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TECHNICAL REPORTS

Atmospheric Pollutants and Trace Gases

Growth and Yield Responses of Potato to Mixtures of Carbon Dioxide and Ozone

^a USDA Agricultural Research Service, Air Quality–Plant Growth and Development Research Unit, 3908 Inwood Road, Raleigh, NC 27603
^b Department of Crop Science, North Carolina State University, Raleigh, NC 27695

^* Corresponding author (ahea{at}earthlink.net).

Received for publication July 1, 2002.

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Elevated carbon dioxide (CO₂) concentrations in the atmosphere can stimulate plant growth and yield, whereas ground-level ozone (O₃) concentrations cause the opposite effect in many areas of the world. Recent experiments show that elevated CO₂ can protect some plants from O₃ stress, but this has not been tested for most crop species. Our objective was to determine if elevated CO₂ protects Irish potato (Solanum tuberosum L.) from foliar injury and suppression of growth and yield caused by O₃. An O₃–resistant cultivar (Superior) and an O₃–sensitive cultivar (Dark Red Norland) were exposed from within 10 d after emergence to maturity to mixtures of three CO₂ and three O₃ treatments in open-top field chambers. The three CO₂ treatments were ambient (370 µL L^-1) and two treatments with CO₂ added to ambient CO₂ for 24 h d^-1 (540 and 715 µL L^-1). The O₃ treatments were charcoal-filtered air (15 nL L^-1), nonfiltered air (45 nL L^-1), and nonfiltered air with O₃ added for 12 h d^-1 (80 nL L^-1). Elevated O₃ and CO₂ caused extensive foliar injury of Dark Red Norland, but caused only slight injury of Superior. Elevated CO₂ increased growth and tuber yield of both cultivars, whereas elevated O₃ generally suppressed growth and yield, mainly of Dark Red Norland. Elevated CO₂ appeared to protect Dark Red Norland from O₃–induced suppression of shoot, root, and tuber weight as measured at midseason but did not protect either cultivar from O₃ stress at the final harvest. The results further illustrate the difficulty in predicting effects of O₃ + CO₂ mixtures based on the effects of the individual gases.

Abbreviations: DAP, days after planting

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OZONE CONCENTRATIONS in the troposphere are high enough to suppress plant growth and yield in many areas of the world (Heck et al., 1984; USEPA, 1996), whereas CO₂ concentrations are expected to continue rising to levels that significantly increase plant growth and yield (Kimball et al., 1993; Watson et al., 1990).

Research to measure effects of mixtures of O₃ and CO₂ often shows that growth stimulation caused by CO₂ enrichment is greater when O₃ concentrations are also high (Barnes and Pfirrmann, 1992; Heagle et al., 1998; Idso and Idso, 1994; Miller et al., 1998; Mulchi et al., 1992). Apparently, CO₂ can protect some plants from O₃ stress. When this occurs, CO₂ response curves are steeper for plants exposed simultaneously to stressful levels of O₃ than for plants exposed to lower O₃ levels. An exception occurred for an O₃–sensitive selection (S156) of bean (Phaseolus vulgaris L.), however. Ozone injured S156 as much at elevated as at ambient CO₂, and the response to CO₂ enrichment was similar at all O₃ levels (Heagle et al., 2002).

Plant species and cultivars vary in response to elevated O₃ and CO₂ singly and to mixtures of CO₂ and O₃. Cultivars of Irish potato display a wide range in sensitivity to O₃ (Brasher et al., 1973; DeVos et al., 1983; Heggestad, 1973). Some cultivars such as Superior and Kennebec are relatively resistant whereas others such as Norchip and Norland are relatively sensitive (Heggestad, 1973; Holmes et al., 1998). Several studies have confirmed that ambient concentrations of O₃ can suppress tuber yield (Pell et al., 1988) and affect tuber quality (Pell and Pearson, 1984). Elevated CO₂ generally increases potato yield (Donnelly et al., 2001b; Miglietta et al., 1998; Schapendonk et al., 2000).

Effects of season-long exposure to mixtures of CO₂ and O₃ on potato (cv. Bintje) were reported recently from several locations in Europe. Elevated CO₂ usually increased tuber yield and ameliorated foliar injury caused by O₃ (Finnan et al., 2002; Donnelly et al., 2001b; Lawson et al., 2001). However, the O₃ stress in these European studies was not great enough to significantly decrease tuber yield, and significant protection from O₃–induced suppression of tuber yield by elevated CO₂ was not shown. Our objective was to investigate the effects of mixtures of CO₂ and O₃ on foliar injury, growth, and yield of potato. We examined the effects of season-long exposure to mixtures of three CO₂ and three O₃ concentrations on an O₃–resistant and an O₃–sensitive cultivar of potato in open-top field chambers.

	MATERIALS AND METHODS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Cultural
The experiment was performed at our field site 5 km south of Raleigh, NC (35.4° N, 78.4° W). The potato cultivars Superior and Dark Red Norland were chosen based on observed cultivar differences in foliar sensitivity to O₃ at Raleigh (Holmes et al., 1998) and at other locations (Heggestad, 1973; Brasher et al., 1973). Superior is very resistant, whereas Dark Red Norland is very sensitive to O₃.

Plants were started using whole potato seed tubers. Mean weight per tuber was 62 g (52–71 g) for Superior and 103 g (85–131 g) for Dark Red Norland. One tuber per pot was planted on 28 Mar. 2001 in 21-L pots filled with Metro-Mix 200 and 45 g of Osmocote (14–14–14, N–P–K) slow-release fertilizer (Scotts-Sierra Horticultural Products Co., Marysville, OH). The fertilizer was placed in a layer (approximately 20 cm in diameter) approximately 3 cm below each potato seed tuber. Four pots were placed in each of four rows in each chamber. The eight pots of each cultivar were arranged so that two pots of a given cultivar were not adjacent to each other within a given row or column. Plants began emerging 18 days after planting (DAP) and were irrigated throughout the season with drip tubes to prevent chronic water stress. Pot rooting medium temperature was moderated with an insulating cylinder composed of 0.6-cm-thick bubble wrap coated on both sides with aluminum (Reflectix, Markleville, IN) wrapped tightly around each pot (Heagle et al., 1999). All plants were treated at 57 DAP with imidacloprid [1-((6-chloro-3-pyridinyl)methyl)-N-nitro-imidazolidinimine] (Provado 1.6F) at 1.8 mL L^-1 to control aphids in a few plots.

Exposures
Plants were exposed to O₃ and CO₂ in open-top field chambers, 3 m in diameter x 2.4 m tall (Heagle et al., 1973). General dispensing and monitoring protocols have been described for O₃ (Heagle et al., 1979b) and for CO₂ (Rogers et al., 1983). Carbon dioxide exposures began at 26 DAP and O₃ exposures began at 27 DAP. Ozone was dispensed 12 h d^-1 (0800–2000 h EST), and CO₂ was dispensed for 24 h d^-1. The whole plot (chamber) design was the nine possible paired combinations of three O₃ and three CO₂ treatments. The O₃ treatments were charcoal-filtered air (approximately 0.3 times ambient O₃), nonfiltered air (approximately 0.9 times ambient O₃), and nonfiltered air with O₃ added proportionally to the ambient O₃ concentration (approximately 1.6 times ambient O₃). The CO₂ treatments were ambient (seasonal 12 h d^-1 mean of 370 µL L^-1), and two treatments with CO₂ added to achieve proportions of approximately 1.5 and 1.9 times ambient. Both gases were monitored for 24 h d^-1 at canopy height in the center of each chamber. Ozone was monitored with UV analyzers (TECO Model 49; Thermo Environmental, Franklin, MA) calibrated biweekly with a TECO Model 49 PS calibrator. Carbon dioxide was monitored with infrared analyzers (LI 6252; LI-COR, Lincoln, NE) calibrated biweekly with pressurized tank CO₂ over the range of concentrations used in these experiments. Exposures continued until 104 DAP except during thunderstorms or equipment malfunction (Table 1).

Stomatal conductance and transpiration measurements were made for each of four treatment combinations containing the highest and lowest O₃ and CO₂ concentrations using a LI-1600 steady state porometer (LI-COR). Measures were made at midday for both surfaces of at least two upper canopy (full-sun-exposed) leaves per plant on two or more plants of each cultivar. Two replicates of each treatment combination were sampled at 82 and 84 DAP, and one replicate was sampled at 76, 89, and 90 DAP.

First Harvest
Two plants of each cultivar were harvested from the southern row of each chamber at 75 DAP (11 June). Foliar injury was estimated in 5% increments (0–100%) for five leaves at alternating nodes on one dominant stem of each plant. The remaining stems and leaves were bagged separately, dried, and weighed. Dried leaves from the six plants of each cultivar per chamber were combined and ground to pass a 2-mm screen. Ground leaf samples were analyzed for carbon and nutrient elements. One day after harvest, tubers were measured and separated into small (<35 mm in diameter), medium (35–50 mm in diameter), and large (>50 mm in diameter) sizes. Tubers in each size class were counted and weighed separately.

Final Harvest
Six plants of each cultivar in each chamber were harvested by removing consecutive rows at 103, 104, and 105 DAP (9, 10, and 11 July). Tubers were cleaned, separated into the three size classes, and counted and weighed as described for the first harvest. Roots were washed, dried, and weighed. A section (2 to 3 cm thick) from one large tuber per plant was cut and weighed immediately. Each section was subdivided, dried at 50°C to constant weight, and weighed. The dry weight to fresh weight ratios of each 2- to 3-cm tuber section was calculated to indicate percent dry matter. One subdivided tuber piece from each of the six plants for each cultivar per chamber was combined, ground to pass a 2-mm mesh screen, and analyzed for carbon and nutrient elements.

Statistical Analyses
Split-plot models were used to analyze means of all pots per chamber for a given harvest for all measured response variables. The O₃ and CO₂ treatment combination was the whole-plot treatment and the subplot factor was the two cultivars. The assumption of equal variances between the cultivars was evaluated for a representative subset of tuber number, tuber weight, and element responses. The assumption of homogeneous variances was not obviously violated in the responses examined. All models were fit using SAS PROC GLM (SAS Institute, 1990) with the treatment factors (cultivar, O₃, and CO₂) as fixed effects and the replicate x CO₂ x O₃ terms treated as random effects. The significance of treatments and interactions between treatments was tested with F tests. The error term used in the denominator of the F statistic was replicate x CO₂ x O₃ for the whole-plot effects, and the residual for the subplot effects. Only standard errors were calculated for stomatal conductance data.

	RESULTS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Stomatal Conductance
Stomatal conductance decreased as the season progressed for both cultivars (Table 2). In the open-top chamber receiving charcoal-filtered air (CF) treatment, stomatal conductance was generally lower at the elevated than at ambient CO₂. This was also true for Superior in the high O₃ treatment, except at 90 DAP. However, for Dark Red Norland in the high O₃ treatment, there was no consistent CO₂ effect on conductance. With few exceptions, for both cultivars, conductance at 80 nL L^-1 O₃ was usually less than at 15 nL L^-1.

View this table: [in this window] [in a new window]   Table 3. Effect of ozone (O3) and carbon dioxide (CO2) mixtures on foliar injury, weight of stems, leaves, and roots, and number and weight of tubers at the first harvest on 11 June, 75 d after planting.

The trend for O₃–induced suppression of leaf, stem, and root weight of Dark Red Norland at 370 µL L^-1 CO₂ was diminished or absent at 540 and 715 µL L^-1 and was reversed for Superior at 715 µL L^-1. This same trend (diminished O₃–induced suppression with increased CO₂) was also evident for Dark Red Norland tubers. At ambient CO₂, total tuber yield at 80 nL L^-1 was 66% less than at 15 nL L^-1, but at double-ambient CO₂, yield was almost identical at 80 and 15 nL L^-1 (Table 3). The significance of the cultivar x CO₂ x O₃ interaction for large tuber weight (P 0.08) was apparently due to different amounts of O₃ suppression across CO₂ levels for Dark Red Norland and little or no suppressive effect of O₃ on Superior at all CO₂ levels (Table 3).

Final Harvest
Elevated CO₂ significantly increased tuber number, tuber weight, tuber solids, and root weight (Table 4). Elevated CO₂ generally caused more tuber weight increase for Dark Red Norland than Superior, and the cultivar x CO₂ interaction was significant for most tuber variables. Elevated CO₂ increased tuber solids more for Superior than for Dark Red Norland.

View this table: [in this window] [in a new window]   Table 4. Effect of ozone (O3) and carbon dioxide (CO2) mixtures on number and weight of tubers, tuber solids, and root weight of Dark Red Norland and Superior potatoes at the final harvest.

There were no significant CO₂ x O₃ interactions for any measured response for either cultivar. The significant cultivar x CO₂ x O₃ interaction for medium tuber number (P 0.03) and weight (P 0.07) was apparently caused by greater O₃–induced tuber suppression at high than at low CO₂ concentrations for Dark Red Norland but no O₃–induced suppression at any CO₂ concentration for Superior. The significant cultivar x CO₂ x O₃ interaction for root weight may have been caused by O₃–induced suppression of Dark Red Norland roots, but not of Superior roots, at high than at low CO₂. Cause for the significant cultivar x CO₂ x O₃ interaction for tuber solids was not apparent.

Foliar Elements
Except for C and K, concentrations of all elements were higher in Dark Red Norland than in Superior (Table 5). Tissue levels of C, N, Zn, and Cu decreased with increasing CO₂ exposure (Table 5). Iron increased with increasing CO₂ in Dark Red Norland but not in Superior, whereas C increased with increasing O₃ more in Dark Red Norland than in Superior (Table 5). Potassium decreased with increasing O₃ at all CO₂ levels in Dark Red Norland but not in Superior (Table 5). Carbon, Fe, Zn, and Cu levels were generally higher at high than low O₃ in both cultivars (Table 5). Manganese increased with increased O₃ at all CO₂ levels for Superior, but this occurred only at ambient CO₂ for Dark Red Norland (Table 5).

	DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Although plant growth in pots will be different from plant growth in the ground, there is increasing evidence that plant response to CO₂ enrichment is not necessarily affected by baseline plant growth rates. For example, whereas growth and yield of cotton (Gossypium hirsutum L.) and winter wheat (Triticum aestivum L.) plants grown in open-top field chambers were different than that of plants grown outside, proportional response to CO₂ enrichment was similar for plants in both environments (Kimball et al., 1993). For soybean [Glycine max (L.) Merr.], baseline growth and yield were significantly different for plants grown in 15-L pots and in the ground, but the proportional yield response to CO₂ enrichment was similar under both conditions (Heagle et al., 1999). Differences in baseline growth and yield per se do not appear to have major effects on plant response to O₃ either. Soybean, field corn (Zea mays L.), and winter wheat response to elevated O₃ was similar for plants grown in 15-L pots or in the ground (Heagle et al., 1979a, c, 1983).

Demonstrating significant protection from O₃ stress by elevated CO₂ during concurrent exposure to CO₂ and O₃ requires the potential for significant O₃ stress. Significant O₃ stress was present in several previous studies with soybean, cotton, and winter wheat, in which elevated CO₂ provided significant protection. At the first harvest of the present study, elevated CO₂ appeared to prevent O₃–induced suppression of tuber yield (especially large tubers) of Dark Red Norland. For example, at ambient CO₂, total tuber yield at 80 nL L^-1 was 88% less than at 15 nL L^-1, whereas at double ambient CO₂, O₃ did not affect yield. However, at the final harvest of the present study and for a previous study with bean (Heagle et al., 2002), elevated CO₂ did not provide significant protection. Too much O₃ stress may have offset possible protection of bean by elevated CO₂ (Heagle et al., 2002). One reason for protection of Dark Red Norland early in the season but not later may be related to different degrees of O₃ stress. Ozone stress is cumulative with continuing daily exposure, so the degree of stress that had accumulated at the first harvest was much less severe than occurred between the first and final harvest.

A European project "Changing Climate and Potential Impacts on Potato Yield and Quality" (CHIPS) using the cultivar Bintje (Fangmeier et al., 2002) and the present study both show that elevated CO₂ generally decreases nutrient element concentrations and that elevated O₃ generally increases element concentrations in potato. However, there was little agreement between the two studies regarding effects on individual elements. For example, for shoot analyses, we showed that CO₂ decreased C, N, and Zn and that O₃ increased C, Fe, and Zn whereas the CHIPS project reported that elevated CO₂ decreased shoot P and K and that O₃ increased Ca. For tuber elements, we found that elevated CO₂ decreased N, P, and Zn, whereas CHIPS reported decreased N, K, and Mg. We found that O₃ exposure increased tuber N, P, K, and Zn, and CHIPS reported that O₃ increased N and Mn. Differences in experimental methods (nutrient availability, climate, and cultivar, etc.) may be responsible for these differences, but specific reasons are unknown.

Reports of foliar injury of crop species caused by elevated O₃ and by elevated CO₂ are fairly common, and this occurred for Dark Red Norland in the present experiment. In most studies with mixtures of O₃ and CO₂, elevated CO₂ has protected plants from injury caused by O₃, and this has been reported for Bintje potato (Donnelly et al., 2001a; Finnan et al., 2002). However, elevated CO₂ did not protect Dark Red Norland in the present experiment; at 80 nL L^-1 O₃ foliar injury increased as the CO₂ concentration increased. We were not able to determine if stress caused by O₃ predisposed leaves to injury caused by CO₂ or vice-versa. This unusual interaction highlights a need to better understand mechanisms whereby O₃ and CO₂ cause injury per se and how they may interact to alleviate or exacerbate foliar injury.

Exact mechanisms whereby elevated CO₂ protects plants from O₃ stress remain unknown. Elevated CO₂ routinely decreases stomatal conductance, but our measurements have not been detailed enough to show if differences in conductance can explain differences in the level of protection. Protection might result from increased rates of repair of incipient O₃ injury, but measures to identify biochemical mechanisms to explain this possibility are also rudimentary. Mechanisms whereby elevated CO₂ protects plants from O₃ stress must be identified to better estimate the influence of elevated CO₂ concentrations on food and fiber production.

	ACKNOWLEDGMENTS

 
We thank Bob Philbeck, Fred Mowry, and Jeff Barton for dispensing and monitoring support; Brandon Puckett, Phillip Cathcart, Gwen Palmer, Michael Durham, Renee Tucker, and Salvio Torres for technical support; Marc Cubeta for supplying seed tubers, technical advice, and review of this manuscript; Douglas Sanders for technical advice; Julie Pilar-McIntyre and Leonard Stefanski for statistical analyses; and Barbara Shew for review of this manuscript.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Cooperative investigation of the USDA-ARS Air Quality Research Unit and North Carolina State University. Funded in part by the North Carolina Agricultural Research Service. The use of trade names in this publication does not imply endorsement by the North Carolina Agricultural Research Service or the USDA of the products named, nor criticism of similar ones not mentioned.

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