Long-term CO2 Enrichment Increases Biomass but Results in Rapid Physiological Acclimation of Petunia and Pansy

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David W. McKinney Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Avenue, Fort Collins, CO 80521-1173, USA

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Joshua K. Craver Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Avenue, Fort Collins, CO 80521-1173, USA

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Abstract

Although crops often respond immediately to enriched CO2 concentrations (e.g., increased photosynthesis), this initial response is often not sustained throughout production, thus reducing the benefit of this input. For horticulture species, the timing and extent of these acclimation responses are still widely uncertain. Therefore, the objective of this research was to determine species-specific acclimation responses to elevated CO2 concentrations for pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’) and petunia (Petunia ×hybrida ‘Dreams Midnight’). Seedlings were transplanted to 11.5-cm pots and placed in growth chambers with air temperature, relative humidity, and radiation intensity setpoints of 21 °C, 55%, and 250 μmol⋅m2⋅s1, respectively. Carbon dioxide treatments were established using the two growth chambers with setpoints of either 400 (ambient) or 1000 μmol⋅mol−1 (elevated) maintained during a 16-hour photoperiod. In addition to data collected through destructive harvest, the rate of photosynthesis (A) in response to increasing internal leaf CO2 concentration (A-Ci) and at the operating CO2 concentration (A-Ca) were measured weekly with a portable leaf photosynthesis system at saturating [A-Ci (1000 μmol⋅m2⋅s1)] or production [A-Ca (250 μmol⋅m2⋅s1)] radiation intensities. For both pansy and petunia, elevated CO2 produced greater total shoot dry mass than ambient CO2 after 4 weeks. However, the decreased maximum rate of photosynthetic electron transport, maximum rate of Rubisco carboxylase, and triose phosphate utilization rate of both species were also observed under elevated CO2. Similarly, A measured at 400 and 1000 μmol⋅mol−1 was reduced for both pansy and petunia grown under the elevated compared with ambient CO2 concentration based on A-Ca responses after 7 days, indicating quick physiological acclimation to this input. These results provide information regarding the timing and extent of physiological acclimation in response to elevated CO2 concentrations. However, because of physiological acclimation potentially occurring within 7 days of treatment initiation, additional research is necessary to develop species-specific recommendations for controlled environment production.

Floriculture crops in the United States had an estimated wholesale value of $4.77 billion in 2018, with annual bedding plants comprising approximately one-third of this total (US Department of Agriculture, National Agricultural Statistics Service 2019). Although the average ambient CO2 concentration currently exceeds 400 μmol⋅mol−1, concentrations in the greenhouse environment commonly decrease to less than 200 μmol⋅mol−1 during production in the winter and early spring (Both et al. 2017; Erwin and Gesick 2017; Mortensen 1987). However, the current atmospheric concentration does not maximize photosynthetic capacity; therefore, there is potential to enhance plant growth by enriching controlled environments with CO2 (Mortensen 1987; Mortensen and Moe 1992). Studies have shown that CO2 concentrations between 800 and 1200 μmol⋅mol−1 have great potential to increase plant growth, with concentrations more than 900 μmol⋅mol−1 nearly eliminating photorespiration (Erwin and Gesick 2017; Gunderson and Wullschleger 1994; Mortensen 1987). However, previous studies have established that the most practical CO2 concentration range for most species is 600 to 1000 μmol⋅mol−1 (Mortensen 1987). Early short-term studies showed that an economically efficient way to enhance ornamental plant growth in controlled environments was to increase the CO2 concentration within this target range (Mortensen 1987; Prior et al. 2011).

Short-duration experiments concluded that elevated CO2 immediately stimulates photosynthetic rates up to 58%, leading to increased carbon assimilation and plant growth (Drake et al. 1997; Kirschbaum and Lambie 2015; Prior et al. 2003, 2011). For instance, Mortenson (1986) found that the net photosynthetic rate increased by 50% in chrysanthemum (Chrysanthemum morifolium ‘Horim’) when grown at 900 μmol⋅mol−1 CO2 for 5 d compared with plants grown at ambient CO2 concentrations. Additional commonly observed short-term responses to elevated CO2 concentrations include reduced stomatal conductance and reduced transpiration, leading to improved water-use efficiency (Ainsworth and Long 2004; Anderson et al. 2001; Drake et al. 1997). For example, Mortensen (1987) concluded that an elevated CO2 concentration can improve water-use efficiency by 30%, possibly because of reduced stomatal aperture and transpiration. Similarly, Drake et al. (1997) showed that stomatal conductance was reduced by an average of 20% across 41 observations covering 28 species. These short-term responses to elevated CO2 show potential for enhancing plant growth while possibly contributing to fewer production inputs (Both et al. 2017). However, the benefit of an increased photosynthetic rate observed with elevated CO2 is not often realized throughout production.

Long-term exposure to elevated CO2 concentrations results in many morphological and physiological responses. Elevated CO2 often shows an increase in carbohydrate concentration in plant tissues, usually resulting in increased biomass (Drake et al. 1997; Erwin and Gesick 2017; Frantz and Ling 2011; Kirschbaum 2011). For example, Zhang et al. (2012) found that elevated CO2 (760 μmol⋅mol−1) increased the soluble sugar content by 78.8% and starch by 122.4% in New Guinea impatiens (Impatiens hawkeri). This increase in carbohydrate concentration in response to elevated CO2 concentrations not only increases aboveground biomass but also tends to specifically increase the leaf mass area (LMA) (Frantz and Ling 2011; Giri et al. 2016; Mortensen and Moe 1992; Mortensen and Ulsaker 1985; Prior et al. 2011). However, long-term exposure to elevated CO2 concentrations has been correlated with a reduction in photosynthetic capacity and decreased biochemical processes of photosynthesis, showing diminishing positive return for this input (Ainsworth and Long 2004, 2021; Dillon et al. 2018; Drake et al. 1997; Gunderson and Wullschleger 1994; Kirschbaum and Lambie 2015). One indicator of photosynthetic acclimation is the decreased maximum rate of Rubisco carboxylase (Vcmax) and photosynthetic electron transport (Jmax). Specifically, a reduction in the Rubisco content is commonly observed among C3 plants in response to growth under an elevated CO2 concentration, thus reducing the potential benefit to photosynthesis under this condition (Ainsworth and Long 2021). Photosynthetic acclimation is also accompanied by a decreased triose phosphate utilization (TPU) rate, indicating an excess of carbohydrates outpacing utilization (Dahal and Vanlerberghe 2018; Lombardozzi et al. 2018; Yang et al. 2016). However, impacts of CO2 concentration on biomass, leaf area (LA), net photosynthetic rate, and other photosynthetic biochemical processes, as well as the magnitude of acclimation responses, have been found to vary among species and cultivars while also being dependent on production practices and inputs (Ainsworth and Long 2021; Anderson et al. 2001; Erwin and Gesick 2017; Frantz and Ling 2011; Giri et al. 2016; Pérez-López et al. 2015).

Early studies have suggested intermittent CO2 application possibly bypasses the photosynthetic acclimation response to elevated CO2 (Frantz and Ling 2011; Kirschbaum and Lambie 2015; Mortensen and Moe 1992; Prior et al. 2011). These studies evaluated intermittent CO2 elevation over a few hours rather than continuous daily elevation, which did not show benefits for African violet (Saintpaulia ionantha ‘Nicole’, ‘Lena’, and ‘Rosa Roccoco’) (Mortensen 1986), soybean (Glycine max ‘Fiskeby V’) (Clough and Peet 1981), and tomato (Solanum lycopersicum ‘Virosa’) (Calvert and Slack 1976) compared with plants grown at ambient concentrations. Frantz and Ling (2011) suggested that to bypass the detrimental effects of long-term exposure, elevated CO2 can be applied short-term during a few days or weeks at a time. Jones et al. (1985) showed that photosynthesis could be returned to its original rate before acclimation with a 5-d break from elevated CO2 for soybean, suggesting a duration component to CO2 application and possible success with oscillation. As a result, studies call for more research of responses to short-term CO2 elevation at varying stages of plant development (Frantz and Ling 2011; Kirschbaum and Lambie 2015; Mortensen 1987; Mortensen and Moe 1992; Prior et al. 2011).

Horticulture species have received much less attention compared with agronomic and forest species when it comes to evaluating the effects of elevated CO2, and research to support the benefit of long-term elevated CO2 during production is lacking (Prior et al. 2011). This lack of information is especially prevalent among the diverse range of floriculture crops. Previous studies have shown potential for long-term CO2 elevation to be beneficial for ornamental plant production during the finishing stage; however, research is still needed to evaluate the extent and timing of morphological and physiological responses to elevated CO2 application by horticultural species (Frantz and Ling 2011; Kirschbaum and Lambie 2015; Mortensen 1987; Mortensen and Moe 1992; Prior et al. 2011). By further evaluating these responses of horticulture species, programs can be developed by establishing best management practices for elevated CO2, including the timing and duration of exposure, based on the production stage. Therefore, the objective of this study was to evaluate species-specific morphological and physiological responses to long-term exposure of elevated CO2 concentrations in controlled environments for petunia (Petunia ×hybrida ‘Dreams Midnight’) and pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’) to determine the timing and extent of potential acclimation responses. These species were selected based on their relevance to the horticulture industry and similar production time.

Materials and Methods

Plant material and germination environment.

Petunia ‘Dreams Midnight’ and pansy ‘Matrix Blue Blotch Improved’ seeds were sown in 128-cell trays (14-mL individual cell volume) filled with commercial germination mix comprising (by volume) 80% fine sphagnum peat, 10% perlite, and 10% vermiculite (BM2 Germinating Mix; Berger Horticultural Products Ltd., Saint-Modeste, Quebec City, Canada). Trays were immediately placed in a reach-in growth chamber (PG2500; Conviron, Winnipeg, Manitoba, Canada) with air temperature, relative humidity, and CO2 concentration setpoints of 21 °C, 55%/65% day/night, and 400 μmol⋅mol−1, respectively. Light was provided by light-emitting diode (LED) fixtures (GreenPower LED DR/W production modules; Signify, Eindhoven, The Netherlands) with a 16-h photoperiod (0800–0000 HR) and an average photosynthetic photon flux density (PPFD) at canopy height of 250 μmol⋅m−2⋅s−1. Seedlings were irrigated daily with water-soluble fertilizer at a concentration of 150 mg⋅L−1 N (Jack’s LX 13N–0.9P–10.8K Plug Formula for High Alkalinity Water; JR Peters Inc., Allentown, PA, USA). Other macronutrients and micronutrients contained in the fertilizer were (in mg⋅L−1) 22.5 P, 150 K, 69 Ca, 34.5 Mg, 0.15 B, 0.075 Cu, 0.75 Fe, 0.375 Mn, 0.075 Mo, and 0.375 Zn. Seedlings were thinned to one plant per cell 4 d after germination.

Growth chamber environment.

At 28 d after germination, 40 uniform seedlings were randomly selected and transplanted into 11.4-cm (550 mL) containers using commercial potting media comprising (by volume) 85% sphagnum peat and 15% perlite (BM6 Growing Mix; Berger Horticultural Products Ltd.). Twenty plants were randomly assigned to one of two reach-in growth chambers (PG2500), with each maintaining a CO2 concentration treatment setpoint of either 400 (ambient) or 1000 μmol⋅mol−1 (elevated) during the established 16-h photoperiod with injection controlled using a CO2 gas analyzer (LI-830; LI-COR Inc., Lincoln, NE, USA). The CO2 concentration in each chamber was measured over the 16-h photoperiod using a CO2 probe (GMP252; Vaisala, Woburn, MA, USA), with means ± SD over the 16-h photoperiod of 425 ± 55 and 1014 ± 84 μmol⋅mol−1 for ambient and elevated conditions, respectively, across three experimental replications. The CO2 setpoints were alternated between growth chambers for each replication to randomize for chamber effects. Fixed mounted infrared thermocouples with acrylonitrile butadiene styrene plastic housing (OS36-01-T-80F; Omega Engineering Inc., Norwalk, CT, USA) were installed in each chamber to measure leaf temperature, with means ± SD of 21 ± 0.6 and 21 ± 0.4 °C, and precision thermistors (ST-100; Apogee Instruments Inc., Logan, UT, USA) were used to measure air temperature, with means ± SD of 21 ± 0.1 and 21 ± 0.1 °C for ambient and elevated conditions, respectively. Relative humidity probes (EE-08-SS; Apogee Instruments Inc.) were installed in each chamber to measure relative humidity, with means ± SD of 62% ± 11% and 63% ± 9% during the day and 70% ± 6% and 70% ± 3% during the night for ambient and elevated conditions, respectively. Radiation quality and intensity were measured at the beginning of each experimental replication by taking 17 spectral scans per treatment using a spectrometer (LI-180, LI-COR Inc.) at canopy height averaging 250 ± 15 and 252 ± 15 μmol⋅m−2⋅s−1 for ambient and elevated conditions, respectively. Environmental setpoints were measured every 30 s, and the average was logged every 15 min by a data logger (model CR1000X; Campbell Scientific, Logan, UT, USA). Plants were irrigated as needed with water-soluble fertilizer at a concentration of 150 mg⋅L−1 N (Jack’s LX 21N–2.2P–16.6K All Purpose Formula for High Alkalinity Water; JR Peters Inc.). Other macronutrients and micronutrients contained in the fertilizer were (in mg⋅L−1) 36 P, 142.5 K, 1.05 Mg, 0.15 B, 0.075 Cu, 0.75 Fe, 0.375 Mn, 0.075 Mo, and 0.375 Zn.

Gas exchange data collection.

Gas exchange measurements were collected using a portable photosynthesis meter (LI-6800, LI-COR Inc.). The rate of photosynthesis (A) in response to the increasing internal leaf CO2 concentration (A-Ci) was determined using a combined 6 cm2 leaf chamber and light source (LI-6800–01A Multiphase Flash Fluorometer; LI-COR Inc.). Measurements were collected beginning 7 d after transplant and continued every 7 d, for a total of 28 d. For each day of data collection, the most recent fully expanded leaf of five plants from each treatment was selected for gas exchange measurements. For plants grown in the ambient treatment, the CO2 concentration inside the cuvette was decreased from 400 to 50 μmol⋅mol−1, returned to 400 μmol⋅mol−1, and then increased to a maximum of 1000 μmol⋅mol−1 in steps of 100 μmol⋅mol−1 to prevent feedback inhibition during measurements. For plants grown in the elevated treatment, the CO2 concentration inside the cuvette was decreased from the maximum level of 1000 to 50 μmol⋅mol−1 in steps of 100 μmol⋅mol−1. Two minutes of acclimation were allowed at each step before measuring. Cuvette leaf temperature and relative humidity matched the growth chamber environment. An LED light source provided a PPFD of 1000 μmol⋅m−2⋅s−1 to achieve light saturation. The Plantecophys package (Duursma 2015), an R package for analyzing and modeling leaf gas exchange data, was used to determine photosynthesis parameters by fitting individual A-Ci curves with the fitaci function. The curves were analyzed at leaf temperature, with the TPU limitation set at the measured vapor pressure deficit. The TPU was used in the model to estimate differences more accurately for photosynthetic measurements (Lombardozzi et al. 2018; Yang et al. 2016). Estimates included Vcmax and Jmax. The photosyn function from the Plantecophys package was used to estimate stomatal conductance (Gs) (Duursma 2015). Additional gas exchange measurements were collected from five test plants per treatment to determine the photosynthetic rate under operating conditions (A-Ca), specifically at a target PPFD of 250 μmol⋅m−2⋅s−1. For plants grown in the ambient treatment, the CO2 concentration inside the cuvette was increased from 400 to 1000 μmol⋅mol−1. For plants grown in the elevated treatment, the CO2 concentration inside the cuvette was decreased from 1000 to 400 μmol⋅mol−1. Cuvette leaf temperature and relative humidity matched the growth chamber environment.

Morphological data collection.

Immediately after obtaining gas exchange measurements, plants were harvested. The relative chlorophyll content (RCC) (SPAD-502 Chlorophyll Meter; Konica Minolta Inc., Chiyoda City, Tokyo, Japan) was collected from the most recent fully expanded leaf. The number of leaves was determined by removing the leaves at the axil, and the LA (cm2) was measured using an LA meter (LI-3100C; LI-COR Inc.). The stem caliper (mm) was measured just above the hypocotyl and at the junction of the first axillary bud. The stem length (cm) from the apical bud to the soil line was measured. Then, leaves and stems were dried in a forced-air oven maintained at 70 °C to determine the leaf dry mass (LDM) (mg) and shoot dry mass (SDM) (stems plus leaves) (mg). The LMA (mg/cm2) was calculated using the measured values for the LDM and LA. Flowering data of plants harvested at day 28, including time to flower (d) and number of flowers, were collected.

Statistical analysis.

The analysis was performed using R statistical software (R Core Team 2022) and the lme4, lmerTest, and emmeans packages (Bates et al. 2015; Kuznetsova et al. 2017). One observational unit was one measurement per plant, with a total of 60 observations. A mixed model was fit using morphological data collected (continuous) as the response. Fixed effects included CO2 treatment (categorical: 400 and 1000 μmol⋅mol−1). Repetition (categorical: 1, 2, and 3) was included as a random effect to account for the split plot design. CO2 treatments were compared using Tukey adjusted pairwise comparisons.

Model assumptions of linearity and equal scatter were both satisfied and checked using residual diagnostic plots. Week (harvest time) was not included in the model, but each week (1, 2, 3, and 4) was treated as a discrete event. No trend over time was tested. This model was chosen with repetition as random to account for the effect of randomizing the chambers between repetitions. This allowed the analysis to show the comparisons between the CO2 treatments accounting for the effect of any possible differences between environments in the chambers. After the model was tested with the rand() function (Kuznetsova et al. 2017), the random effect was found to be statistically significant, thus justifying its use in the model.

Results

Morphological data.

Stem caliper and length showed no difference between CO2 treatments for petunia for all harvest days (Table 1). However, pansy stem caliper and stem length on day 21 were 10% and 6% greater under elevated compared with ambient conditions, respectively (Table 2). Differences were not observed for pansy stem caliper and stem length for any other harvest days (Table 2). Leaf number was 13% greater under elevated conditions for petunia compared with ambient conditions on day 7, with no differences observed for any other harvest day (Table 1). For pansy, the leaf number was similar between CO2 treatments for all harvest days (Table 2). The LA was only different between CO2 treatments on day 14 for both species, with a 13% and 14% increase under elevated conditions compared with ambient conditions for petunia and pansy, respectively (Tables 1 and 2). Petunia RCC only showed differences on day 21, with 14% greater RCC observed under elevated conditions compared with ambient conditions (Table 1). No differences in RCC were observed for pansy on any harvest day (Table 2).

Table 1.

Morphological data for petunia (Petunia ×hybrida ‘Dreams Midnight’), including stem caliper, stem length, leaf number, leaf area (LA), leaf dry mass (LDM), shoot dry mass (SDM), leaf mass area (LMA), and relative chlorophyll content (RCC). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated) and harvested at 7, 14, 21, and 28 d after experiment initiation.

Table 1.
Table 2.

Morphological data for pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’) including stem caliper, stem length, leaf number, leaf area (LA), leaf dry mass (LDM), shoot dry mass (SDM), leaf mass area (LMA), and relative chlorophyll content (RCC). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated) and harvested at 7, 14, 21, and 28 d after experiment initiation.

Table 2.

For petunia, differences in LDM were observed on days 7, 14, and 21, with the highest values observed under elevated conditions. For example, on day 21, LDM for plants grown under elevated conditions was 22% greater than those grown under ambient conditions (Table 1). Similarly, LDM for pansy was greatest under elevated conditions on days 7, 14, and 21. Specifically, on day 21, LDM was 17% greater under elevated conditions compared with ambient conditions (Table 2). However, on day 28, no difference in LDM between ambient conditions and elevated conditions was observed for either species (Tables 1 and 2). Differences in SDM for petunia and pansy were observed on all harvest dates, with greater biomass accumulation under elevated conditions compared with ambient conditions. For example, petunia SDM on days 7, 14, 21, and 28 were 15.6%, 21.6%, 26%, and 19.2% greater under elevated conditions compared with ambient conditions, respectively (Table 1). Similarly, pansy SDM on days 7, 14, 21, and 28 were 26%, 28.8%, 21.9%, and 14.9% greater under elevated conditions compared with ambient conditions, respectively (Table 2).

For petunia, LMA differed between treatments on days 14, 21, and 28, with the highest values observed for plants grown under elevated conditions. For instance, on day 28, petunia LMA under elevated conditions was 9% greater than that under ambient conditions (Table 1). Comparably, pansy LMA was greater under elevated conditions compared with ambient conditions on days 7, 14, and 28 (Table 2). Specifically, on day 28, pansy LMA was 17% greater under elevated compared with ambient conditions (Table 2). There were no observable differences in time to flower or number of flowers for either species (Table 3).

Table 3.

Flowering data for petunia (Petunia ×hybrida ‘Dreams Midnight’) and pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’), including time to flower and number of flowers at harvest. Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated) and data of plants harvested at 28 d after experiment initiation were collected.

Table 3.

Gas exchange data.

Higher Vcmax values were observed for petunia under ambient conditions on all measurement days. For example, Vcmax was 27% greater under ambient conditions than under elevated conditions on day 28 (Table 4). Similarly, higher Vcmax values were observed for pansy under ambient conditions on days 14, 21, and 28. On day 28, Vcmax for pansy grown under ambient conditions was 20% greater than under elevated conditions (Table 5). Petunia Jmax differed on all measurement days between CO2 treatments, with higher values observed for plants grown under ambient conditions compared with those grown under elevated conditions. For instance, on day 28, Jmax for petunia was 7% greater under ambient conditions than under elevated conditions (Table 4). Differences in Jmax for pansy were observed on days 14, 21, and 28, with the highest values under ambient conditions. Specifically, Jmax was 27% greater under ambient conditions than under elevated conditions for pansy on day 28 (Table 5).

Table 4.

Parameters estimated from photosynthetic (A) responses to increasing internal leaf CO2 concentrations (Ci) for petunia (Petunia ×hybrida ‘Dreams Midnight’), including maximum photosynthetic rate of Rubisco carboxylation (Vcmax), maximum rate of photosynthetic electron transport (Jmax), triose phosphate utilization (TPU) rate, and stomatal conductance measured at the operating point (Gs; 400 and 1000 μmol⋅mol−1 CO2 for ambient and elevated conditions, respectively). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated). Gas exchange measurements were obtained using a portable photosynthesis meter (LI-6400XT; LI-COR Inc., Lincoln, NE, USA) at 7, 14, 21, and 28 d after experiment initiation.

Table 4.
Table 5.

Parameters estimated from photosynthetic (A) responses to increasing internal CO2 concentrations (Ci) for pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’), including maximum photosynthetic rate of Rubisco carboxylation (Vcmax), maximum rate of photosynthetic electron transport (Jmax), triose phosphate utilization (TPU) rate, and stomatal conductance measured at the operating point (Gs; 400 and 1000 μmol⋅mol−1 CO2 for ambient and elevated conditions, respectively). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated). Gas exchange measurements were obtained using a portable photosynthesis meter (LI-6400XT; LI-COR Inc., Lincoln, NE, USA) at 7, 14, 21, and 28 d after experiment initiation.

Table 5.

A reduced TPU was observed for petunia grown under elevated conditions on all measurement days. For example, on day 28, petunia TPU was 15% greater under ambient conditions than under elevated conditions (Table 4). Similarly, pansy TPU was reduced under elevated conditions on days 14, 21, and 28. For instance, on day 28, TPU under ambient conditions was 15% greater than under elevated conditions (Table 5). For Gs measured at operating point (measured at the CO2 concentration of respective treatment environment), values were greater under ambient conditions for both species on all measurement days. For example, on day 28, Gs under ambient conditions was 103% and 71% greater than under elevated conditions for petunia and pansy, respectively (Tables 4 and 5).

The net photosynthetic rate for petunia and pansy measured at 400 μmol⋅mol−1 CO2 under operating conditions was greater for plants grown under ambient conditions than for plants grown under elevated conditions for all measurement days (Fig. 1). For example, the net photosynthetic rates of petunia at a CO2 concentration of 400 μmol⋅mol−1 were 36%, 27%, 27%, and 23% greater for plants grown under ambient conditions than for plants grown under elevated conditions on days 7, 14, 21, and 28, respectively. For pansy, the net photosynthetic rates at a CO2 concentration of 400 μmol⋅mol−1 were 28%, 17%, 19%, and 14% greater under ambient conditions than under elevated conditions on days 7, 14, 21, and 28, respectively. The net photosynthetic rates measured at 1000 μmol⋅mol−1 CO2 under operating conditions were also significant for all measurement days for both species (Fig. 1). Specifically, the net photosynthetic rates of petunia at a CO2 concentration of 1000 μmol⋅mol−1 were 21%, 17%, 16%, and 19% greater under ambient conditions than under elevated conditions on days 7, 14, 21, and 28, respectively. Similarly, the net photosynthetic rates at 1000 μmol⋅mol−1 CO2 were 16%, 9%, 9%, and 11% greater for pansy grown under ambient conditions than under elevated conditions on days 7, 14, 21, and 28, respectively.

Fig. 1.
Fig. 1.

Net photosynthetic rate measured at 400 and 1000 μmol⋅mol−1 CO2 for petunia (Petunia ×hybrida ‘Dreams Midnight’) and pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated). Gas exchange measurements were obtained using a portable photosynthesis meter (LI-6400XT; LI-COR Inc., Lincoln, NE, USA) at 7 (A and B), 14 (C and D), 21 (E and F), and 28 (G and H) d after experiment initiation with cuvette conditions matching the production environment; specifically, leaf temperature, relative humidity, and photosynthetic photon flux density (PPFD) were 21 °C, 55%, and 250 μmol⋅m−2⋅s−1, respectively. A significant difference between CO2 treatments was observed at both CO2 concentrations on all data collection days for both species according to Tukey’s honest significant difference (HSD) test at P ≤ 0.05. No trends over time or between measurements collected at the two CO2 concentrations were tested.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05304-23

Discussion

Morphological data.

In the present study, elevated CO2 had little effect on stem caliper and stem length for pansy or petunia. Similarly, the leaf number and LA showed a limited response to elevated CO2 compared with ambient CO2 for both species, with differences only observable before day 14. An adjustment in shoot growth rate may be attributable to a sink limitation response; as the plant reaches maximum capacity for root growth in its container, the shoot growth rate becomes restricted while the carbohydrate concentration increases, as indicated by an increase in biomass and LMA (Arp 1991). This is consistent with previous research of petunia ‘Madness White’; 5 weeks at 800 μmol⋅mol−1 CO2 had no significant influence on stem morphology compared with that under ambient conditions (Frantz and Ling 2011). Similarly, Frantz and Ling (2011) found no change in leaf number or LA for petunia ‘Madness White’ after 5 weeks of exposure to 800 μmol⋅mol−1 CO2 compared with those under ambient conditions, showing that long-term exposure to CO2 may reduce the benefit to plant growth that is expected when using short-term predictions (Mortensen 1987; Mortensen and Ulsaker 1985). Although short-term studies predict large differences in LA, long-term studies show no change in the total LA in response to elevated CO2 across many species, indicating that a response to elevated CO2 may be acclimation of the growth rate compared with initial increases in ontogeny (Drake et al. 1997; Gunderson and Wullschleger 1994). There is also the possibility of sink limitation combined with an inability to metabolize accumulated carbohydrates. A common response during long-term CO2 studies is that as plants fill their container, their ability to use carbon for plant growth becomes limited. Carbon accumulates rather than being used for plant growth, and this inability to metabolize carbohydrates reduces the potential for plant growth stimulation and dampens photosynthesis (Arp 1991; Frantz and Ling 2011; Makino and Mae 1999). Although the growth rate of the shoot may acclimate to elevated CO2 over the long-term with no differences in stem caliper or length and LA or leaf number, plants commonly respond with increased biomass and LMA (Frantz and Ling 2011; Gislerod and Nelson 1989; Mortensen and Ulsaker 1985).

In the present study, LDM was greater for plants grown at an elevated CO2 concentration on days 7, 14, and 21, but not on day 28, for both species, possibly indicating acclimation of leaf mass to elevated CO2. Furthermore, SDM was greatest under elevated conditions for both species on all harvest dates. Increased aboveground biomass in response to elevated CO2 is a common response across species during long-term studies (Frantz and Ling 2011; Mortensen 1987; Mortensen and Moe 1992; Prior et al. 2011). However, previous studies have also concluded that long-term exposure to elevated CO2 does not sustain increased biomass (Frantz and Ling 2011). Specifically, Frantz and Ling (2011) found that LDM was unaffected by elevated CO2 compared with ambient conditions for petunia ‘Madness White’ after 7 weeks of exposure to 800 μmol⋅mol−1 CO2, with a 10% increase in LDM at 5 weeks. However, the present study observed plants grown at 1000 rather than 800 μmol⋅mol−1 CO2, possibly hastening this response. Similar LDM between CO2 treatments on day 28 can be attributed to multiple factors. The photosynthetic rate had been reduced, possibly causing a decrease in leaf carbohydrate content, and flower initiation began after day 21, possibly opening up new sinks for carbohydrates to be used for plant growth. Although LDM showed no difference after 28 d, SDM showed an increase in biomass at elevated CO2 for every harvest date, consistent with previous studies. For example, elevated CO2 was shown to increase dry weight by 10% to 30% for pansy ‘Delta Yellow Blotch’ and ‘Delta Primrose Blotch’ after 4 weeks at 1000 μmol⋅mol−1 (Niu et al. 2000). However, similar to LDM, the magnitude of difference between CO2 treatments for SDM began to diminish after 21 d, when plants started flowering, possibly indicating biomass being allocated to the new sink potential (Lewis et al. 2002; Niu et al. 2000).

An increase in biomass with no significant increase in LA, leaf number, or stem length insinuates the accumulation of sugars, for example, hexose carbohydrates and starch (Arp 1991; Giri et al. 2016; Gunderson and Wullschleger 1994). This is reflected in LMA differences for both species, because long-term exposure to elevated CO2 consistently results in increased LMA (Ainsworth and Long 2004; Arp 1991; Drake et al. 1997; Frantz and Ling 2011; Kirschbaum and Lambie 2015). This significant increase in sugars possibly helps explain physiological changes and responses of photosynthesis to an elevated CO2 concentration because of feedback inhibition to the photosynthetic mechanism (Cave et al. 1981; Drake et al. 1997; Makino and Mae 1999; Wulff and Strain 1982).

Few differences in RCC from the CO2 treatment were observed for both species. Chlorophyll responses to elevated CO2 are species-specific, with the possibility of a slight increase in the short-term but no change in the long-term (Ainsworth and Long 2004; Giri et al. 2016; Gunderson and Wullschleger 1994). Shifts in the ratio of chlorophyll-α and chlorophyll-β are common in response to elevated CO2 concentrations, but they usually do not result in a change in the total chlorophyll content (Arp 1991). This may be attributed to a mutual shading response caused by thicker leaves from increased LMA or additional palisade layers (Arp 1991). Similarly, starch accumulation caused by long-term elevated CO2 exposure can inhibit the function of chlorophyll in the leaves, causing a reduction in the photosynthetic rate and processes as a symptom of acclimation (Cave et al. 1981; Makino and Mae 1999; Wulff and Strain 1982).

There were no observable differences in either petunia or pansy for time to flower or number of flowers on the harvest date. This is consistent with previous studies that evaluated petunia ‘Madness White’, which showed no difference in timing for the appearance of the first flower between 400 and 800 μmol⋅mol−1 CO2 (Frantz and Ling 2011). Similarly, an elevated CO2 concentration (1000 μmol⋅mol−1) did not influence time to flower or development of pansy ‘Delta Yellow Blotch’ or ‘Delta Primrose Blotch’ (Niu et al. 2000). The widely observed response of no change to flowering may be attributable to a reduced photosynthetic capacity caused by acclimation to elevated CO2, possibly showing little benefit to using long-term exposure for improved plant quality or hastened production. Specifically, although flowers may present the opportunity for new carbon sinks, the dry masses of individual flowers have been shown to increase in response to elevated CO2 rather than development or number (Frantz and Ling 2011; Niu et al. 2000; Prior et al. 2011). More studies are needed to specifically observe flower timing in response to elevated CO2 because there is little evidence of CO2 causing flower induction alone. Previous studies observed that earlier flower induction is often a response to an interaction between lighting treatment and elevated CO2 (Frantz and Ling 2011; Mortensen and Moe 1992; Niu et al. 2000; Prior et al. 2011). For example, Niu et al. (2000) found that changes in the daily light integral possibly interacted with elevated CO2 to alter flower development of pansy ‘Delta Yellow Blotch’ and ‘Delta Primrose Blotch’; however, no difference in the flowering rate was observed when comparing solely 400 and 600 μmol⋅mol−1 CO2.

Gas exchange data.

In the present study, both species displayed higher Vcmax and Jmax for plants grown under ambient conditions compared with elevated conditions on all measurement days. Changes in Jmax tended to mirror those associated with changes in Vcmax, which is consistent with other species (Gunderson and Wullschleger 1994). For example, a survey of free-air CO2 enrichment studies across 109 species found that Vcmax was reduced, on average, by 13%, and Jmax was reduced, on average, by 5% in response to enriched CO2 concentrations, indicating a decrease in the efficacy of Rubisco dehydrogenase, with changes in Jmax tending to mirror those in Vcmax (Ainsworth and Long 2004, 2021; Bunce 1994; Drake et al. 1997; Kirschbaum 2011). In another study, Eucalyptus camaldulensis showed a 39% decrease in Jmax and 34% decrease in Vcmax compared with those under ambient conditions after 10 weeks of exposure at 800 μmol⋅mol−1 CO2 (Dillon et al. 2018). A decrease in the Rubisco dehydrogenase content or activity has been proposed to coincide with reductions in Vcmax (Bunce 1994; Drake et al. 1997; Wullschleger et al. 1994). Similarly, TPU was greater for both species under ambient conditions across all measurement dates. This is consistent with prior studies because decreased TPU is a common physiological response to elevated CO2 concentrations and is associated with accumulated hexose sugars and starch, as also indicated by the increase in LMA (Dahal and Vanlerberghe 2018; Lombardozzi et al. 2018; Yang et al. 2016). For example, Eucalyptus camaldulensis displayed a decrease in TPU of 38% in response to 10 weeks at 800 μmol⋅mol−1 compared with ambient conditions (Dillon et al. 2018). Similarly, tobacco (Nicotiana tabacum) was found to reduce TPU after 18 d of exposure to 1000 μmol⋅mol−1 CO2 (Dahal and Vanlerberghe 2018). Both pansy and petunia showed a decrease in Vcmax, Jmax, and TPU in response to elevated CO2 concentrations. This indicated photosynthetic acclimation as early as 7 d from initial exposure for petunia and 14 d for pansy. This difference in time for photosynthetic processes to acclimate may also emphasize the contention of species-specific responses. The difference in these rates mirror the results seen for growth measurements as possible feedback inhibition and damage to the photosynthetic apparatus can occur because of the accumulated carbohydrates indicated by the increased biomass and LMA.

Both species in the present study displayed decreased Gs measured at the operating point in response to production under elevated conditions for all measurement days. Stomatal conductance has been commonly shown to decrease in response to elevated CO2 (Arp 1991). For example, Gs was found to decrease in multiple species after elevation of CO2 across many field and chamber studies (Anderson et al. 2001). After 3 weeks at an elevated CO2 concentration, the Gs of kale (Brassica oleracea), spinach (Spinacea oleracea), and lettuce were reduced by nearly 60%, 65%, and 65%, respectively, compared with the ambient concentration (Erwin and Gesick 2017; Giri et al. 2016). Stomatal conductance is mediated by changes in photosynthesis; therefore, the reduced photosynthetic capacity coinciding with the lower Gs is expected (Drake et al. 1997). A reduced Gs could be a function of the reduced stomatal aperture affecting the ability of CO2 to enter the stomata or diffuse into the leaf, further limiting the photosynthesis rate (Drake et al. 1997; Gislerod and Nelson 1989; Gunderson and Wullschleger 1994).

The net photosynthetic rates measured at the 400 and 1000 μmol⋅mol−1 CO2 concentrations were higher for plants grown under ambient conditions than for those grown under elevated conditions for both species at all measurement days. Long exposure to elevated CO2 by a broad range of natural species has shown downregulation of net photosynthesis from survey measurements (Dillon et al. 2018). For example, Eucalyptus camaldulensis showed an 11% reduction in net photosynthetic rate for plants grown at 800 μmol⋅mol−1 CO2 for 10 weeks compared with plants grown under ambient concentration measured at the same concentration (Dillon et al. 2018). The same trend was detected when assessing the overall net photosynthesis observed from A-Ci curves (Dillon et al. 2018). This coincided with an overall decrease in biochemical processes of photosynthesis, such as Vcmax, Jmax, and TPU. Acclimation to elevated CO2 in many species is often measured between 1 and 6 d, with longer exposure showing a steady decrease in the net photosynthetic rate (Drake et al. 1997; Gunderson and Wullschleger 1994; Kirschbaum and Lambie 2015; Mortensen 1987). This is consistent with the observations of the present study. Petunia and pansy showed photosynthetic acclimation within as few as 7 d. Furthermore, once plants showed acclimation in photosynthetic processes, plants remained in this physiological state for the duration of the study, as differences in the net photosynthetic rate were observed between ambient and elevated CO2 concentrations at all days for both species. From a production standpoint, the immediate photosynthetic increase is often at least 40% compared with that under ambient conditions, with the potential for exponential growth based on early photosynthetic model predictions (Drake et al. 1997; Prior et al. 2011). However, the present study observed a nearly 40% decrease in the net photosynthetic capacity after 7 d for plants grown at 1000 μmol⋅mol−1 CO2 compared with those grown under ambient conditions. This emphasizes the discrepancy between the predicted benefits of elevated CO2 compared with the realized responses throughout production. Moreover, an increase in LMA for plants grown at elevated conditions did not lead to an expected increase in the net photosynthetic rate based on the leaf-level gas exchange, further demonstrating acclimation to elevated CO2 (Poorter et al. 2009). However, there is evidence that plants grown under elevated CO2 in the present study were still operating at an increased photosynthetic rate compared with those grown under ambient CO2 despite acclimation, resulting in moderate increases in LDM and SDM compared with those grown under ambient CO2. Thus, the utilization of long-term elevated CO2 for controlled environment production is understandable because of the marginal benefit to biomass accumulation. However, it is possible that extending the present study an additional 28 d likely would have shown even fewer differences between treatments based on the incremental decline in biomass observed during previous studies (Frantz and Ling 2011). As anticipated based on extensive previous research, the plants in this study acclimated both morphologically and physiologically to long-term exposure to elevated CO2 concentrations; however, this study showed that plants displayed symptoms of acclimation to elevated CO2 concentrations within 7 d of exposure, minimizing the potential benefits to plant production. Speculatively, short-term exposure to elevated CO2 at the end of production could provide a more drastic positive response because of a greater canopy size existing before acclimation. However, further research is needed to evaluate whether capitalizing on the potential increase in photosynthesis before acclimation is attainable and meaningful to enhance production.

Conclusions

Although responses of horticulture species to long-term elevated CO2 concentrations continue to be studied, further research is needed to identify the timing and extent of these species-specific responses to better understand CO2 as an input for controlled environment production. For the horticulture industry, although an increase in biomass was observed for both petunia ‘Dreams Midnight’ and pansy ‘Matrix Blue Blotch Improved’ under an elevated CO2 concentration compared with ambient conditions at all days, physiological acclimation to this input within 7 d of production likely limited the potential of this increase in biomass. Specifically, there was a significant reduction in the photosynthetic rate and processes, translating into quick photosynthetic acclimation for both species. However, the results are constrained to the environmental conditions and container limitations used for this study, with the potential for sink limitations and interactions with other production inputs (e.g., temperature, nutrition) warranting further research to elucidate responses to elevated CO2 concentrations for a diverse array of horticulture species (Ainsworth and Long 2021). With this information, improved strategies for CO2 enrichment that bypass acclimation limitations may be developed, which could increase production efficiency for controlled environments.

References Cited

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  • Fig. 1.

    Net photosynthetic rate measured at 400 and 1000 μmol⋅mol−1 CO2 for petunia (Petunia ×hybrida ‘Dreams Midnight’) and pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated). Gas exchange measurements were obtained using a portable photosynthesis meter (LI-6400XT; LI-COR Inc., Lincoln, NE, USA) at 7 (A and B), 14 (C and D), 21 (E and F), and 28 (G and H) d after experiment initiation with cuvette conditions matching the production environment; specifically, leaf temperature, relative humidity, and photosynthetic photon flux density (PPFD) were 21 °C, 55%, and 250 μmol⋅m−2⋅s−1, respectively. A significant difference between CO2 treatments was observed at both CO2 concentrations on all data collection days for both species according to Tukey’s honest significant difference (HSD) test at P ≤ 0.05. No trends over time or between measurements collected at the two CO2 concentrations were tested.

  • Ainsworth EA, Long SP. 2004. What have we learned from 15 years of free-air CO2, enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy, properties and plant production to rising CO2 . New Phytol. 165:351372. https://doi.org/10.1111/j.1469-8137.2004.01224.x.

    • Search Google Scholar
    • Export Citation
  • Ainsworth EA, Long SP. 2021. 30 years of free-air carbon dioxide enrichment (FACE): What have we learned about future crop productivity and its potential for adaptation? Glob Change Biol. 27:2749. https://doi.org/10.1111/gcb.15375.

    • Search Google Scholar
    • Export Citation
  • Anderson LJ, Maherali H, Johnson HB, Polley HW, Jackson RB. 2001. Gas, exchange and photosynthetic acclimation over subambient to elevated CO2 in a C3-C4, grassland. Glob Change Biol. 7:693707. https://doi.org/10.1046/j.1354-1013.2001.00438.x.

    • Search Google Scholar
    • Export Citation
  • Arp WJ. 1991. Effects of source-sink relations on photosynthetic acclimation to elevated CO2 . Plant Cell Environ. 14:869875. https://doi.org/10.1111/j.1365-3040.1991.tb01450.x.

    • Search Google Scholar
    • Export Citation
  • Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models, using lme4. J Stat Softw. 67:148. https://doi.org/10.48550/arXiv.1406.5823.

    • Search Google Scholar
    • Export Citation
  • Both AJ, Frantz JM, Bugbee B. 2017. Carbon dioxide enrichment in controlled environments, p. 82–86. In: Lopez R, Runkle E (eds). Light management in controlled environments. Meister Media Worldwide, Willoughby, OH, USA.

  • Bunce JA. 1994. Responses of respiration to increasing atmospheric carbon dioxide concentrations. Physiol Plant. 90:427430. https://doi.org/10.1111/j.1399-3054.1994.tb00409.x.

    • Search Google Scholar
    • Export Citation
  • Calvert A, Slack G. 1976. Effect of carbon dioxide enrichment on growth, development and yield of glasshouse tomatoes. II. The duration of daily periods of enrichment. J Hortic Sci. 51:401409. https://doi.org/10.1080/00221589.1976.11514705.

    • Search Google Scholar
    • Export Citation
  • Cave G, Tolley LC, Strain BR. 1981. Effect of carbon dioxide enrichment on chlorophyll content, starch content and starch grain structure in Trifolium subterraneum leaves. Physiol Plant. 51:171174. https://doi.org/10.1111/j.1399-3054.1981.tb02694.x.

    • Search Google Scholar
    • Export Citation
  • Clough JM, Peet MM. 1981. Effects of intermittent exposure to high atmospheric CO2 on vegetative growth in soybean. Physiol Plant. 53:565569. https://doi.org/10.1111/j.1399-3054.1981.tb02752.x.

    • Search Google Scholar
    • Export Citation
  • Dahal K, Vanlerberghe GC. 2018. Growth at elevated CO2 requires acclimation of the respiratory chain to support photosynthesis. Plant Physiol. 178:82100. https://doi.org/10.1104/pp.18.00712.

    • Search Google Scholar
    • Export Citation
  • Drake BG, Gonzàlez-Meler MA, Long SP. 1997. More efficient plants: A consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol. 48:609639. https://doi.org/10.1146/annurev.arplant.48.1.609.

    • Search Google Scholar
    • Export Citation
  • Dillon S, Quentin A, Ivković M, Furbank RT, Pinkard E. 2018. Photosynthetic variation and responsiveness to CO2 in a widespread riparian tree. PLoS One. 13:e0189635. https://doi.org/10.1371/journal.pone.0189635.

    • Search Google Scholar
    • Export Citation
  • Duursma RA. 2015. Plantecophys – An R package for analysing and modelling leaf gas exchange data. PLoS One. 10:e0143346. https://doi.org/10.1371/journal.pone.0143346.

    • Search Google Scholar
    • Export Citation
  • Erwin J, Gesick E. 2017. Photosynthetic responses of swiss chard, kale, and spinach cultivars to irradiance and carbon dioxide concentration. HortScience. 52:706712. https://doi.org/10.21273/HORTSCI11799-17.

    • Search Google Scholar
    • Export Citation
  • Frantz JM, Ling P. 2011. Growth, partitioning, and nutrient and carbohydrate concentration of Petunia ×hybrida Vilm. are influenced by altering light, CO2, and fertility. HortScience. 46:228235. https://doi.org/10.21273/HORTSCI.46.2.228.

    • Search Google Scholar
    • Export Citation
  • Giri A, Armstrong B, Rajashekar CB. 2016. Elevated carbon dioxide level suppresses nutritional quality of lettuce and spinach. Am J Plant Sci. 7:246258. https://doi.org/10.4236/ajps.2016.71024.

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David W. McKinney Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Avenue, Fort Collins, CO 80521-1173, USA

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Joshua K. Craver Department of Horticulture and Landscape Architecture, Colorado State University, 301 University Avenue, Fort Collins, CO 80521-1173, USA

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Contributor Notes

We gratefully acknowledge Mike Hazelett for technical assistance, Ball Horticultural Co. for seed, and the US Department of Agriculture, National Institute of Food and Agriculture, Hatch project #1022681 for funding. The use of trade names in this publication does not imply endorsement by Colorado State University of products named nor criticism of similar ones not mentioned.

J.K.C. is the corresponding author. E-mail: Joshua.Craver@colostate.edu.

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  • Fig. 1.

    Net photosynthetic rate measured at 400 and 1000 μmol⋅mol−1 CO2 for petunia (Petunia ×hybrida ‘Dreams Midnight’) and pansy (Viola ×wittrockiana ‘Matrix Blue Blotch Improved’). Plants were grown in 11.4-cm containers (550 mL) using reach-in growth chambers with CO2 concentration set points of 400 μmol⋅mol−1 (ambient) and 1000 μmol⋅mol−1 (elevated). Gas exchange measurements were obtained using a portable photosynthesis meter (LI-6400XT; LI-COR Inc., Lincoln, NE, USA) at 7 (A and B), 14 (C and D), 21 (E and F), and 28 (G and H) d after experiment initiation with cuvette conditions matching the production environment; specifically, leaf temperature, relative humidity, and photosynthetic photon flux density (PPFD) were 21 °C, 55%, and 250 μmol⋅m−2⋅s−1, respectively. A significant difference between CO2 treatments was observed at both CO2 concentrations on all data collection days for both species according to Tukey’s honest significant difference (HSD) test at P ≤ 0.05. No trends over time or between measurements collected at the two CO2 concentrations were tested.

 

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