Photosynthetic Acclimation, Biomass Allocation, and Water Use Efficiency of Garlic in Response to Carbon Dioxide Enrichment and Nitrogen Fertilization

in Journal of the American Society for Horticultural Science
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Lloyd L. NackleyDepartment of Plant Sciences, University of California, Davis, CA 95616

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Jig Han JeongSchool of Environmental and Forest Sciences, University of Washington, Seattle, WA 98195

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Lorence R. OkiDepartment of Plant Sciences, University of California, Davis, CA 95616

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Soo-Hyung KimSchool of Environmental and Forest Sciences, University of Washington, Seattle, WA 98195

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Garlic (Allium sativum) is a commercially and culturally important crop worldwide. Despite the importance of garlic, there have been few studies investigating how garlic growth and development will be affected by the atmospheric enrichment of carbon dioxide (CO2). A split-plot experiment with CO2 concentrations as main plot and nitrogen (N) fertilization as subplot was carried out to examine the effects of elevated CO2 at (mean ± sd) 745 ± 63 µmol·mol−1 across three levels of N: high-N (16.0 mm), mid-N (4.0 mm), and low-N (1.0 mm). Three hypotheses were tested: 1) garlic plants will allocate proportionally more biomass to bulb when grown in elevated CO2 compared with the plants grown in ambient CO2; 2) plants will sustain improved photosynthesis without downregulation in elevated CO2, irrespective of N; and 3) elevated CO2 will improve plant water use efficiency (WUE) across N fertilization levels. We found that proportional biomass allocation to bulb was not significantly enhanced by CO2 enrichment in garlic. Overall biomass accumulation represented by leaf, stem, and bulb did not respond significantly to CO2 enrichment but responded strongly to N treatments (P < 0.001). Contrary to our hypothesis, photosynthetic downregulation was apparent for garlic plants grown in elevated CO2 with a decrease in Rubisco capacity (P < 0.01). Instantaneous leaf WUE improved in response to elevated CO2 (P < 0.001) and also with increasing N fertilization (P < 0.001). Finally, our results indicate that bulbing ratio is likely to remain unchanged with CO2 or N levels and may continue to serve as a useful nondesctructive metric to estimate harvest timing and bulb size.

Abstract

Garlic (Allium sativum) is a commercially and culturally important crop worldwide. Despite the importance of garlic, there have been few studies investigating how garlic growth and development will be affected by the atmospheric enrichment of carbon dioxide (CO2). A split-plot experiment with CO2 concentrations as main plot and nitrogen (N) fertilization as subplot was carried out to examine the effects of elevated CO2 at (mean ± sd) 745 ± 63 µmol·mol−1 across three levels of N: high-N (16.0 mm), mid-N (4.0 mm), and low-N (1.0 mm). Three hypotheses were tested: 1) garlic plants will allocate proportionally more biomass to bulb when grown in elevated CO2 compared with the plants grown in ambient CO2; 2) plants will sustain improved photosynthesis without downregulation in elevated CO2, irrespective of N; and 3) elevated CO2 will improve plant water use efficiency (WUE) across N fertilization levels. We found that proportional biomass allocation to bulb was not significantly enhanced by CO2 enrichment in garlic. Overall biomass accumulation represented by leaf, stem, and bulb did not respond significantly to CO2 enrichment but responded strongly to N treatments (P < 0.001). Contrary to our hypothesis, photosynthetic downregulation was apparent for garlic plants grown in elevated CO2 with a decrease in Rubisco capacity (P < 0.01). Instantaneous leaf WUE improved in response to elevated CO2 (P < 0.001) and also with increasing N fertilization (P < 0.001). Finally, our results indicate that bulbing ratio is likely to remain unchanged with CO2 or N levels and may continue to serve as a useful nondesctructive metric to estimate harvest timing and bulb size.

Garlic is an important food crop (Food and Agriculture Organization of the United Nations, 2011) that has been incorporated into cuisines around the world. In addition to its culinary contributions, for millennia garlic has been used medicinally as a remedy for a wide variety of medical conditions (Kik et al., 2001; Rivlin, 2006; Tattelman, 2005). Multiple books and reports have been written detailing optimal garlic horticulture (Andrews, 1998; Meredith, 2008) in regard to N fertilization (Bertoni et al., 1992; Buwalda, 1986) and water inputs (Villalobos et al., 2004). For example, Buwalda and Freeman (1987) reported that the N fertilization rate of 120 kg·ha−1 yielded highest harvestable bulb yield under a field condition. Despite the economic and cultural importance of garlic, there have been few studies investigating garlic growth and development in future environmental conditions predicted with global environmental change, in particular the atmospheric enrichment of CO2. One of the most consistent responses to CO2 enrichment has been an increase in biomass and total nonstructural carbohydrates in plant tissues (Körner, 2000). As we prepare to adapt crop management to predicted elevated CO2 concentrations (Ziska et al., 2012), it is particularly important to understand how CO2 enrichment will affect carbon allocation to the belowground storage structures for garlic, and other valued crops that form bulbs, corms, or rhizomes.

Extensive research has demonstrated that atmospheric enrichment of CO2 will stimulate photosynthetic responses for C3 plant growth. However, the substantial increases in net photosynthesis immediately after doubling CO2 are typically unsustainable as a consequence of decreased photosynthetic capacity (Leakey et al., 2009; Sage, 1994; Sage et al., 1989). This unsustained stimulation of photosynthesis is thought to be an acclimation response to high CO2 environment as a result of decreased Rubisco activity (Faria et al., 1996; Vu et al., 2008) and is often accompanied with an accumulation of nonstructural carbohydrates and the dilution of N illustrated by a higher C/N ratio (Stitt, 1991; Stitt and Krapp, 1999). This feedback inhibition, known as the “carbon sink limitation hypothesis,” ascribes the downregulation of photosynthesis to carbohydrate buildup, which is due to an imbalance between carbohydrate quantity and plant sinks mediated by N nutrition (Pollock and Farrar, 1996). Carbon assimilated during photosynthesis is competitively partitioned to active sinks, and the stimulating effects of CO2 enrichment on photosynthesis will be negated unless a plant has sufficient sinks with which to store the additional carbohydrates (Paul and Foyer, 2001). Carbon sink limitations may not be marked in plants with large carbon sinks such as bulbs and rhizomes (Kinmonth-Schultz and Kim, 2011), or in trees and other perennial species for which long-term storage of carbon is important for their fitness. In optimal conditions, belowground carbohydrate storage structures have been attributed to sustained photosynthetic capacity throughout the plant life cycle (Monje and Bugbee, 1998). However, row crops, like garlic, grow in a dynamic environment with naturally or induced (e.g., targeted drought) suboptimal conditions.

In suboptimal conditions, there is uncertainty whether assimilated carbon will be allocated to storage, reproduction, or defenses (Bazzaz, 1996). Plants allocate biomass to belowground parts for the acquisition of water and nutrients, and to aboveground parts for the acquisition of light and CO2. It has been reported that when plants are grown in elevated CO2, there is a reduction in the relative investment in leaf areas with a concomitant increase in the partitioning of carbon to belowground carbon sinks (Körner, 2000). Rogers et al. (1994) suggested that increasing levels of CO2 in the earth’s atmosphere will positively affect root dry weight, length, diameter, width, and root:shoot ratio. To date, many studies focus on roots as the representative belowground structure (Pendall et al., 2004; Rogers et al., 1992; Volder et al., 2007; Xu et al., 2007) with limited studies examining bulbs, corms, or rhizomes. However, the current practices of categorizing plant tissues by location (i.e., belowground structures) may be misleading because these structures are morphologically and anatomically distinct, which may result in diverse physiological responses. For instance, fleshy leaf scales are the primary storage tissues for garlic, whereas the root cortex is the primary storage organ for carrot (Daucus carota). Questions remain whether plants will prioritize growth or development of long-term reserves when atmospheric CO2 supplies are abundant, but other resources such as nutrients or water may be limiting.

Little is known about the link between anatomical and morphological aspects of storage structures and biomass partitioning at the whole plant level under elevated atmospheric CO2 concentrations (Ziska and Bunce, 2006), and how carbon assimilation and allocation responses in high CO2 are related to N availability in bulb-producing plants. The objectives of this study were to determine photosynthetic responses, patterns of biomass allocation to bulbs, and WUEs of garlic plants grown in elevated CO2 across a range of N levels. Specifically, our hypotheses consisted of the following: 1) garlic plants will allocate proportionally more biomass to bulb, a storage structure consisting of modified leaves, when grown in elevated CO2 compared with the plants grown in ambient CO2; 2) garlic plants will sustain improved photosynthesis with little downregulation in elevated CO2 irrespective of N supply due to increased sink strength represented by large bulb size; and 3) elevated CO2 will improve plant WUE across N fertilization levels.

Materials and Methods

Plant materials and facilities.

An Asiatic hardneck garlic (cv. Korean Mountain) purchased from Filaree Garlic Farm (Okanogan, WA) was used for this study. On 13 Jan. 2011, 60 pots (2.54-L tree pots) were filled with unfertilized, sterilized, potting mix (Sunshine Potting Mix #2; Sun Gro Horticulture, Vancouver, BC, Canada), and planted with one clove per pot. The pots were then placed on wire tables in a glasshouse located in Seattle, WA, and watered from a hose by hand. Daylight was supplemented in the glasshouse with high-pressure sodium 400-W single-phase bulbs during 0800 to 2200 hr. The glasshouse uses natural ventilation, exhaust fans, and evaporative cooling pads to prevent excessive temperatures. After 14 d, all cloves had germinated and the pots were organized into experimental treatment groups.

Experimental design.

Three N levels and two CO2 levels were used as the experimental treatments. First, the 60 pots were randomly split into three N groups of 20 pots each. The treatments were three levels of N delivered as ammonium nitrate delivered as part of a modified Hoagland’s liquid fertilizer solution: full strength [high-N (16.0 mm N, 0.224 g·L−1)], 1/4 strength [mid-N (4.0 mm N, 0.056 g·L−1)], and 1/16 strength [low-N (1.0 mm N, 0.014 g·L−1)]. The macronutrients were provided as follows: (NH4)(NO3), CaCl2·2H2O, K2SO4, and KH2PO4 (concentrations for K, Ca, P, Mg, S, and Cl were 6.0, 3.0, 2.0, 3.0, 1.0, and 6.0 mm, respectively). The micronutrients were in the forms of H3BO3, MnSO4·H2O, ZnSO4·7H2O, CuSO4·5H2O, H2MoO4, and NaFeDTPA (concentrations of B, Mn, Zn, Cu, Mo, and Fe chelate were 25, 2.0, 2.0, 0.5, 0.5, and 18 μm, respectively). Only N levels differed; all other elements were maintained at equal levels between treatments. The treatments were applied when the plants were watered by hand at least once per week for the duration of the experiment. Next, the pots were organized into CO2 treatment groups, “ambient” and “elevated.” Five pots from each N group were randomly placed in one of four CO2 controlled sunlit growth chambers that were located inside the glasshouse. The growth chambers (100 × 100 × 200 cm) were closed-topped, polyvinyl chloride-framed units, surrounded with Mylar polyester sheeting (DuPont Teijin Films, Chester, VA). For additional details of the chamber see Kinmonth-Schultz and Kim (2011). In each chamber, temperature/light sensors (HOBO Pendant Temperature/Light senor; Onset Computer, Bourne, MA) recorded temperature and illuminance (kilolux) every 15 min for the experimental period January to June (Fig. 1). After the experiment concluded, a quantum sensor (LI-190; LI-COR, Lincoln, NE) was installed inside the chambers to measure greenhouse photosynthetic photon flux [PPF (μmol·m−2·s−1)]. The PPF data from the subsequent 2 years (i.e., 2012 and 2013) are also provided herein to illustrate the expected characteristics of the chamber light environment during the 2011 experiment (Fig. 1).

Fig. 1.
Fig. 1.

Diurnal patterns of light inside the sunlit growth chambers. (A) Illuminance data inside the growth chambers during the period of leaf gas-exchange measurements (i.e., May through June 2011). (B) Photosynthetic photon flux (PPF) inside the growth chambers collected during May and June, the 2 years (2012 and 2013) following the experiment (2011). Dashed lines represent regression curves fitted to the maximum hourly values for both data sets. (C) Daily PPF integrals from January through June periods in 2012 and 2013 (open circle); these data are shown as a proxy to represent the PPF patterns at the site during the experimental period in 2011. Also shown are monthly temperature averages with sd error bars (closed circle) inside the growth chambers.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 141, 4; 10.21273/JASHS.141.4.373

Fans forced air through ventilation ducts from outside the greenhouse into the chambers. Two of the chambers were assigned “ambient” air and received air directly through the pipes from outside. The remaining two were designated as “elevated” and were supplemented with additional CO2 that was added to the ventilation ducts through flexible plastic tubing delivered from a 22.70-kg tank (Praxair, Seattle, WA). The elevated CO2 concentrations were maintained by using bubble flow meters (FL-2000; Omega, Stamford, CT). CO2 concentrations were automatically measured, every 15 min, by sampling air from within the chambers through an infrared gas analyzer (IRGA) (CIRAS-1; PP Systems International, Amesbury, MA). The CIRAS-1 IRGA has two channels to detect CO2 concentrations, reference (ref.) and differential (diff.). We were able to continuously monitor both of the “elevated” CO2 chambers by connecting a flexible plastic tubing from the two chambers to the ref. and diff. ports. Once a week, for the duration of the experiment, the CIRAS-1 was taken to an adjacent laboratory and was calibrated against two gas cylinders of certified CO2 concentrations (0 and 700 µmol·mol−1). The “ambient” CO2 was measured, every 15 min, with a sensor (Carbocap GMP242; Vaisala, Vantaa, Finland) placed in one of the “ambient” chambers. The daily mean value with sd for the “elevated” treatment was (mean ± sd) 745 ± 63 µmol·mol−1 of CO2. The mean “ambient” chamber concentration was recorded at 437 µmol·mol−1 of CO2. CO2 and temperature data were stored automatically in a data-logger (CR1000; Campbell Scientific, Logan, UT). To summarize, there were 10 pots from each N treatment in each of the two CO2 treatments.

Leaf gas exchange measurements.

A portable photosynthesis system with a leaf chamber fluorometer (LI-6400-40, LI-COR) was used to measure the net CO2 assimilation rates [A (μmol·m−2·s−1)], and transpiration [E (mmol·m−2·s−1)], as well as the differences between atmospheric (Ca) and internal (Ci) CO2 concentrations. Gas exchange data were collected on fully expanded young leaves from six to eight randomly selected plants per treatment group (CO2 × N). All gas exchange measurements were allowed 5–7 min to stabilize, light intensity (PPF) was set at 1500 µmol·m−2·s−1, the flow rate was set to 300 µmol·m−2·s−1, and the chamber block temperatures were set to 15 or 25 °C, reflective of the mean daily temperature range (Fig. 1). Gas exchange measurements were recorded at these settings across a range of Ca levels from 50 to 1500 μmol·mol−1 CO2. These gas exchange measurements were collected from 1 May 2011, through 12 June 2011, between 0800 and 1400 hr. These CO2 responses (i.e., ACi) data were used to determine the presence and extent of photosynthetic acclimation to elevated CO2 (Sage, 1994). Briefly, Rubisco capacity (Vcmax), maximum rate of electron transport (Jmax), and Aelev/Aambi (the ratio of A of elevated [CO2] grown leaves over A of ambient [CO2] grown leaves) at multiple Ci values were estimated to test for photosynthetic downregulation under elevated CO2 conditions (for detailed methods see Kim and Lieth, 2003; Kinmonth-Schultz and Kim, 2011; Sharkey et al., 2007). In addition, A and WUE were compared for all CO2·N treatments. WUE was evaluated with the IRGA by comparing instantaneous WUE (A/E), as well as the Ci/Ca ratio. The Ci/Ca ratio reflects the balance between net assimilation and stomatal conductance (gS); whereas A/E reflects the amount of carbon gained per water lost. In addition, carbon isotopes (13C, 12C) compositions were analyzed from leaf samples to indicate long-term internal regulation of carbon uptake and water loss.

The carbon isotope discrimination (δ 13C) was evaluated from five randomly selected plants from each treatment group. Leaves of these plants were milled through 1-mm mesh screen using a Wiley mini-mill (Thomas Scientific, Swedesboro, NJ). The pulverized leaf samples were then processed at the University of California at Davis stable isotope laboratory with an elemental analyzer (PDZ Europa ANCA-GSL elemental analyzer; Sercon, Irvine, UK) interfaced to a continuous flow isotope ratio mass spectrometer (PDZ Europa 20–20 isotope ratio mass spectrometer, Sercon). Farquhar and Richards (1984) proposed the use of Δ as a measure of the carbon isotope discrimination by the plant as shown below:
UNDE1

The CO2 tanks were filled with gas that was captured during fossil fuel refining, which had been measured (Nackley et al., 2014) as having a different isotopic signature (δ13C, −35.5‰) compared with atmospheric CO213C, −8‰). As previously stated, the supplemental gas was used to elevate the CO2 concentration from ambient levels (≈390 μmol·mol−1) to 745 μmol·mol−1. Therefore, the air within the elevated chambers was composed of 52% of the −8‰ δ13C air and 48% of the −35.5‰ δ13C gas from the tanks creating an atmosphere with an isotopic composition of −21.2‰ δ13C chamber. Although the ambient CO2 outside of the greenhouse was measured at ≈390 μmol·mol−1, the average CO2 concentration recorded within the ambient chambers was 437 ± 1 μmol·mol−1. Therefore, the isotopic composition of the ambient chambers was −11.025‰ δ13C.

Biomass growth and allocation.

The N and CO2 treatments were applied to the garlic plants for 152 d. The experiment concluded on 14 June 2011, at which point all of the plants were harvested. The harvest involved separating the plants into leaves, stem, bulb, and roots; stem part included pseudostem (i.e., sheath) and scape when present. Because of incomplete separation of roots from media in multiple samples, root biomass was not included in the final analysis. The harvested plant parts were bagged in paper and dried for 48 h in a forced air oven heated to 80 °C. The oven-dry biomass was weighed and analyzed to compare the effects of CO2 and N on biomass development and allocation.

Leaf N concentrations and C/N ratio.

When the plants were harvested on 14 June 2011, 36 leaf samples were randomly selected for determining leaf C and N concentrations (w/w). These leaves were clipped, bagged, and placed in a forced air oven at 80 °C for 48 h. The dried leaf samples were then ground with a Wiley mini-mill to fit through a 1-mm mesh. The ground leaf samples were transferred into consumable aluminum capsules and combusted in a pure oxygen environment with a CHN analyzer (model-2400; PerkinElmer, Waltham, MA) to determine C and N contents in the leaves.

Data analysis.

The experiment constituted a split-plot design with CO2 being the main plot and N being the subplot. Accordingly, CO2 and N were considered fixed effects and the chambers (blocks) were treated as random effects. Initially, a linear mixed-effects model was used to determine whether significant variability could be attributed to the chambers. When the chamber effects were not found to be significant (P > 0.05), they were removed from further linear models that tested the main effects. Succeeding analyses included two-way analyses of variance, using type III sums of squares, to quantify the main effects and interactions from CO2 and N for biomass responses, leaf gas exchange, and leaf tissue composition. For leaf gas exchange data analysis, we used the temperature (i.e., 15 or 25 °C) as a blocking variable to account for the variability due to different measurement temperatures although no significant differences were found between the two measurement temperatures in all gas exchange parameters with an exception of the rate of transpiration (E), similar to the findings in a previous study (Kim et al., 2013). All statistical analyses were calculated using SAS (version 9.4; SAS Institute, Cary, NC) or R 3.2.1 statistical software (R Development Core Team 2011). SigmaPlot 12.5 (Systat software, San Jose, CA) was used to plot the figures.

Results

Biomass allocation and leaf N status.

Nitrogen treatments resulted in significant differences in leaf, bulb, and leaf-stem-bulb (LSB) biomass [P < 0.05 (Fig. 2)], whereas elevated CO2 produced marginally greater stem biomass (P = 0.08). With little response of bulb biomass to elevated CO2, none of the biomass ratios involving bulb (i.e., bulb/leaf, bulb/stem, bulb/LSB) were significant (Figs. 3 and 4); this result suggests that garlic plants did not allocate preferentially more biomass to the bulb when grown in elevated CO2. Similarly, the bulb biomass ratio to LSB or other plant parts did not change in response to N levels (Figs. 3 and 4). On the other hand, bulb diameter increased with N level (P < 0.001) but bulbing ratio (bulb diameter/stem diameter) did not change in response to CO2 or N (Fig. 3). Biomass allocation to leaf increased with N treatment levels [P < 0.05 (Fig. 2)].

Fig. 2.
Fig. 2.

Biomass by constituent part of garlic plants grown in response to ambient and elevated carbon dioxide at three nitrogen (N) levels: low-, mid-, and high-N (n = 9–10, mean ± se). (A) Leaf, (B) stem, (C) bulb, and (D) the sum of leaf, stem, and bulb parts.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 141, 4; 10.21273/JASHS.141.4.373

Fig. 3.
Fig. 3.

Biomass ratios in relation to the sum of leaf, stem, and bulb parts (LSB) and bulb characteristics of garlic plants grown in response to ambient and elevated carbon dioxide and nitrogen (N) treatments: low-, mid-, and high-N (n = 9–10, mean ± se). (A) Bulb/leaf-stem-bulb (LSB) biomass ratio, (B) leaf/LSB biomass ratio, (C) bulb diameter, and (D) bulbing ratio determined as bulb diameter divided by neck diameter.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 141, 4; 10.21273/JASHS.141.4.373

Fig. 4.
Fig. 4.

Leaf N concentration in garlic plants in response to ambient and elevated carbon dioxide at three nitrogen (N) levels: low-, mid-, and high-N. (A) In % (w/w) and (B) C/N ratio (n = 6; mean ± se).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 141, 4; 10.21273/JASHS.141.4.373

Leaf N concentration increased (P < 0.001) with N supply and decreased in response to CO2 enrichment [P < 0.05 (Fig. 4B)]. Reduction in leaf N under elevated CO2 was greater when N supply was the highest as evidenced by a significant interaction [P < 0.05 (Fig. 4A)]. Leaf C/N ratios decreased with increasing N supply (Fig. 4B) but did not change in response to elevated CO2 treatment.

CO2 assimilation and photosynthetic downregulation.

As expected for a C3 plant, the leaf net CO2 assimilation rate (A) increased with increasing CO2 concentrations (P < 0.05) and also with N levels [P < 0.05 (Table 1)]. When the LI-6400 leaf chamber was set to CO2 concentrations near the growth CO2 concentrations (i.e., 400 or 700 µmol·mol−1), A increased by 23% on average in plants grown in elevated CO2 compared with those from the ambient CO2 treatment (Table 1). Similarly, A increased 39% and 40% under mid- and high-N treatments, respectively, compared with low-N treatment (Table 1). This increase in A under elevated CO2 with increasing N levels is likely to have contributed to a marginal increase in biomass responses (Fig. 2).

Table 1.

Leaf gas-exchange parameters (n = 6–8) and 13C stable isotope ratios [Δ13C in ‰ (n = 5)] of garlic plants in response to carbon dioxide (CO2) and nitrogen (N) treatments. Leaf gas-exchange parameters include net CO2 assimilation rates (A), instantaneous leaf water use efficiency (WUE), Rubisco capacity (Vcmax), and potential electron transport rate (Jmax).

Table 1.

The Vcmax was significantly affected by both CO2 and N treatments (P < 0.01). CO2 enrichment significantly decreased Vcmax rates with the average ambient rates being ≈1/3 greater than the Rubisco capacity of the plants grown in elevated CO2 (Table 1). Nitrogen fertilization had a positive relationship with Vcmax. The low-N treatment had significantly lower rates than the mid- and high-N treatments at either CO2 treatment level (Table 1). The CO2 effect on Jmax was marginal (P = 0.08), whereas the N was found to play a significant role (P < 0.01). At either CO2, Jmax was found to be much lower for the low-N treatment compared with the mid- and high-N treatments (Table 1). The Aelev/Aambi ratios stayed below one in most cases indicating apparent photosynthetic downregulations especially at low intercellular CO2 concentrations in mid- and high-N. The values were more variable when N supply was low (Fig. 5). Together with a lower Vcmax, this result suggests that biochemical downregulation associated with carboxylation efficiency at low CO2 was highly likely present.

Fig. 5.
Fig. 5.

Photosynthetic acclimation to elevated carbon dioxide (CO2) in garlic plants at (A) low-nitrogen (N), (B) mid-N, and (C) high-N. The ratio of net CO2 assimilation rates (A) between elevated and ambient CO2 grown leaves (n = 6–8, mean ± se) are plotted over [CO2] at the intercellular air spaces (Ci). The ratios (Aelev/Aambi) below 1 are indicative of photosynthetic downregulation.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 141, 4; 10.21273/JASHS.141.4.373

Instantaneous and long-term WUE.

The leaf gas exchange indicated enhanced instantaneous WUE (A/E) in response to increasing CO2 [P < 0.001 (Table 1)]. The positive relationship between N fertilization and WUE (Table 1) is also evidenced by the significant difference in A/E (P < 0.001) between N treatments. In both cases, the improvements in WUE were more attributable to gains by A, which were significantly improved by N and CO2 enrichment, than by the limited differences in E, which did not respond significantly to either CO2 or N treatments (data not shown). The interaction between CO2 and N on WUE was significant (P < 0.05) indicating that instantaneous WUE increased more with N levels in elevated CO2 than in ambient CO2 conditions. Similar to the instantaneous WUE, the Δ13C results were also significantly related to the CO2 treatments (P < 0.001). Δ13C results did not indicate an effect from the N treatment or an interaction between CO2 and N.

Discussion

Garlic, like other C3 crops, exhibited beneficial responses to both CO2 and N enrichment. However, the results were not uniform for all plant parts and processes. Specifically, our results did not support our first hypothesis that garlic plants would allocate proportionally more biomass to bulb in response to CO2 enrichment. Although the results indicated that net CO2 assimilation rate (A) was enhanced by CO2 enrichment (Table 1) neither bulb nor leaf biomass responded significantly to elevated CO2. Overall, garlic plant biomass did not increase significantly in response to CO2 (P = 0.11) with the stem biomass being marginally responsive (P = 0.08) (Fig. 2). Studies that investigated the effects of CO2 enrichment on the growth and biomass of crop species with underground storage organs [e.g., potato (Solanum tuberosum), onion (Allium cepa), carrot, and radish (Raphanus sativus)] reported highly variable biomass accumulation and allocation responses (Jasoni et al., 2004; Mortensen, 1994; Schapendonk et al., 2000). For example, Mortensen (1994) reported that the yield of carrot and onion increased under elevated CO2, whereas leek (Allium ampeloprasum) yields were not significantly affected by the CO2 concentration. Further variation was reported by biomass grasses with rhizomes. Like garlic both reed canary grass (Phalaris arundinacea), and giant reed (Arundo donax) showed increased stem biomass and total biomass with elevated CO2 (Kinmonth-Schultz and Kim, 2011; L.L. Nackley, N. Hough-Snee, and S.-H. Kim, unpublished data). Yet, unlike garlic, giant reed had increased allocation to belowground storage organs (L.L. Nackley, N. Hough-Snee, and S.-H. Kim, unpublished data); reed canary grass did not (Kinmonth-Schultz and Kim, 2011).

The observed insignificant biomass response to CO2 enrichment could be an outcome of photosynthetic acclimation to elevated CO2 concentrations. The photosynthetic downregulation has been reported in experiments on other C3 plant species (Sage et al., 1989) including bulbous crops such as onion (Wheeler et al., 2004). In this study, we hypothesized that photosynthetic downregulation under elevated CO2 would be minimal in garlic because of the bulb serving as a strong carbon sink. We evaluated the different gas exchange measurements to discover any potential mechanisms responsible for the growth patterns. When the net CO2 assimilation rate (A) was compared with the respective chamber CO2 conditions (Table 1), after more than 5 months of CO2 enrichment the plants grown in the elevated CO2 chambers had consistently greater net assimilation rates across all N treatments (Table 1). However, decomposition of the A-Ci curves showed that elevated CO2 decreased carboxylation capacity (Vcmax) significantly (P < 0.01) whereas its effect was marginal on Jmax (P = 0.08). On the other hand, Jmax responded strongly to N levels (P < 0.01). These findings are consistent with other research on impacts of CO2 and N interactions in photosynthetic downregulations to elevated CO2 (Sims et al., 1998). The greater sensitivity of Vcmax implies that the amount, activation state, and kinetic properties of Rubisco were more responsive to CO2 enrichment compared with the rate of electron transport rate (i.e., Jmax), which did not respond strongly to CO2 enrichment. The Jmax is a measure linked to RuBP regeneration rate in the Calvin Cycle, which will depend on energetics, light availability, and photochemistry (Sharkey et al., 2007). These factors were less affected by CO2 enrichment, yet can be significantly affected by N as shown in our results on Jmax (Table 1). The decreased Jmax values in the low-N treatment were likely caused by limited availability of the N-dependent molecules in the light reactions of photosynthesis [e.g., chlorophyll, light harvesting complex, electron transport components, and coupling factor (Evans, 1989)]. Our results on Vcmax and Jmax suggest that elevated CO2 was likely to have reduced the Rubisco capacity in association with photosynthetic downregulation in garlic (Table 1); this was further corroborated by the reduced Aelev/Aambi ratios (Fig. 5). It has been pointed out that the biochemical signals of photosynthetic downregulation in response to CO2 enrichment may be influenced by pot-size limitations (Poorter et al., 2012; Sage, 1994). Our plants were not root bound at harvest suggesting that pot size was unlikely to limit belowground sink capacity in our experiment. As discussed by Wullschleger (1993), leaf responses do not always relate to whole plant responses; and it is important to recognize the photosynthesis model parameters (i.e., Vcmax and Jmax) describe the initial fixation of CO2 in the chloroplast by Rubisco, and that the subsequent translocation and allocation of this carbon for the growth of organs is a separate question.

Both leaf gas exchange and 13C stable isotope data supported the hypothesis that elevated CO2 improved WUE of garlic plants across N treatments (Table 1). The combination of short-term (gas exchange) and long-term (Δ13C) metrics provides us with insights about the mechanics of WUE. The results show that of the WUE parameters, A/E and Δ13C were significantly affected by the CO2 treatment, whereas E and gs alone were not (P > 0.05). For many other plants, improved WUE at elevated levels of CO2 has been attributed to partial stomatal closure (Field et al., 1995; Nackley et al., 2014) and subsequently reduced stomatal water loss. In our study, the instantaneous WUE (i.e., A/E) increased as a result of an increase in photosynthesis rather than a decrease in transpiration (Table 1). The measured conductance and transpiration rates remained unchanged in elevated CO2. Overtime, this increase in A/E is likely to have resulted in an increase in the long-term WUE represented by the decreased Δ13C (Table 1). Indication of short- and long-term improvements in WUE suggest that garlic plants will likely gain more carbon per unit water used in elevated CO2 irrespective of soil N fertility. The importance of gaining more carbon per unit water loss is especially relevant for garlic agriculture in arid and semiarid climates (i.e., California and other Mediterranean climate zones) where climate change has been predicted to increase summer temperatures and decrease fresh water supplies (Giorgi and Lionello, 2008) exacerbating growing season drought (Seager et al., 2013).

Despite the treatment effects on growth and N content, the bulbing ratio remained consistent (Fig. 3). This result is important considering that the bulbing ratio is a common allometric relationship used by garlic farmers as a nondestructive indicator of harvest time. Our results suggest that the bulbing ratio can continue to be a robust proxy across a range of soil fertility and in light of climate change, because the relationship was unaffected by either N or CO2 treatments (Fig. 3). Research shows that optimal garlic harvests are recommended when the foliage collapses and starts to senesce, and when the bulbing ratio is about four or five (Takagi, 1990). When these phenological stages occur, the garlic plants allocate photosynthates to storage carbohydrates including fructans and other metabolites in the bulb. Our values are slightly lower than the recommended bulbing ratio for harvest. This is likely because our final destructive harvest was conducted before the bulbs were completely mature to compare biomass of other plant parts in addition to bulbs.

In summary, our results did not support our first two hypotheses. That is, 1) garlic plants did not allocate proportionally more biomass to bulb when grown in elevated CO2 compared with the plants grown in ambient CO2, whereas other growth and physiological parameters such as stem biomass and A have been increased in elevated CO2 and 2) the Vcmax and Aelev/Aambi ratios decreased in response to elevated CO2 irrespective of N; this result is a strong indicator of photosynthetic downregulations in response to CO2, irrespective of N. Our third hypothesis was supported as elevated CO2 increased instantaneous WUE and reduced Δ13C across N levels. On the other hand, almost all growth and physiological parameters we tested responded strongly to N treatments. Our result also indicate that bulbing ratio is likely to remain unchanged with CO2 or N levels and may continue to serve as a useful metric to determine harvest timing in a changing climate.

Literature Cited

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  • Bertoni, G., Soubieille, P.C. & Llorens, J.M. 1992 Growth and nitrogen nutrition of garlic (Allium sativum L.) during bulb development Sci. Hort. 50 187 195

    • Search Google Scholar
    • Export Citation
  • Buwalda, J.G. 1986 Nitrogen nutrition of garlic (Allium sativum L.) under irrigation, crop growth and development Sci. Hort. 29 55 68

  • Buwalda, J.G. & Freeman, R.E. 1987 Effects of nitrogen fertilisers on growth and yield of potato (Solanum tuberosum L. ‘Ilam Hardy’), onion (Allium cepa L. ‘Pukekohe Longkeeper’), garlic (Allium sativum L. ‘Y strain’) and hybrid squash (Cucurbita maxima ‘L. Delica’) Sci. Hort. 32 161 173

    • Search Google Scholar
    • Export Citation
  • Evans, J.R. 1989 Photosynthesis and nitrogen relationships in leaves of C3 plants Oecologia 78 9 19

  • Faria, T., Wilkins, D., Besford, R.T., Vaz, M., Pereira, J.S. & Chaves, M.M. 1996 Growth at elevated CO2 leads to down-regulation of photosynthesis and altered response to high temperature in Quercus suber L. seedlings J. Expt. Bot. 47 1755 1761

    • Search Google Scholar
    • Export Citation
  • Farquhar, G.D. & Richards, R.A. 1984 Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes Funct. Plant Biol. 11 539 552

    • Search Google Scholar
    • Export Citation
  • Field, C.B., Jackson, R.B. & Mooney, H.A. 1995 Stomatal responses to increased CO2—Implications from the plant to the global-scale Plant Cell Environ. 18 1214 1225

    • Search Google Scholar
    • Export Citation
  • Food and Agriculture Organization of the United Nations 2011 The state of the world’s land and water resources for food and agriculture (SOLAW)—Managing systems at risk. Earthscan, Rome, Italy

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  • Jasoni, R., Kane, C., Green, C., Peffley, E., Tissue, D., Thompson, L., Payton, P. & Pare, P.W. 2004 Altered leaf and root emissions from onion (Allium cepa L.) grown under elevated CO2 conditions Environ. Expt. Bot. 51 273 280

    • Search Google Scholar
    • Export Citation
  • Kik, C., Kahane, R. & Gebhardt, R. 2001 Garlic and health Nutr. Metab. Cardiovasc. Dis. 11 57 65

  • Kim, S.-H., Jeong, J.H. & Nackley, L.L. 2013 Photosynthetic and transpiration responses to light, CO2, temperature, and leaf senescence in garlic: Analysis and modeling J. Amer. Soc. Hort. Sci. 138 149 156

    • Search Google Scholar
    • Export Citation
  • Kim, S.-H. & Lieth, J.H. 2003 A coupled model of photosynthesis, stomatal conductance and transpiration for a rose leaf (Rosa hybrida L.) Ann. Bot. (Lond.) 91 771 781

    • Search Google Scholar
    • Export Citation
  • Kinmonth-Schultz, H. & Kim, S.-H. 2011 Carbon gain, allocation and storage in rhizomes in response to elevated atmospheric carbon dioxide and nutrient supply in a perennial C3 grass, Phalaris arundinacea Funct. Plant Biol. 38 797 807

    • Search Google Scholar
    • Export Citation
  • Körner, C. 2000 Biosphere responses to CO2 enrichment Ecol. Appl. 10 1590 1619

  • Leakey, A.D.B., Ainsworth, E.A., Bernacchi, C.J., Rogers, A., Long, S.P. & Ort, D.R. 2009 Elevated CO2 effects on plant carbon, nitrogen, and water relations: Six important lessons from FACE J. Expt. Bot. 60 2859 2876

    • Search Google Scholar
    • Export Citation
  • Meredith, T.J. 2008 The complete book of garlic: A guide for gardeners, growers, and serious cooks. Timber Press, Portland, OR

  • Monje, O. & Bugbee, B. 1998 Adaptation to high CO2 concentration in an optimal environment: Radiation capture, canopy quantum yield and carbon use efficiency Plant Cell Environ. 21 315 324

    • Search Google Scholar
    • Export Citation
  • Mortensen, L.M. 1994 Effects of elevated CO2 concentrations on growth and yield of eight vegetable species in a cool climate Sci. Hort. 58 177 185

    • Search Google Scholar
    • Export Citation
  • Nackley, L.L., Vogt, K.A. & Kim, S.-H. 2014 Arundo donax water use and photosynthetic responses to drought and elevated CO2 Agr. Water Mgt. 136 13 22

  • Paul, M.J. & Foyer, C.H. 2001 Sink regulation of photosynthesis J. Expt. Bot. 52 1383 1400

  • Pendall, E., Bridgham, S., Hanson, P.J., Hungate, B., Kicklighter, D.W., Johnson, D.W., Law, B.E., Luo, Y., Megonigal, J.P., Olsrud, M., Ryan, M.G. & Wan, S. 2004 Below-ground process responses to elevated CO2 and temperature: A discussion of observations, measurement methods, and models New Phytol. 162 311 322

    • Search Google Scholar
    • Export Citation
  • Pollock, J. & Farrar, C. 1996 Source-sink relations: The role of sucrose, p. 262–276. In: N.R. Baker (ed.). Photosynthesis and the environment. Kluwer Academic Publishers, Dordrecht, the Netherlands/Boston, MA

  • Poorter, H., Bühler, J., Van Dusschoten, D., Climent, J. & Postma, J.A. 2012 Pot size matters : A meta-analysis of the effects of rooting volume on plant growth Funct. Plant Biol. 39 839 850

    • Search Google Scholar
    • Export Citation
  • Rivlin, R.S. 2006 Is garlic alternative medicine? J. Nutr. 136 713S 715S

  • Rogers, H.H., Peterson, C., McCrimmon, J. & Cure, J. 1992 Response of plant roots to elevated atmospheric carbon dioxide Plant Cell Environ. 15 749 752

  • Rogers, H.H., Runion, G.B. & Krupa, S.V. 1994 Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere Environ. Pollut. 83 155 189

    • Search Google Scholar
    • Export Citation
  • Sage, R.F. 1994 Acclimation of photosynthesis to increasing atmospheric CO2: The gas exchange perspective Photosyn. Res. 39 351 368

  • Sage, R.F., Sharkey, T.D. & Seemann, J.R. 1989 Acclimation of photosynthesis to elevated CO2 in five C3 species Plant Physiol. 89 590 596

  • Schapendonk, A., van Oijen, M., Dijkstra, P., Pot, C., Jordi, W. & Stoopen, G. 2000 Effects of elevated CO2 concentration on photosynthetic acclimation and productivity of two potato cultivars grown in open-top chambers Funct. Plant Biol. 27 1119 1130

    • Search Google Scholar
    • Export Citation
  • Seager, R., Ting, M., Li, C., Naik, N., Cook, B., Nakamura, J. & Liu, H. 2013 Projections of declining surface-water availability for the southwestern United States Nat. Clim. Change 3 482 486

    • Search Google Scholar
    • Export Citation
  • Sharkey, T.D., Bernacchi, C.J., Farquhar, G.D. & Singsaas, E.L. 2007 Fitting photosynthetic carbon dioxide response curves for C3 leaves Plant Cell Environ. 30 1035 1040

    • Search Google Scholar
    • Export Citation
  • Sims, D.A., Luo, Y. & Seemann, J.R. 1998 Comparison of photosynthetic acclimation to elevated CO2 and limited nitrogen supply in soybean Plant Cell Environ. 21 945 952

    • Search Google Scholar
    • Export Citation
  • Stitt, M. 1991 Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells Plant Cell Environ. 14 741 762

  • Stitt, M. & Krapp, A. 1999 The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background Plant Cell Environ. 22 583 621

    • Search Google Scholar
    • Export Citation
  • Takagi, H. 1990 Garlic Allium sativum, p. 110–157. In: H.D. Rabinowitch and J.L. Brewster (eds.). Onions and allied crops. CRC Press, Boca Raton, FL

  • Tattelman, E. 2005 Health effects of garlic Amer. Fam. Physician 72 103 106

  • Villalobos, F.J., Testi, L., Rizzalli, R. & Orgaz, F. 2004 Evapotranspiration and crop coefficients of irrigated garlic (Allium sativum L.) in a semi-arid climate Agr. Water Mgt. 64 233 249

    • Search Google Scholar
    • Export Citation
  • Volder, A., Gifford, R.M. & Evans, J.R. 2007 Effects of elevated atmospheric CO2, cutting frequency, and differential day/night atmospheric warming on root growth and turnover of Phalaris swards Glob. Change Biol. 13 1040 1052

    • Search Google Scholar
    • Export Citation
  • Vu, J.C.V., Allen, L.H., Boote, K.J. & Bowes, G. 2008 Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean Plant Cell Environ. 20 68 76

    • Search Google Scholar
    • Export Citation
  • Wheeler, T.R., Daymond, A.J., Morison, J.I.L., Ellis, R.H. & Hadley, P. 2004 Acclimation of photosynthesis to elevated CO2 in onion (Allium cepa) grown at a range of temperatures Ann. Appl. Biol. 144 103 111

    • Search Google Scholar
    • Export Citation
  • Wullschleger, S.D. 1993 Biochemical limitations to carbon assimilation in C3 plants—A retrospective analysis of the A/Ci curves from 109 species J. Expt. Bot. 44 907 920

    • Search Google Scholar
    • Export Citation
  • Xu, Z., Zhou, G. & Wang, Y. 2007 Combined effects of elevated CO2 and soil drought on carbon and nitrogen allocation of the desert shrub Caragana intermedia Plant Soil 301 87 97

    • Search Google Scholar
    • Export Citation
  • Ziska, L.H. & Bunce, J.A. 2006 Plant responses to rising atmospheric carbon dioxide, p. 17–47. In: J.I.L. Morison and M.D. Morecroft (eds.). Plant growth and climate change. Blackwell Publ., Oxford, UK

  • Ziska, L.H., Bunce, J.A., Shimono, H., Gealy, D.R., Baker, J.T., Newton, P.C.D., Reynolds, M.P., Jagadish, K.S.V., Zhu, C., Howden, M. & Wilson, L.T. 2012 Food security and climate change: On the potential to adapt global crop production by active selection to rising atmospheric carbon dioxide Proc. Biol. Sci. 279 4097 4105

    • Search Google Scholar
    • Export Citation

Contributor Notes

This work was supported by a Cooperative Research Program for Agricultural Science and Technology Development (project no. PJ01000707), Rural Development Administration, Republic of Korea.

We thank Zeesoo Han for her assistance with data collection and crop management, and Bruno Pitton and Jared Sisneroz for helpful comments on earlier drafts of the manuscript.

Corresponding author. E-mail: soohkim@uw.edu.

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    Diurnal patterns of light inside the sunlit growth chambers. (A) Illuminance data inside the growth chambers during the period of leaf gas-exchange measurements (i.e., May through June 2011). (B) Photosynthetic photon flux (PPF) inside the growth chambers collected during May and June, the 2 years (2012 and 2013) following the experiment (2011). Dashed lines represent regression curves fitted to the maximum hourly values for both data sets. (C) Daily PPF integrals from January through June periods in 2012 and 2013 (open circle); these data are shown as a proxy to represent the PPF patterns at the site during the experimental period in 2011. Also shown are monthly temperature averages with sd error bars (closed circle) inside the growth chambers.

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    Biomass by constituent part of garlic plants grown in response to ambient and elevated carbon dioxide at three nitrogen (N) levels: low-, mid-, and high-N (n = 9–10, mean ± se). (A) Leaf, (B) stem, (C) bulb, and (D) the sum of leaf, stem, and bulb parts.

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    Biomass ratios in relation to the sum of leaf, stem, and bulb parts (LSB) and bulb characteristics of garlic plants grown in response to ambient and elevated carbon dioxide and nitrogen (N) treatments: low-, mid-, and high-N (n = 9–10, mean ± se). (A) Bulb/leaf-stem-bulb (LSB) biomass ratio, (B) leaf/LSB biomass ratio, (C) bulb diameter, and (D) bulbing ratio determined as bulb diameter divided by neck diameter.

  • View in gallery

    Leaf N concentration in garlic plants in response to ambient and elevated carbon dioxide at three nitrogen (N) levels: low-, mid-, and high-N. (A) In % (w/w) and (B) C/N ratio (n = 6; mean ± se).

  • View in gallery

    Photosynthetic acclimation to elevated carbon dioxide (CO2) in garlic plants at (A) low-nitrogen (N), (B) mid-N, and (C) high-N. The ratio of net CO2 assimilation rates (A) between elevated and ambient CO2 grown leaves (n = 6–8, mean ± se) are plotted over [CO2] at the intercellular air spaces (Ci). The ratios (Aelev/Aambi) below 1 are indicative of photosynthetic downregulation.

  • Andrews, G. 1998 Growing and using garlic. Storey Books, Pownal, VT

  • Bazzaz, F.A. 1996 Plants in changing environments: Linking physiological, population, and community ecology. Cambridge Univ. Press, Cambridge, UK

  • Bertoni, G., Soubieille, P.C. & Llorens, J.M. 1992 Growth and nitrogen nutrition of garlic (Allium sativum L.) during bulb development Sci. Hort. 50 187 195

    • Search Google Scholar
    • Export Citation
  • Buwalda, J.G. 1986 Nitrogen nutrition of garlic (Allium sativum L.) under irrigation, crop growth and development Sci. Hort. 29 55 68

  • Buwalda, J.G. & Freeman, R.E. 1987 Effects of nitrogen fertilisers on growth and yield of potato (Solanum tuberosum L. ‘Ilam Hardy’), onion (Allium cepa L. ‘Pukekohe Longkeeper’), garlic (Allium sativum L. ‘Y strain’) and hybrid squash (Cucurbita maxima ‘L. Delica’) Sci. Hort. 32 161 173

    • Search Google Scholar
    • Export Citation
  • Evans, J.R. 1989 Photosynthesis and nitrogen relationships in leaves of C3 plants Oecologia 78 9 19

  • Faria, T., Wilkins, D., Besford, R.T., Vaz, M., Pereira, J.S. & Chaves, M.M. 1996 Growth at elevated CO2 leads to down-regulation of photosynthesis and altered response to high temperature in Quercus suber L. seedlings J. Expt. Bot. 47 1755 1761

    • Search Google Scholar
    • Export Citation
  • Farquhar, G.D. & Richards, R.A. 1984 Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes Funct. Plant Biol. 11 539 552

    • Search Google Scholar
    • Export Citation
  • Field, C.B., Jackson, R.B. & Mooney, H.A. 1995 Stomatal responses to increased CO2—Implications from the plant to the global-scale Plant Cell Environ. 18 1214 1225

    • Search Google Scholar
    • Export Citation
  • Food and Agriculture Organization of the United Nations 2011 The state of the world’s land and water resources for food and agriculture (SOLAW)—Managing systems at risk. Earthscan, Rome, Italy

  • Giorgi, F. & Lionello, P. 2008 Climate change projections for the Mediterranean region Global Planet. Change 63 90 104

  • Jasoni, R., Kane, C., Green, C., Peffley, E., Tissue, D., Thompson, L., Payton, P. & Pare, P.W. 2004 Altered leaf and root emissions from onion (Allium cepa L.) grown under elevated CO2 conditions Environ. Expt. Bot. 51 273 280

    • Search Google Scholar
    • Export Citation
  • Kik, C., Kahane, R. & Gebhardt, R. 2001 Garlic and health Nutr. Metab. Cardiovasc. Dis. 11 57 65

  • Kim, S.-H., Jeong, J.H. & Nackley, L.L. 2013 Photosynthetic and transpiration responses to light, CO2, temperature, and leaf senescence in garlic: Analysis and modeling J. Amer. Soc. Hort. Sci. 138 149 156

    • Search Google Scholar
    • Export Citation
  • Kim, S.-H. & Lieth, J.H. 2003 A coupled model of photosynthesis, stomatal conductance and transpiration for a rose leaf (Rosa hybrida L.) Ann. Bot. (Lond.) 91 771 781

    • Search Google Scholar
    • Export Citation
  • Kinmonth-Schultz, H. & Kim, S.-H. 2011 Carbon gain, allocation and storage in rhizomes in response to elevated atmospheric carbon dioxide and nutrient supply in a perennial C3 grass, Phalaris arundinacea Funct. Plant Biol. 38 797 807

    • Search Google Scholar
    • Export Citation
  • Körner, C. 2000 Biosphere responses to CO2 enrichment Ecol. Appl. 10 1590 1619

  • Leakey, A.D.B., Ainsworth, E.A., Bernacchi, C.J., Rogers, A., Long, S.P. & Ort, D.R. 2009 Elevated CO2 effects on plant carbon, nitrogen, and water relations: Six important lessons from FACE J. Expt. Bot. 60 2859 2876

    • Search Google Scholar
    • Export Citation
  • Meredith, T.J. 2008 The complete book of garlic: A guide for gardeners, growers, and serious cooks. Timber Press, Portland, OR

  • Monje, O. & Bugbee, B. 1998 Adaptation to high CO2 concentration in an optimal environment: Radiation capture, canopy quantum yield and carbon use efficiency Plant Cell Environ. 21 315 324

    • Search Google Scholar
    • Export Citation
  • Mortensen, L.M. 1994 Effects of elevated CO2 concentrations on growth and yield of eight vegetable species in a cool climate Sci. Hort. 58 177 185

    • Search Google Scholar
    • Export Citation
  • Nackley, L.L., Vogt, K.A. & Kim, S.-H. 2014 Arundo donax water use and photosynthetic responses to drought and elevated CO2 Agr. Water Mgt. 136 13 22

  • Paul, M.J. & Foyer, C.H. 2001 Sink regulation of photosynthesis J. Expt. Bot. 52 1383 1400

  • Pendall, E., Bridgham, S., Hanson, P.J., Hungate, B., Kicklighter, D.W., Johnson, D.W., Law, B.E., Luo, Y., Megonigal, J.P., Olsrud, M., Ryan, M.G. & Wan, S. 2004 Below-ground process responses to elevated CO2 and temperature: A discussion of observations, measurement methods, and models New Phytol. 162 311 322

    • Search Google Scholar
    • Export Citation
  • Pollock, J. & Farrar, C. 1996 Source-sink relations: The role of sucrose, p. 262–276. In: N.R. Baker (ed.). Photosynthesis and the environment. Kluwer Academic Publishers, Dordrecht, the Netherlands/Boston, MA

  • Poorter, H., Bühler, J., Van Dusschoten, D., Climent, J. & Postma, J.A. 2012 Pot size matters : A meta-analysis of the effects of rooting volume on plant growth Funct. Plant Biol. 39 839 850

    • Search Google Scholar
    • Export Citation
  • Rivlin, R.S. 2006 Is garlic alternative medicine? J. Nutr. 136 713S 715S

  • Rogers, H.H., Peterson, C., McCrimmon, J. & Cure, J. 1992 Response of plant roots to elevated atmospheric carbon dioxide Plant Cell Environ. 15 749 752

  • Rogers, H.H., Runion, G.B. & Krupa, S.V. 1994 Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere Environ. Pollut. 83 155 189

    • Search Google Scholar
    • Export Citation
  • Sage, R.F. 1994 Acclimation of photosynthesis to increasing atmospheric CO2: The gas exchange perspective Photosyn. Res. 39 351 368

  • Sage, R.F., Sharkey, T.D. & Seemann, J.R. 1989 Acclimation of photosynthesis to elevated CO2 in five C3 species Plant Physiol. 89 590 596

  • Schapendonk, A., van Oijen, M., Dijkstra, P., Pot, C., Jordi, W. & Stoopen, G. 2000 Effects of elevated CO2 concentration on photosynthetic acclimation and productivity of two potato cultivars grown in open-top chambers Funct. Plant Biol. 27 1119 1130

    • Search Google Scholar
    • Export Citation
  • Seager, R., Ting, M., Li, C., Naik, N., Cook, B., Nakamura, J. & Liu, H. 2013 Projections of declining surface-water availability for the southwestern United States Nat. Clim. Change 3 482 486

    • Search Google Scholar
    • Export Citation
  • Sharkey, T.D., Bernacchi, C.J., Farquhar, G.D. & Singsaas, E.L. 2007 Fitting photosynthetic carbon dioxide response curves for C3 leaves Plant Cell Environ. 30 1035 1040

    • Search Google Scholar
    • Export Citation
  • Sims, D.A., Luo, Y. & Seemann, J.R. 1998 Comparison of photosynthetic acclimation to elevated CO2 and limited nitrogen supply in soybean Plant Cell Environ. 21 945 952

    • Search Google Scholar
    • Export Citation
  • Stitt, M. 1991 Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells Plant Cell Environ. 14 741 762

  • Stitt, M. & Krapp, A. 1999 The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background Plant Cell Environ. 22 583 621

    • Search Google Scholar
    • Export Citation
  • Takagi, H. 1990 Garlic Allium sativum, p. 110–157. In: H.D. Rabinowitch and J.L. Brewster (eds.). Onions and allied crops. CRC Press, Boca Raton, FL

  • Tattelman, E. 2005 Health effects of garlic Amer. Fam. Physician 72 103 106

  • Villalobos, F.J., Testi, L., Rizzalli, R. & Orgaz, F. 2004 Evapotranspiration and crop coefficients of irrigated garlic (Allium sativum L.) in a semi-arid climate Agr. Water Mgt. 64 233 249

    • Search Google Scholar
    • Export Citation
  • Volder, A., Gifford, R.M. & Evans, J.R. 2007 Effects of elevated atmospheric CO2, cutting frequency, and differential day/night atmospheric warming on root growth and turnover of Phalaris swards Glob. Change Biol. 13 1040 1052

    • Search Google Scholar
    • Export Citation
  • Vu, J.C.V., Allen, L.H., Boote, K.J. & Bowes, G. 2008 Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean Plant Cell Environ. 20 68 76

    • Search Google Scholar
    • Export Citation
  • Wheeler, T.R., Daymond, A.J., Morison, J.I.L., Ellis, R.H. & Hadley, P. 2004 Acclimation of photosynthesis to elevated CO2 in onion (Allium cepa) grown at a range of temperatures Ann. Appl. Biol. 144 103 111

    • Search Google Scholar
    • Export Citation
  • Wullschleger, S.D. 1993 Biochemical limitations to carbon assimilation in C3 plants—A retrospective analysis of the A/Ci curves from 109 species J. Expt. Bot. 44 907 920

    • Search Google Scholar
    • Export Citation
  • Xu, Z., Zhou, G. & Wang, Y. 2007 Combined effects of elevated CO2 and soil drought on carbon and nitrogen allocation of the desert shrub Caragana intermedia Plant Soil 301 87 97

    • Search Google Scholar
    • Export Citation
  • Ziska, L.H. & Bunce, J.A. 2006 Plant responses to rising atmospheric carbon dioxide, p. 17–47. In: J.I.L. Morison and M.D. Morecroft (eds.). Plant growth and climate change. Blackwell Publ., Oxford, UK

  • Ziska, L.H., Bunce, J.A., Shimono, H., Gealy, D.R., Baker, J.T., Newton, P.C.D., Reynolds, M.P., Jagadish, K.S.V., Zhu, C., Howden, M. & Wilson, L.T. 2012 Food security and climate change: On the potential to adapt global crop production by active selection to rising atmospheric carbon dioxide Proc. Biol. Sci. 279 4097 4105

    • Search Google Scholar
    • Export Citation
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