmol·m−2·s−1 (Samuoliene et al., 2013). In contrast, Colonna et al. (2016) showed that the impact of irradiance on the nutritional value of 10 leafy vegetables varied with species.

Daily light integral can be more associated with yield than with irradiance as it represents the cumulative light delivered over 24 h. For instance, spinach dry weight as a ratio of fresh weight increased as normalized daily light integral (DLI/leaf area index) increased from 3 to 27 mol·m−2·d−1 (Gent, 2016). However, it is important to note that a high correlation between DLI and plant dry weight will occur only if irradiance is below the LSP; irradiance levels above the LSP would not result in an increase in Pn.

Based on the instantaneous Pn data here, kale and chard may be better suited for production in naturally low irradiance locations or facilities than spinach as their LSP were lower than that of spinach (Table 2). Also, as spinach had a higher LCP (60–75 μmol·m−2·s−1) than kale (10–15 μmol·m−2·s−1), kale may be grown under lower irradiance conditions than spinach and still have a net increase in mass. Again, we emphasize that these assumptions are based on instantaneous data, and plants may acclimate to lower irradiance levels over time.

Table 4 shows predicted percent changes in Pn when irradiance was increased from 300 to 350 μmol·m−2·s−1 on kale, chard, and spinach (DLI = +3.24 mol·m−2·d−1 for chard and kale, and +1.44 mol·m−2·d−1 for spinach as photoperiod differed). Increasing irradiance from 300 to 350 μmol·m−2·s−1 increased predicted spinach Pn by 15% and that of kale and chard by 9% to 11% (Table 4).

Responses to CO2.

Kale and chard CSP was lower (600–800 ppm) than that of spinach (1000–1200 ppm) (irradiance = 300 μmol·m−2·s−1; Fig. 1; Table 3). Responses observed on kale here were similar to those observed by others (700 ppm CO2) on B. oleracea and B. napus under different irradiance levels (Bunce and Sicher, 2003; Dahal et al., 2012, respectively). Given all CSPs reported here are higher than the ambient CO2 levels, supplementing greenhouses or growth rooms with CO2 (above ambient) would likely increase the Pn of crops studied here (Table 3). In fact, injecting CO2 to increase CO2 levels to 800–1000 ppm is commonplace in commercial vegetable production greenhouses to increase yield (personal observation; Dorais, 2003). For instance, increasing CO2 from 330 to 900 ppm increased tomato yield by 21% (Dorais, 2003).

Pn in unventilated greenhouses or enclosed rooms can be limited by declining CO2 levels as plants use CO2 for photosynthesis. It is not uncommon for CO2 levels in a canopy to drop to 200–250 ppm during the day in an unvented greenhouse or growth room (J. Erwin and J. Frantz, personal observations). Therefore, ventilating production environments with outdoor air (400 ppm CO2) will increase CO2 concentration inside thus increasing Pn. Our data predict ventilating greenhouses to increase CO2 levels from 200 to 400 ppm can result in a greater increase in Pn than that from increasing CO2 from 400 to 800 ppm as would occur when using a CO2 injection system (Table 4). For instance, increasing CO2 from 200 to 400 ppm increased predicted Pn by 75% to 98% across species whereas increasing CO2 levels from 400 ppm to the CSP increased predicted Pn by 38% to 68% across species (Table 4). These data emphasize the importance of ventilating to ensure canopy CO2 levels are at least similar to ambient outdoor levels. Of course, the predicted increases in Pn if CO2 is increased from 400 to 800 ppm may be greater if irradiance was simultaneously increased to the LSP.

As with Pn responses to irradiance, although CO2 levels on the uppermost leaves may be at CSP levels, lower leaf Pn is likely not at CSP levels as CO2 is consumed by photosynthesis in the canopy and replaced slowly (depending on air circulation and ventilation). Therefore, increasing CO2 levels to above the CSP often results in increased yields as lower leaf Pn is less CO2 limited. This is increasingly important as leaf area index increases in a canopy. Kale and chard had lower CSP than spinach; therefore, these crops would perform better in greenhouses with poor ventilation or with close plant spacing than spinach (Table 3).

Respiration.

Spinach, kale, and chard predicted Rd (24 °C) observed here are comparable with those measured by others although temperatures differed somewhat (Dahal et al., 2012; Yamori et al., 2005). We observed variation in Rd among species and among varieties of some species. Although spinach variety Rd was high and similar, kale and chard variety Rd varied with some varieties having a 4-fold higher Rd than with other varieties (Table 2). Variation in Rd among varieties of other vegetable species (such as asparagus) has also been observed (Kitazawa et al., 2011). Such variation in Rd among species and varieties here are especially important to quantify as Rd can be negatively correlated with postharvest performance (Kitazawa et al., 2011). For instance, data here suggest that spinach may have a shorter postharvest life than kale and that among kale varieties and among chard varieties, ‘Bright Lights’ may have a shorter postharvest life than ‘Rhubarb’ (Table 2).

Irradiance versus CO2.

The question arises as to whether a spinach, kale, or chard producer should increase irradiance or CO2 to increase yield most. Low CO2 conditions (200 ppm) reduced predicted Pn more than low irradiance (200 μmol·m−2·s−1) conditions on both kale and chard here (Table 4). Therefore, ventilating enclosed production spaces (where CO2 may have dropped to 200 ppm) to ensure CO2 levels are at ambient levels (400 ppm) may increase Pn and likely yield on kale and chard more than on spinach. In contrast, in nearly all cases (except ‘Toscano’ kale, and ‘Yellow’ and ‘Bright Lights’ chard), increasing irradiance from ambient irradiance (300 μmol·m−2·s−1) to the LSP increased predicted Pn more than increasing CO2 from ambient (400 ppm) to the CSP (Table 4). This suggests that irradiance may be more limiting than CO2 with the crops studied here.

Future work must examine the synergy between irradiance and CO2 on kale, chard, and spinach. Increasing CO2 from 400 to 800 ppm and increasing irradiance from 400 to 800 μmol·m−2·s−1 significantly increased lettuce dry weight by 25% (1.5 g/plant) and 19%, (1.15 g/plant), respectively (Chagvardieff et al., 1994). However, increasing CO2 concentration and irradiance simultaneously acted synergistically [2.65 g/plant when benefits added individually vs. 4.21 g/plant (+69%) when increased together] when conducted 23 to 40 d after sowing (Chagvardieff et al., 1994).

Variety differences.

Varieties (of some species) differed in response to increasing irradiance or CO2 suggesting different genetic backgrounds. There was little variation among spinach varieties in Pmax, LCP, CCP, LSP, and CSP (Tables 1 and 2). However, there were substantial differences among kale and chard varieties for these same parameters (Tables 1 and 2). This was not unexpected as vegetable crops are often interspecific hybrids, and varieties can vary greatly genetically. Similar variation in Pmax among lettuce varieties was observed by Behr and Wiebe (1992). Gu et al. (2012) observed variation in Pmax (17% to 25% variation) in rice (13 lines; Oryza sativa L.) at ambient CO2 levels (380 ppm) and that variation was associated with stomatal and mesophyll conductance. Yu et al. (2016) found variation in Cucumis Pn varieties to changes in irradiance was associated with differences in leaf cholorophyll content. In another work, differences in Arabidopsis variety Pn responses to changing irradiance was associated with differences in Rubsico activation and gS (Kaiser et al., 2016). Whatever the basis, our data infer genetic diversity (based on Pn responses) of kale and chard may be greater than that of the spinach varieties studied here.

Combining both Pn and Rd.

It cannot also be assumed that higher Pn will result in increased fresh or dry weight and yield as yield is associated with carbon loss or Rd. As Rd occurs during both day and night, it can have a significant negative impact on net daily carbon gain. When predicted daily carbon gain was calculated by taking both Pn (Rd already quantified in direct Pn readings) and Rd (at night only) into account {net carbon gain = [(Pmax × 18 h·d−1 (kale) or 8 h·d−1 (spinach)] – [(Rd × 8 h·d−1 (kale) or 16 h·d−1 (spinach)]}, we observed spinach carbon gain/d (380.8–80.0 = 300.8 μmol CO2·m−2·s−1) was lower than that of kale (365.4–6.6 = 358.8 μmol CO2·m−2·s−1) even though Pmax was greater (Table 2).

Take home messages.

  1. Kale and chard Pn saturated at lower (600–800 μmol·m−2·s−1) irradiance levels than spinach Pn (1000–1200 μmol·m−2·s−1), and kale and chard may be better suited for production in low-irradiance facilities than spinach. Also, as spinach had a higher LCP (60–75 μmol·m−2·s−1) than kale (10–15 μmol·m−2·s−1), kale may be grown under lower irradiance conditions than spinach and still have an increase in mass.

  2. Kale and chard CSP were lower (600–800 ppm) than that of spinach (1000–1200 ppm). Given all CSPs reported here are higher than ambient CO2 levels, supplementing CO2 would increase the Pn of crops studied here.

  3. Ventilating greenhouses to increase CO2 from 200 to 400 ppm may result in a greater increase in Pn than that from increasing CO2 from 400 to 800 ppm.

  4. Although spinach variety Rd was similar, kale and chard variety Rd varied with some varieties having a 4-fold higher Rd than others.

  5. Low CO2 reduced kale and chard Pn more than low irradiance. Therefore, ventilating production spaces to ensure CO2 levels are at 400 ppm may increase yield more on kale and chard than on spinach.

  6. In nearly all cases (except ‘Toscano’ kale, and ‘Yellow’ and ‘Bright Lights’ chard), increasing irradiance from 300 μmol·m−2·s−1 to the LSP increased the Pn more than increasing CO2 from ambient to the CSP. This suggests irradiance may be more limiting than CO2 on these crops.

  7. When predicted daily carbon gain was calculated by taking both Pn and Rd into account, spinach carbon gain per day was lower than that of kale even though the Pmax was greater.

Literature Cited

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    • Search Google Scholar
    • Export Citation
  • Austin, R.B. 1989 Genetic variation in photosynthesis J. Agr. Sci. Camb. 112 287 294

  • Behr, U. & Wiebe, H.J. 1992 Relations between photosynthesis and nitrate content of lettuce cultivars Sci. Hort. 49 175 179

  • Bertoia, M.L., Mukamal, K.J., Cahill, L.E., Hou, T., Ludwig, D.S., Mozaffarian, D., Willett, W.C., Boese, F.B. & Huner, N.P.A. 1990 Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis Plant Physiol. 94 1830 1836

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  • Bertoia, M.L., Mukamal, K.J., Cahill, L.E., Hou, T., Ludwig, D.S., Mozaffarian, D., Willett, W.C., Hu, F.B. & Rimm, E.B. 2015 Changes in intake of fruits and vegetables and weight change in United States men and women followed for up to 24 years: Analysis from three prospective cohort studies PLOS Medicine doi: 10.1371/journal.pmed.1001878

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  • Björkman, O. 1981 Responses of different quantum flux densities, p. 57–107. In: O.L. Lange, P.S. Nobel, C.B. Osmond, and H. Ziegler (eds.). Encyclopedia of plant physiology. vol. 12A, Springer-Verlag, Berlin, Germany

  • Boese, S.R. & Huner, N.P.A. 1990 Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis Plant Physiol. 94 1830 1836

    • Search Google Scholar
    • Export Citation
  • Bunce, J.A. & Sicher, R.C. 2003 Daily irradiance and feedback inhibition of photosynthesis at elevated carbon dioxide concentration in Brassica oleracea Photosynthetica 41 4 481 488

    • Search Google Scholar
    • Export Citation
  • Bunce, J.A. & Ziska, L.H. 2000 Impact of measurement irradiance on acclimation of photosynthesis to elevated CO2 concentration in several plant species Photosynthetica 37 4 509 517

    • Search Google Scholar
    • Export Citation
  • Chagvardieff, P., d’Aletto, T. & André, M. 1994 Specific effects of irradiance and CO2 concentration doublings on productivity and mineral content in lettuce Adv. Space Res. 14 11 269 275

    • Search Google Scholar
    • Export Citation
  • Colonna, E., Rouphaei, Y., Barbieri, G. & De Pascale, S. 2016 Nutritional quality of ten leafy vegetables harvested at two light intensities Food Chem. 199 702 710

    • Search Google Scholar
    • Export Citation
  • Dahal, K., Kane, K., Gadapati, W., Webb, E., Savitch, L.V., Singh, J., Sharma, P., Sarhan, F., Longstaffe, F.J., Grodzinski, B. & Hüner, N.P.A. 2012 The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus Physiol. Plant. 144 2 169 188

    • Search Google Scholar
    • Export Citation
  • Dorais, M. 2003 The use of supplemental lighting for vegetable crop production: Light intensity, crop response, nutrition, crop management, cultural practices. Can. Greenhouse Conf. 2003, 1–8

  • Farquhar, G.D., von Caemmerer, S. & Berry, J.A. 1980 A biochemical model of CO2 assimilation in leaves of C3 species Planta 149 78 90

  • Feldmann, C. & Hamm, U. 2015 Consumers’ perceptions and preferences for local food: A review Food Qual. Prefer. 40 152 164

  • Fu, Y., Li, H., Yu, J., Liu, H., Cao, Z., Manukovsky, N.S. & Liu, H. 2017 Interaction effects of light intensity and nitrogen concentration on growth, photosynthetic characteristics and quality of lettuce (Lactuca sativa L. var. youmaicai) Sci. Hort. 214 5 51 57

    • Search Google Scholar
    • Export Citation
  • Gaudreau, L., Charbonneau, J., Vezina, L.P. & Gosselin, A. 1994 Photoperiod and PPF influence growth and quality of greenhouse-grown lettuce HortScience 29 1285 1289

    • Search Google Scholar
    • Export Citation
  • Gent, M.P.N. 2016 Effect of irradiance and temperature on composition of spinach HortScience 51 133 140

  • Goudrian, J. 1979 A family of saturation type curves, especially in relation to photosynthesis Ann. Bot. 43 783 785

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    • Search Google Scholar
    • Export Citation
  • Heuvelink, E. & Dorais, M. 2003 Crop growth and yield. In: E. Heuvelink (ed.). Tomato. CAB International, Wallingford, Oxon, UK

  • Hu, E. & Rimm, B. 2015 Changes in intake of fruits and vegetables and weight change in United States men and women followed for up to 24 years: Analysis from three prospective cohort studies PLOS Medicine 12 e1001878

    • Search Google Scholar
    • Export Citation
  • Johnson, I.R., Thornley, J., Frantz, J.M. & Bugbee, B. 2010 A model of canopy photosynthesis incorporating protein distribution through the canopy and its acclimation to light, temperature and CO2 Ann. Bot. 106 735 749

    • Search Google Scholar
    • Export Citation
  • Kaiser, E., Morales, A., Harbinson, J., Kromdijk, J., Heuvelink, E. & Marcelis, L.F.M. 2015 Dynamic photosynthesis in different environmental conditions J. Expt. Bot. 66 9 2415 2426

    • Search Google Scholar
    • Export Citation
  • Kaiser, E., Morales, A., Harbinson, J., Heuvelink, E., Prinzenberg, A.E. & Marcelis, L.F.M. 2016 Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana Sci. Rep. 6 31252

    • Search Google Scholar
    • Export Citation
  • Kitazawa, H., Motoki, S., Maeda, T., Ishikawa, Y., Hamauzu, Y., Matsushima, K., Sakai, H., Shiina, T. & Kyutoku, Y. 2011 Effects of storage temperature on the postharvest quality of three asparagus cultivars harvested in spring J. Jpn. Soc. Hort. Sci. 80 1 76 81

    • Search Google Scholar
    • Export Citation
  • Kretchen, D.W. & Howlett, F.S. 1970 CO2 enrichment for vegetable production Transactions of the ASAE 13 252 256

  • Laitat, E. & Boussard, H. 1995 Comparative response on gas exchange of Picea spp. exposed to increased atmospheric CO2 in open top chambers at two test sites, p. 241–248. Journal of Biogeography, Vol. 22, No. 2/3, Terrestrial Ecosystem Interactions with Global Change, Volume 1 (March–May 1995)

  • Lambers, H., Chapin, F.S. III & Pons, T.L. 2008 Photosynthesis, p. 11–99. Plant Physiological ecology. Springer, New York, NY

  • Marino, G., Aqil, M. & Shipley, B. 2010 The leaf economics spectrum and the prediction of photosynthetic light–response curves Funct. Ecol. 24 263 272

    • Search Google Scholar
    • Export Citation
  • Peek, M.S., Russek-Cohen, E., Wait, D.A. & Forseth, I.N. 2002 Physiological response curve analysis using nonlinear mixed models Oecologia 132 175 180

  • Pons, T.L. 2012 Interaction of temperature and irradiance effects on photosynthetic acclimation in two accessions of Arabidopsis thaliana Photosynth. Res. 113 207 219

    • Search Google Scholar
    • Export Citation
  • Potvin, C., Lechowicz, M.J. & Tardif, S. 1990 The statistical analysis of eco- physiological response curves obtained from experiments involving repeated measures Ecology 71 1389 1400

    • Search Google Scholar
    • Export Citation
  • Ruhil, K., Sheeba,, Ahmad, A., Iqbal, M. & Tripathy, B.C. 2015 Photosynthesis and growth responses of mustard (Brassica juncea L. cv Pusa Bold) plants to free air carbon dioxide enrichment Protoplasma 252 935 946

    • Search Google Scholar
    • Export Citation
  • Samuoliene, G., Brazaityte, A., Jankauskiene, J., Virsile, A., Sirtautas, R., Novickovas, A., Sakalauskaite, S. & Duchovskis, P. 2013 LED irradiance level affects growth and nutritional quality of Brassica microgreens Cent. Eur. J. Biol. 8 1241 1249

    • Search Google Scholar
    • Export Citation
  • Yamori, W., Noguchi, K. & Terashima, I. 2005 Temperature acclimation of photosynthesis in spinach leaves: Analysis of photosynthetic components and temperature dependencies of photosynthetic partial reactions Plant Cell Environ. 28 536 547

    • Search Google Scholar
    • Export Citation
  • Yu, X., Zhou, R., Wang, X., Kjaer, K.H., Rosenqvist, E., Ottosen, C. & Chen, J. 2016 Evaluation of genotypic variation during leaf development in four Cucumis genotypes and their response to high light conditions Environ. Expt. Bot. 124 100 109

    • Search Google Scholar
    • Export Citation

Contributor Notes

The authors acknowledge and appreciate the financial support of the Minnesota Agriculture Experiment Station, USDA-ARS Floriculture and Nursery Research Initiative (FNRI), National Institute of Food and Agriculture (NIFA), and members of the University of Minnesota through the Floriculture Research Alliance including Altman Plants, Inc., Rocket Farms, Inc., Smith Gardens, Inc., and Green Circle Growers, Inc.

Professor.

Research Fellow.

Corresponding author. E-mail: erwin001@umn.edu.

  • View in gallery

    Effect of increasing irradiance (A) or carbon dioxide (CO2) concentration (B) on spinach (Spinacea oleracea), kale (Brassica oleracea and B. napus pabularia), and Swiss chard (Beta vulgaris) photosynthetic rate across cultivars. Bars represent the ± mean square error as identified through analysis of variance (α < 0.05).

  • Aleric, K.M. & Kirkman, K.L. 2005 Growth and photosynthetic responses of the federally endangered shrub, Lindera melissifolia (Lauraceae), to varied light environments Amer. J. Bot. 92 682 689

    • Search Google Scholar
    • Export Citation
  • Austin, R.B. 1989 Genetic variation in photosynthesis J. Agr. Sci. Camb. 112 287 294

  • Behr, U. & Wiebe, H.J. 1992 Relations between photosynthesis and nitrate content of lettuce cultivars Sci. Hort. 49 175 179

  • Bertoia, M.L., Mukamal, K.J., Cahill, L.E., Hou, T., Ludwig, D.S., Mozaffarian, D., Willett, W.C., Boese, F.B. & Huner, N.P.A. 1990 Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis Plant Physiol. 94 1830 1836

    • Search Google Scholar
    • Export Citation
  • Bertoia, M.L., Mukamal, K.J., Cahill, L.E., Hou, T., Ludwig, D.S., Mozaffarian, D., Willett, W.C., Hu, F.B. & Rimm, E.B. 2015 Changes in intake of fruits and vegetables and weight change in United States men and women followed for up to 24 years: Analysis from three prospective cohort studies PLOS Medicine doi: 10.1371/journal.pmed.1001878

    • Search Google Scholar
    • Export Citation
  • Björkman, O. 1981 Responses of different quantum flux densities, p. 57–107. In: O.L. Lange, P.S. Nobel, C.B. Osmond, and H. Ziegler (eds.). Encyclopedia of plant physiology. vol. 12A, Springer-Verlag, Berlin, Germany

  • Boese, S.R. & Huner, N.P.A. 1990 Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis Plant Physiol. 94 1830 1836

    • Search Google Scholar
    • Export Citation
  • Bunce, J.A. & Sicher, R.C. 2003 Daily irradiance and feedback inhibition of photosynthesis at elevated carbon dioxide concentration in Brassica oleracea Photosynthetica 41 4 481 488

    • Search Google Scholar
    • Export Citation
  • Bunce, J.A. & Ziska, L.H. 2000 Impact of measurement irradiance on acclimation of photosynthesis to elevated CO2 concentration in several plant species Photosynthetica 37 4 509 517

    • Search Google Scholar
    • Export Citation
  • Chagvardieff, P., d’Aletto, T. & André, M. 1994 Specific effects of irradiance and CO2 concentration doublings on productivity and mineral content in lettuce Adv. Space Res. 14 11 269 275

    • Search Google Scholar
    • Export Citation
  • Colonna, E., Rouphaei, Y., Barbieri, G. & De Pascale, S. 2016 Nutritional quality of ten leafy vegetables harvested at two light intensities Food Chem. 199 702 710

    • Search Google Scholar
    • Export Citation
  • Dahal, K., Kane, K., Gadapati, W., Webb, E., Savitch, L.V., Singh, J., Sharma, P., Sarhan, F., Longstaffe, F.J., Grodzinski, B. & Hüner, N.P.A. 2012 The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus Physiol. Plant. 144 2 169 188

    • Search Google Scholar
    • Export Citation
  • Dorais, M. 2003 The use of supplemental lighting for vegetable crop production: Light intensity, crop response, nutrition, crop management, cultural practices. Can. Greenhouse Conf. 2003, 1–8

  • Farquhar, G.D., von Caemmerer, S. & Berry, J.A. 1980 A biochemical model of CO2 assimilation in leaves of C3 species Planta 149 78 90

  • Feldmann, C. & Hamm, U. 2015 Consumers’ perceptions and preferences for local food: A review Food Qual. Prefer. 40 152 164

  • Fu, Y., Li, H., Yu, J., Liu, H., Cao, Z., Manukovsky, N.S. & Liu, H. 2017 Interaction effects of light intensity and nitrogen concentration on growth, photosynthetic characteristics and quality of lettuce (Lactuca sativa L. var. youmaicai) Sci. Hort. 214 5 51 57

    • Search Google Scholar
    • Export Citation
  • Gaudreau, L., Charbonneau, J., Vezina, L.P. & Gosselin, A. 1994 Photoperiod and PPF influence growth and quality of greenhouse-grown lettuce HortScience 29 1285 1289

    • Search Google Scholar
    • Export Citation
  • Gent, M.P.N. 2016 Effect of irradiance and temperature on composition of spinach HortScience 51 133 140

  • Goudrian, J. 1979 A family of saturation type curves, especially in relation to photosynthesis Ann. Bot. 43 783 785

  • Gu, J., Yin, X., Stomph, T., Wang, H. & Struik, P.C. 2012 Physiological basis of genetic variation in leaf photosynthesis among rice (Oryza sativa L.) introgression lines under drought and well-watered conditions J. Expt. Bot. 63 14 5137 5153

    • Search Google Scholar
    • Export Citation
  • Heuvelink, E. & Dorais, M. 2003 Crop growth and yield. In: E. Heuvelink (ed.). Tomato. CAB International, Wallingford, Oxon, UK

  • Hu, E. & Rimm, B. 2015 Changes in intake of fruits and vegetables and weight change in United States men and women followed for up to 24 years: Analysis from three prospective cohort studies PLOS Medicine 12 e1001878

    • Search Google Scholar
    • Export Citation
  • Johnson, I.R., Thornley, J., Frantz, J.M. & Bugbee, B. 2010 A model of canopy photosynthesis incorporating protein distribution through the canopy and its acclimation to light, temperature and CO2 Ann. Bot. 106 735 749

    • Search Google Scholar
    • Export Citation
  • Kaiser, E., Morales, A., Harbinson, J., Kromdijk, J., Heuvelink, E. & Marcelis, L.F.M. 2015 Dynamic photosynthesis in different environmental conditions J. Expt. Bot. 66 9 2415 2426

    • Search Google Scholar
    • Export Citation
  • Kaiser, E., Morales, A., Harbinson, J., Heuvelink, E., Prinzenberg, A.E. & Marcelis, L.F.M. 2016 Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana Sci. Rep. 6 31252

    • Search Google Scholar
    • Export Citation
  • Kitazawa, H., Motoki, S., Maeda, T., Ishikawa, Y., Hamauzu, Y., Matsushima, K., Sakai, H., Shiina, T. & Kyutoku, Y. 2011 Effects of storage temperature on the postharvest quality of three asparagus cultivars harvested in spring J. Jpn. Soc. Hort. Sci. 80 1 76 81

    • Search Google Scholar
    • Export Citation
  • Kretchen, D.W. & Howlett, F.S. 1970 CO2 enrichment for vegetable production Transactions of the ASAE 13 252 256

  • Laitat, E. & Boussard, H. 1995 Comparative response on gas exchange of Picea spp. exposed to increased atmospheric CO2 in open top chambers at two test sites, p. 241–248. Journal of Biogeography, Vol. 22, No. 2/3, Terrestrial Ecosystem Interactions with Global Change, Volume 1 (March–May 1995)

  • Lambers, H., Chapin, F.S. III & Pons, T.L. 2008 Photosynthesis, p. 11–99. Plant Physiological ecology. Springer, New York, NY

  • Marino, G., Aqil, M. & Shipley, B. 2010 The leaf economics spectrum and the prediction of photosynthetic light–response curves Funct. Ecol. 24 263 272

    • Search Google Scholar
    • Export Citation
  • Peek, M.S., Russek-Cohen, E., Wait, D.A. & Forseth, I.N. 2002 Physiological response curve analysis using nonlinear mixed models Oecologia 132 175 180

  • Pons, T.L. 2012 Interaction of temperature and irradiance effects on photosynthetic acclimation in two accessions of Arabidopsis thaliana Photosynth. Res. 113 207 219

    • Search Google Scholar
    • Export Citation
  • Potvin, C., Lechowicz, M.J. & Tardif, S. 1990 The statistical analysis of eco- physiological response curves obtained from experiments involving repeated measures Ecology 71 1389 1400

    • Search Google Scholar
    • Export Citation
  • Ruhil, K., Sheeba,, Ahmad, A., Iqbal, M. & Tripathy, B.C. 2015 Photosynthesis and growth responses of mustard (Brassica juncea L. cv Pusa Bold) plants to free air carbon dioxide enrichment Protoplasma 252 935 946

    • Search Google Scholar
    • Export Citation
  • Samuoliene, G., Brazaityte, A., Jankauskiene, J., Virsile, A., Sirtautas, R., Novickovas, A., Sakalauskaite, S. & Duchovskis, P. 2013 LED irradiance level affects growth and nutritional quality of Brassica microgreens Cent. Eur. J. Biol. 8 1241 1249

    • Search Google Scholar
    • Export Citation
  • Yamori, W., Noguchi, K. & Terashima, I. 2005 Temperature acclimation of photosynthesis in spinach leaves: Analysis of photosynthetic components and temperature dependencies of photosynthetic partial reactions Plant Cell Environ. 28 536 547

    • Search Google Scholar
    • Export Citation
  • Yu, X., Zhou, R., Wang, X., Kjaer, K.H., Rosenqvist, E., Ottosen, C. & Chen, J. 2016 Evaluation of genotypic variation during leaf development in four Cucumis genotypes and their response to high light conditions Environ. Expt. Bot. 124 100 109

    • Search Google Scholar
    • Export Citation
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