Journal of Experimental Botany

JXB Advance Access originally published online on October 29, 2003

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Journal of Experimental Botany, Vol. 54, No. 393, pp. 2769-2774, December 1, 2003
© 2003 Oxford University Press

Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to Free Air CO₂ Enrichment (FACE)

Received 10 July 2003; Accepted 30 July 2003

Elizabeth A. Ainsworth¹, Alistair Rogers^1,2, Herbert Blum³, Josef Nösberger³ and Stephen P. Long^*,1

¹ Departments of Crop Sciences and of Plant Biology, University of Illinois, Urbana-Champaign, 379 Edward R. Madigan Laboratory, 1201 W. Gregory Drive, Urbana, IL 61801, USA
² Department of Environmental Sciences, Brookhaven National Laboratory, Upton, NY 11973-5000, USA
³ Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Zürich, Switerland

* To whom correspondence should be addressed. Fax: +1 217 244 7563. E-mail: stevel{at}life.uiuc.edu
Abbreviations: A_sat, light-saturated rate of leaf CO₂ assimilation at growth [CO₂]; c_a, atmospheric CO₂ concentration; c_i, intercellular CO₂ concentration; FACE, Free Air CO₂ Enrichment; g_s, stomatal conductance to water vapour; J_max, in vivo maximum rate of electron transport; V_c,max, in vivo maximum rate of carboxylation.

	Abstract

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The initial stimulation of photosynthesis observed on elevation of [CO₂] in grasslands has been predicted to be a transient phenomenon constrained by the loss of photosynthetic capacity due to other limitations, notably nutrients and sinks for carbohydrates. Legumes might be expected partially to escape these feedbacks through symbiotic N₂ fixation. The Free-Air Carbon dioxide Enrichment (FACE) experiment at Eschikon, Switzerland, has been the longest running investigation of the effects of open-air elevation of [CO₂] on vegetation. The prediction of a long-term loss of photosynthetic capacity was tested by analysing photosynthesis in Trifolium repens L. (cv. Milkanova) in the spring and autumn of the eighth, ninth and tenth years of treatment. A high and low N treatment also allowed a test of the significance of exogenous N-supply in maintaining a stimulation of photosynthetic capacity in the long-term. Prior work in this Free Air CO₂ Enrichment (FACE) experiment has revealed that elevated [CO₂] increased both vegetative and reproductive growth of T. repens independent of N treatment. It is shown here that the photosynthetic response of T. repens was also independent of N fertilization under both current ambient and elevated (600 µmol mol^–1) [CO₂]. There was a strong effect of season on photosynthesis, with light-saturated rates (A_sat) 37% higher in spring than in autumn. Higher A_sat in the spring was supported by higher maximum Rubisco carboxylation rates (V_c,max) and maximum rates of electron transport (J_max) contributing to RuBP regeneration. Elevated [CO₂] increased A_sat by 37% when averaged across all measurement periods and both N fertilization levels, and decreased stomatal conductance by 25%. In spring, there was no effect of elevated [CO₂] on photosynthetic capacity of leaves, but in autumn both V_c,max and J_max were reduced by approximately 20% in elevated [CO₂]. The results show that acclimation of photosynthetic capacity can occur in a nitrogen-fixing species, in the field where there are no artificial restrictions on sink capacity. However, even with acclimation there was a highly significant increase in photosynthesis at elevated [CO₂].

Key words: Acclimation, gas exchange, global atmospheric change, global climate change, grassland, nitrogen fixation, photosynthetic electron transport, Rubisco, white clover.

	Introduction

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Species capable of symbiotic N₂ fixation often show a larger stimulation of growth and photosynthetic rate to elevated atmospheric carbon dioxide concentration ([CO₂]) than species or genotypes that do not fix N₂ (Soussana and Hartwig, 1996; Clark et al., 1997; Hebeisen et al., 1997; Schenk et al., 1997; Lüscher et al., 1998, 2000; Ainsworth et al., 2002). One explanation for the greater stimulation in the growth of N₂-fixing species grown at elevated [CO₂] is a smaller tendency toward photosynthetic acclimation, i.e. down-regulation of photosynthetic capacity in leaves developed in elevated [CO₂] (Ryle et al., 1992; Davey et al., 1999). Down-regulation of photosynthetic capacity in response to elevated [CO₂] most commonly involves a decrease in the amount of active Rubisco (Long and Drake, 1992; Rogers and Humphries, 2000). Accelerated growth under elevated [CO₂] increases the demand for nutrients and, in fertile soils, nitrogen is usually the growth-limiting nutrient (Lüscher et al., 1998). In elevated [CO₂] and a limiting N-supply, Rubisco content is often reduced (Rogers et al., 1998). It is possible that because Rubisco can account for a large proportion of leaf N, the amount of the enzyme may be reduced under N-limiting conditions (Drake et al., 1997). Clearly, under elevated [CO₂], N₂-fixing species would have an added advantage over non-N₂-fixing species, and may be able to sustain a higher Rubisco concentration and photosynthetic capacity. On the other hand, in the long-term a decrease in photosynthetic capacity may result because of changes at the whole plant and system level. Elevated [CO₂] may partition resources away from leaves and, through increased production, sequester nutrients into organic matter causing deficiencies which indirectly cause decreased photosynthetic capacity. By modelling these system level feedbacks, Luo and Reynolds (1999) predicted that the initial stimulation of photosynthetic production in grasslands would be lost within nine years of a step increase in [CO₂], as imposed in FACE experiments.

While plants may face increased N demand under elevated [CO₂], evidence suggests that the fundamental cause of acclimation is an inability of plants to utilize photosynthate (Stitt and Krapp, 1999; Ainsworth et al., 2003). Therefore, the strong carbon demand of N₂-fixing species and their ability to adjust symbiotic nitrogen fixation to the growing demand may play an important role in the response to elevated [CO₂] (Zanetti et al., 1996; Lüscher et al., 1998). Trifolium repens (L.) is an important N-fixing species in temperate pastures and grasslands (Parsons et al., 1991). The nodulated root can require up to 60% of the photosynthate produced over a 12 h photoperiod (Gordon et al., 1987). In addition to nodules, T. repens has a large reserve organ (stolon) for starch and vegetative storage proteins, which adds to the strong sink demand of the species. However, the sink demand of T. repens is seasonal. Late in the growing season, when root temperatures drop below 10 °C, shoot growth is greatly reduced, N₂ fixation is inhibited, and vegetative storage proteins begin to accumulate in stolons (Bouchart et al., 1998).

The Free Air CO₂ Enrichment (FACE) experiment at Eschikon in Switzerland, has been investigating the effects of elevated [CO₂] on grassland vegetation under completely open-air conditions. It has been the longest running replicated FACE experiment in the world. It therefore provides a unique opportunity to test predictions on how the grassland legume, T. repens, responds in the long-term to elevated [CO₂]. It has already been shown that growth at elevated [CO₂] in this experiment significantly increased the percentage of plant N derived from symbiotic N₂ fixation in T. repens grown under both high and low N fertilization treatments (Zanetti et al., 1996). Early in the growing season, under low fertilization conditions and elevated [CO₂], over 70% of plant N was derived from symbiosis (Zanetti et al., 1996). However, late in the growing season, the percentage of plant N derived from symbiosis was significantly less, particularly under high N fertilization where it provided less than 10% of total plant N (Zanetti et al., 1996).

In this study, the photosynthetic response of T. repens to elevated [CO₂] in the field at the FACE experiment in Eschikon, Switzerland was investigated after eight years of treatment. Although many studies have examined the effects of elevated [CO₂] on the acclimation of photosynthesis, few have examined either the effect following such a long period (8 years) under open-air treatment, or considered N-fixing species. The responses of light-saturated photosynthesis (A_sat) to intercellular [CO₂] (c_i) were examined at two contrasting periods: early in the growing season when plants were vigorously growing and deriving a significant portion of their N from symbiotic fixation, and late in the autumn, after the first frost, when symbiotic N₂ fixation was low. The aims of this work with T. repens were to determine if there was acclimation of photosynthesis in T. repens in response to long-term growth at elevated [CO₂] and, if so, the extent to which this offset the stimulation of photosynthesis that would otherwise have occurred. Specifically, this work examines two contrasting predictions. (1) Despite long-term growth at elevated [CO₂], there will be no acclimation of photosynthetic capacity because of the N-fixing capacity of the species. (2) Acclimation will occur because of system-level feedbacks that limit the response of grasslands to elevated [CO₂] (Luo and Reynolds, 1999).

	Materials and methods

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Growth conditions and experimental design
Trifolium repens L. (cv. Milkanova) was grown in monoculture plots in the Swiss FACE array (Hebeisen et al., 1997) at Eschikon, Switzerland (8°41' E, 47°27' N), 550 m above sea level. The experiment was designed as a split-plot with three blocks. Blocks were organized according to the crops grown in the year preceding the installation of the FACE facility in 1993. The main plot treatment was carbon dioxide concentration ([CO₂]), with three 18 m diameter circular plots maintained at ambient [CO₂] (360 µmol mol^–1) and three plots maintained at elevated [CO₂] (600 µmol mol^–1). Elevated [CO₂] was obtained using the FACE technology described by Lewin et al. (1992). Fumigation began each year in March when air temperature at 2 m above-ground reached 5 °C; active growth of T. repens requires temperatures above 5 °C (Hart, 1987). Detailed descriptions of the experimental site and initial field conditions are provided by Zanetti et al. (1996) and Lüscher et al. (1998). Within each ring, T. repens stands were grown under two N fertilization levels, 140 and 560 kg N ha^–1 year^–1 applied as NH₄NO₃. Swards were defoliated five times per growing season between April and the beginning of November, and each defoliation removed approximately 80% of the above-ground biomass.

Leaf photosynthetic gas exchange
Photosynthetic gas exchange measurements were taken from 8–12 October 2000, 1–3 May 2001, 25 April to 1 May 2002, and 15–18 October 2002. Measurements in April and May (2001 and 2002) were taken before the first harvest, and measurements in October were taken before the final harvest of the season. The average temperature, total precipitation and average sum global radiation during the times of measurement are listed in Table 1. The response of photosynthesis (A) to changes in intercellular [CO₂] (c_i) was measured with a portable, steady-state gas-exchange system, incorporating an infrared gas analyser (LI-6400, Li-Cor, Lincoln, NE, USA). Photosynthesis was initially induced at the growth [CO₂]. The reference [CO₂] was reduced stepwise to a lower concentration of 50 µmol mol^–1 and then increased stepwise to an upper concentration of 1200–1400 µmol mol^–1. Light-saturated photosynthetic rate (A_sat) and stomatal conductance to water vapour (g_s) at growth [CO₂] were extrapolated from A/c_i response curves. Three to four leaves were measured for each N treatment within each ring. The objective was to infer changes in the underlying photosynthetic capacity of leaves. Transient decrease in water potential, decrease in chloroplast inorganic phosphate concentration, and decrease in maximum photosystem II efficiency can all occur after a few hours of sunlight, and may all alter the A/c_i response. To avoid this complication, gas exchange analysis was conducted on cut leaves, sampled pre-dawn and kept with petioles in water and at low light prior to measurement. Leaves were sampled from the canopy and removed by cutting the petiole under water. A/c_i response curves were measured within 5 h of cutting the leaves. Rates of photosynthesis measured on leaves, sampled in this way, equalled or exceeded those measured in situ suggesting that this procedure did not lower photosynthetic capacity. In total, 184 A/c_i curves, each of 10–11 data points were determined. A Peltier cooling system maintained leaf temperature at 25 °C and an integral red/blue LED light source provided saturating light of 1250 µmol m^–2 s^–1.

View this table: [in this window] [in a new window]   Table 1. The dates of photosynthesis measurements and the meteorological data, mean air temperature (measured over 24 h), average total daily global radiation, and total precipitation, describing the days are listed

 
Photosynthetic parameters were calculated by fitting the equations of Farquhar et al. (1980) and by maximum likelihood regression (Sigmaplot, Jandel Scientific, Erkrath, Germany). The maximum in vivo Rubisco activity (V_c,max) was determined from points below the inflexion of the A/c_i plot, and the maximum in vivo electron transport rate (J_max) was determined from values above the inflexion (Fig. 1).

View larger version (21K): [in this window] [in a new window]   Fig. 1. Average plots of A/ci response curves for T. repens grown (A) at the beginning of the growing season and (B) at the end of the growing season. The modelled values of the maximum RuBP-saturated rate of carboxylation in vivo (Vc,max) and the maximum in vivo rate of electron transport contributing to RuBP regeneration (Jmax) are fitted for each plot. White symbols represent control [CO2] and black circles represent FACE.

 
Statistical analysis
The statistical analysis was carried out using the general linear model (GLM) procedure of the SAS package (SAS Institute, 1996). The original model was a split-plot in time with [CO₂] as the main plot factor and N as the split-plot factor. However, there was no significant effect of N on any of the variables, so N treatments were pooled for the analysis. The [CO₂] effect was tested with the [CO₂] x block interaction as the error term. Preplanned comparisons of means within measurement periods were carried out using linear contrasts.

	Results

Top Abstract Introduction Materials and methods Results Discussion References

 
Growth of T. repens at elevated [CO₂] (600 µmol mol^–1) significantly stimulated the light-saturated photosynthetic rate (A_sat) by 37%, when averaged across all measurement periods (P <0.05, Fig. 2A). Comparisons within [CO₂] treatments revealed that A_sat was higher in the spring (May 2001 and April 2002) than in the autumn (October 2000 and October 2002) (P <0.01 for ambient [CO₂], P <0.001 for elevated [CO₂]). The difference in spring and autumn photosynthetic rates was greater for plants grown at elevated [CO₂] (40% higher in spring) than plants grown at ambient [CO₂] (22% higher in spring).

View larger version (26K): [in this window] [in a new window]   Fig. 2. (A) Light-saturated photosynthetic rate at growth [CO2] (Asat), (B) stomatal conductance to water vapour (gs), and (C) ratio of intercellular CO2 concentration (ci): atmospheric CO2 concentration (ca) for T. repens grown under control (360 µmol mol–1, white bars) and elevated (FACE 600 µmol mol–1, black bars) [CO2] (±1 SE). Mean control and FACE values within time periods (n=6) were separated using linear contrast statements. *P <0.05, **P <0.01, ***P <0.001.

 
The average A/c_i response for plants grown at ambient and elevated [CO₂] during each measurement period is shown in Fig. 1. There was no change in the photosynthetic capacity of T. repens with growth at elevated [CO₂] in May 2001 and April 2002 (Fig. 3), but there was significant down-regulation of photosynthetic capacity in October 2000 and October 2002 (Fig. 3). In October 2000 and October 2002, V_c,max was 19% lower in plants grown under elevated [CO₂] (Fig. 3A), and J_max was 18% lower (Fig. 3B). The ratio of V_c,max:J_max was 0.41, when averaged over all treatments and measurement periods, and was not significantly affected by [CO₂] or season.

View larger version (30K): [in this window] [in a new window]   Fig. 3. (A) Maximum in vivo Rubisco activity (Vc,max), and (B) maximum in vivo electron transport rate (Jmax) of T. repens grown under control (360 µmol mol–1, white bars) and elevated (FACE 600 µmol mol–1, black bars) [CO2] (±1 SE). Mean control and FACE values within time periods (n=6) were separated using linear contrast statements. *P <0.05, **P <0.01, ***P <0.001.

 
Growth at elevated [CO₂] caused a 25% decrease in stomatal conductance (g_s) when averaged over all measurement periods (Fig. 2B). There was no affect of season on g_s of plants grown at ambient [CO₂]; however, g_s was significantly lower in the autumn than the spring for plants grown at elevated [CO₂] (P <0.01, Fig. 2B). The ratio of intercellular [CO₂] (c_i) to atmospheric [CO₂] (c_a) for T. repens was not affected by growth [CO₂] or season (Fig. 2C).

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
T. repens was exposed to elevated [CO₂] and two N fertilization treatments in the field since 1993. There was no effect of N fertilization on T. repens photosynthesis, and prior work has revealed that the growth of T. repens is also unaffected by N fertilization in this experiment (Hebeisen et al., 1997). Long-term growth at elevated [CO₂] is associated with consistently higher photosynthetic rates (Fig. 2A) and lower rates of stomatal conductance (Fig. 2B). The 40% increase in A_sat in the spring and 22% increase in A_sat in the autumn is in close agreement with previously published data for this species (Greer et al., 2000; Laing et al., 2002). The measured 25% reduction in g_s closely agrees with the 24% decrease in g_s reported for 13 prairie grassland species (Lee et al., 2001). However, no change in the c_i:c_a at elevated [CO₂] was observed, indicating that reductions in g_s did not affect photosynthesis any more than at ambient [CO₂] (Drake et al., 1997). These results do not support the prediction that the response of grassland species to elevated [CO₂] will be short-lived as the demand for nutrients increases (Luo and Reynolds, 1999). Increased N₂ fixation per plant under elevated [CO₂] may have allowed for sustained stimulation of photosynthetic capacity, enhancing the response of the ecosystem to elevated [CO₂] (Zanetti et al., 1996).

In the spring, there was no change in photosynthetic capacity of plants with growth at elevated [CO₂]. However, acclimation of photosynthesis to elevated [CO₂] was apparent in October 2000 and October 2002 (Fig. 3). While the cause of acclimation of photosynthesis was not directly measured, the timing of acclimation suggests that sink limitation plays a major role. Observational evidence from many field experiments with white clover in this region showed that the leaf area index of white clover was rapidly decreasing in October (Hebeisen et al., 1997). In addition, the rate of leaf emergence was very low at temperatures below 10 °C (Stäheli Posch, 1998). Acclimation occurred late in the growing season, when the 24 h mean temperature had dropped below 10 °C, and nightly frosts were occurring (Table 1). Under these conditions, shoot growth is limited and the sink for carbohydrate is small (Bouchart et al., 1998), and acclimation of photosynthesis to elevated [CO₂] would be expected (Stitt and Krapp, 1999). While spring temperatures were also cool (Table 1), daylength and radiation were higher and growth of the T. repens sward was approximately four times greater in the spring than the fall, under both ambient and elevated [CO₂] (M Schneider, personal communication). In the spring mean leaflet size rapidly increased, the extension growth of the petioles was enhanced and flowering was also beginning, so plants were unlikely to be sink-limited, and acclimation of photosynthesis to elevated [CO₂] was not expected.

In conclusion, an instantaneous increase in [CO₂] caused a 57% increase in photosynthetic rate of T. repens (Fig. 1). Despite acclimation of photosynthetic capacity in leaves that developed under elevated [CO₂], the long-term effect of growth at elevated [CO₂] was a 37% increase in photosynthesis. Thus, contrary to the belief that the response of grassland species to elevated [CO₂] will be short-lived, stimulation of photosynthesis in T. repens remained after eight years of exposure to elevated [CO₂].

	Acknowledgement

 
EAA is funded by the Graduate Research for the Environment Fellowship, Global Change Education Program, Department of Energy. This work was supported in part by the US Department of Energy under contract number DE-AC02-98CH10886.

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This Article Abstract FREE Full Text (PDF) All Versions of this Article: 54/393/2769    most recent erg309v1 E-letters: Submit a response Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (10) Request Permissions Disclaimer Google Scholar Articles by Ainsworth, E. A. Articles by Long, S. P. Search for Related Content PubMed PubMed Citation Articles by Ainsworth, E. A. Articles by Long, S. P. Agricola Articles by Ainsworth, E. A. Articles by Long, S. P. Social Bookmarking          What's this?

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