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CROP PHYSIOLOGY & METABOLISM

Nitrogen and CO₂ Affect Regrowth and Biomass Partitioning Differently in Forages of Three Functional Groups

^a USDA, ARS Rangeland Resources Research Unit, 1701 Centre Ave., Fort Collins, CO 80526
^b USDA, ARS, Pasture Systems and Watershed Management Research Laboratory, Bldg. 3702 Curtin Road, University Park, PA 16802
^c USDA, ARS, Northern Great Plains Research Laboratory, PO Box 459, Mandan, ND 58554

Corresponding author (morgan{at}lamar.colostate.edu)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Little work has been done to assess the impact of elevated CO₂ on responses of forages to defoliation. This study examines regrowth, biomass partitioning, and labile C and N metabolites in three functional plant-types: a C₃ grass [Pascopyrum smithii (Rydb.) A. Love], a C₄ grass [Bouteloua gracilis (H.B.K.) Lag.], and a forage legume (Medicago sativa L.). Plants were grown from seed, defoliated twice, and grown in a controlled environment under a factorial arrangement of two CO₂ [low CO₂ (LC), 355 µmol mol^-1, and high CO₂ (HC), 700 µmol mol^-1] and two N nutrition regimes [low N (LN), watered twice weekly with half-strength Hoagland's containing 0 N, and high N (HN), half-strength Hoagland's containing 14 mM N]. High N enhanced regrowth in all three species, while high CO₂ enhanced regrowth only in the two C₃ species. In M. sativa, CO₂ and N treatments had no significant effect on k, the allometric growth coefficient. In contrast, k was reduced in P. smithii plants grown under LN (0.63) compared with HN (0.99). In B. gracilis, low N also reduced k, but it interacted with CO₂ so that k was greatest for plants grown at HN/HC (0.95) and HN/LC (0.89), intermediate at LN/LC (0.58), and least at LN/HC (0.44). These results indicate greater partitioning to below-ground organs (reduced k) when N is limiting, particularly under elevated CO₂. Significant correlations were established between k and several measures of plant N status, suggesting that the effects of CO₂ on plant biomass partitioning involve N status.

Abbreviations: C_lab, labile C compounds • DW, dry weight • HC, high CO₂ • HN, high N • k, allometric growth coefficient • LC, low CO₂ • LN, low N • N_lab, labile N compounds • SDW, structural dry weight • TNC, total nonstructural carbohydrates

	INTRODUCTION

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DESPITE THE IMPORTANCE of the effect of grazing pressure on the production and ecology of rangelands and pastures (Harris, 1978; Milchunas and Lauenroth, 1993), only a limited amount of attention has been given to studying how CO₂ enrichment may interact with defoliation. Carbon dioxide enrichment studies with forages have often included defoliation as a component (Bunce, 1995; Campbell and Hart, 1996; Lüscher et al., 1996; Owensby et al., 1999; Schenk et al., 1997), but few have explicitly evaluated how defoliation interacts with CO₂ to effect plant productivity. Growth of frequently (Ryle and Powell, 1992) or periodically (Sæbø and Mortensen, 1995) defoliated white clover (Trifolium repens L.) was significantly enhanced (30–45%) in plants grown at twice ambient CO₂ concentrations, but forage regrowth of several grass species was affected little or reduced (to the point of inhibition in some cases) at elevated CO₂ (Hunt et al., 1995; Sæbø and Mortensen, 1995; Wilsey, 1996). Repeated defoliation decreased CO₂-induced growth enhancements in grasses (Hunt et al., 1995) and in Lolium perenne L. (Hebeisen et al., 1997) under nutrient-limited conditions. However, when nutrients were abundant, positive CO₂-induced growth enhancements were maintained under defoliation. These results indicate the importance of soil nutrients in sustaining CO₂-induced growth responses of forages, especially when subject to defoliation.

The partitioning of biomass between above- and below-ground organs in response to environmental perturbations like CO₂ is another important plant trait that has been studied extensively, but little information exists on how defoliation might interact with CO₂ and affect partitioning. The enhanced plant growth that generally occurs under elevated CO₂ concentrations is often accompanied by shifts in biomass partitioning, often (although not always) with increased partitioning of biomass to belowground organs (Bazzaz, 1990; Rogers et al., 1994, 1996). Several researchers (Campagna and Margolis, 1989; Hunt et al., 1998; Stulen and den Hertog, 1993) have suggested that such CO₂-induced changes in plant biomass partitioning among organs may be best understood through an examination of the effects on labile C and N pools and the functional balance hypothesis. This hypothesis, proposed by Davidson (1969), states that partitioning of biomass among plant organs results from a plant's tendency towards functional balance, a state in which root/shoot activities are adjusted towards maintenance of a stable C/N ratio.

A large body of knowledge exists describing different plant species responses to elevated CO₂, with some progress toward identifying different plant functional groups in terms of their potential responses to CO₂. Plants possessing the C₃ photosynthetic pathway are generally expected to exhibit a greater growth enhancement from CO₂ enrichment since their photosynthetic apparatus is limited more by present ambient CO₂ concentrations compared with C₄ plants (Bowes, 1991). Evidence from numerous studies indicates that this expectation holds (Bazzaz, 1990; Poorter, 1993; Wand et al., 1999), although it can be complicated by other aspects of plant/soil responses to CO₂, as well as interactions of plant CO₂ responses with other environmental parameters (e.g., Hunt et al., 1996, Owensby et al., 1993, 1999). In one of the few studies to evaluate differences among species from different photosynthetic functional groups in how CO₂ enrichment affects regrowth and plant partitioning, Wilsey et al. (1997) observed significant growth enhancements and increased partitioning of plant biomass to storage organs from CO₂ enrichment in growth chamber studies of North American C₃ grasses, but no CO₂ responses in C₃, C₃/C₄ intermediate, and C₄ grasses from Argentina or Tanzania.

Differences in the capability to fix atmospheric N may also determine a species' capacity to respond to atmospheric CO₂ enrichment. Growth of N-fixing species may be more responsive to elevated CO₂ given their additional C sink resulting from N fixation plus the added available N generated; these two factors should increase the capacity and activity of a plant's photosynthetic apparatus, and therefore its capability to respond to CO₂ enrichment. In fact, legumes often do exhibit superior growth response to CO₂ enrichment in N-limited systems compared with associated grasses (Hebeisen et al., 1997; Lüscher et al., 1996; Sæbø and Mortensen, 1995; Schenk et al., 1997), although cool temperature can shift the balance towards cool-season grasses (Campbell and Hart, 1996).

This study evaluates regrowth in three forages of contrasting functional groups, Pascopyrum smithii (C₃ native perennial grass of the Great Plains), Bouteloua gracilis (C₄ perennial grass of the Great Plains) and Medicago sativa (C₃ perennial forage legume) in the 20 d following a defoliation event under two N and CO₂ regimes. We hypothesized that, due to differences in photosynthetic pathway and N-fixing capability, stimulation of regrowth by elevated CO₂ would be greatest in M. sativa and least in B. gracilis, especially under the low N-fertility regime. We also evaluated how CO₂ enrichment affected the partitioning of biomass in defoliated species in relation to the balanced-growth or functional equilibrium concept (Davidson, 1969). Our primary interest was to determine how tissue concentrations of labile C and N metabolites and their relative proportions to each other were affected by different CO₂ and N treatments, and how variability in these labile metabolites related to biomass partitioning in the 10 to 20 d after defoliation. Since elevated CO₂ often leads to reduced tissue N concentrations, we hypothesized that the treatment combination of elevated CO₂ and low soil N availability would likely result in the lowest tissue N concentrations, particularly in the two grass species, and would lead to increased partitioning of biomass to belowground organs.

	MATERIALS AND METHODS

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Plant Culture
Polyvinylchloride cylinders 15-cm diameter by 45 cm deep were filled with a 50:50 mixture of sand and prairie soil [Remit fine sandy loam (Ustollic camborthids)]. Seeds of M. sativa, B. gracilis, and P. smithii were sown in the soil mixture and the columns were placed in a greenhouse for establishment at ambient CO₂ and daytime temperatures of approximately 25°C. After germination, seedlings were thinned to two per column, and N treatments were begun. Columns received biweekly additions of half-strength Hoagland's solution, with half of the columns receiving 0 (LN) and the other half 14 (HN) mM N as NH₄NO₃. As the seedlings grew, columns were irrigated with water as needed to avoid water stress and to flush nutrients through the soil.

Six weeks after emergence, established plants were defoliated with shears to a 5-cm height and columns transferred to an EGC walk-in growth chamber (Environmental Growth Chambers, Inc., Model No. M11, Chagrin Falls, MI, USA)¹ for conditioning to CO₂ regimes. Chambers were maintained at either 355 (ambient or LC) or 700 (elevated or HC) µmol mol^-1 CO₂, a 14-h photoperiod, 28/17°C day/night temperature regime, 700 µmol m^-2 s^-1 photosynthetic photon flux density, and a daytime vapor pressure deficit of 1.7 kPa. The environmental conditions were similar to those observed on the Colorado shortgrass steppe in the summer (Lauenroth and Milchunas, 1991), and were chosen because of the importance of this time of year for cattle grazing. After 3 wk of regrowth in the growth chambers, all plants were defoliated a second time to a 5-cm height. For the grasses, this cutting height removed all mature leaf blades, leaving only sheaths and enclosed elongating laminae. P. smithii is rhizomatous, so in addition to shoot growth arising from the main stem and crowns of the two selected plants, additional shoots were initiated by rhizomes. Any such rhizomatous growth was excised at the soil surface. Any unfolded M. sativa leaves remaining below the 5-cm cutting height were also removed. After this second defoliation, the following biomass and metabolite samples were taken.

Biomass and Metabolites
Sequential harvests made on different columns at 0, 4, 7, 10, 14 and 20 d after cutting were made to analyze how regrowth varied among the three species because of growth under different N and CO₂ regimes. Plants were separated into roots (including rhizomes for P. smithii), crowns, and shoots (regrowth), and lyophilized in a freeze drier. In the grasses, mature sheaths below the 5-cm cutting height were included with crowns, while elongating leaves within sheaths were placed with the regrowth. New emergent tillers were excised at the soil surface and placed with regrowth. The distal 5 cm of each leaf blade that was elongating at the time of cutting was included with the crowns since those tissues were part of the stubble left after clipping. Medicago sativa regrowth included all leaves and stems above a 5-cm height plus all unfolded leaves below that height. Biomass of each organ was analyzed and partitioned into N compounds, nonstructural carbohydrates, and structural biomass [organ dry matter - (nonstructural carbohydrates + labile N compounds)] according to Skinner et al. (1999).

Partitioning Analysis
To examine treatment effects on partitioning of structural biomass between above- and below-ground organs (Troughton, 1956), the allometric growth coefficient (k) was determined for each species according to the following equation:

where S is shoot structural biomass, R is root structural biomass, and b is a constant. If , then relative root and shoot growth are equal. If k < 1, then relative root growth > shoot growth, and when k > 1, then relative root growth < shoot growth. The estimates were obtained from harvests performed 10 to 20 d after defoliation. The first three harvest dates were excluded from analysis because mobilization of labile reserves was active during this period (Skinner et al., 1999); this complicated the analysis of root:shoot partitioning responses, which are better represented by more stable, steady-state conditions. Further, a lack of significant shoot biomass immediately following defoliation compromised our ability to detect accurately labile compounds as well as determine shoot biomass. The allometric growth coefficient k represents the balance between shoot and root relative growth rates, and so provides an estimate of treatment effects on partitioning that is not confounded by ontogenetic attributes like plant size (Coleman et al., 1993; Farrar and Williams, 1991). Calculation of a structural k is presumed to reflect more accurately longer-term partitioning responses, unconfounded by the more short-term build-up of labile C and N compounds in tissues.

We evaluated several measures of whole-plant C and N status and correlated these measures against k to determine how such measures related to the growth coefficient of recently defoliated plants. In particular, we evaluated whole-plant concentrations of total non-structural carbohydrates (TNC), labile N compounds (N_lab), total N, N_lab as a percentage of total plant N, and ratios of various C and N compounds. The N_lab fraction consists mostly of NH₄, NO₃, and free amino acids. The analysis of N_lab, where it is referred to as low molecular weight N compounds, plus the N and TNC analyses are described in Skinner et al. (1999).

Statistics
Since only one growth chamber was available for this study, the experiment was repeated four times, two times at 350 µmol mol^-1 CO₂ and two at 700 µmol mol^-1 CO₂. For each of the four runs, seedlings were established in the greenhouse and procedures followed as previously described before and after transfer to the growth chamber. Within each run, a factorial arrangement of three species, two N concentrations, six harvest dates, plus three subsamples (not counted as replicates) for each factorial combination were randomly arranged within the growth chamber for a total of 108 columns. Therefore, the experiment was analyzed as a split-plot experiment with two replications. The CO₂ treatments which consisted of the four separate runs were treated as the whole plots, and were completely randomized. Because responses varied considerably among the species, separate analyses were conducted for each species. Fishers least significant difference means comparison test was used to test for differences among treatment means when the F test indicated significance (P 0.05). Correlations calculated between the growth coefficient (k) and measures of plant C and N status were performed with treatment means.

	RESULTS AND DISCUSSION

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Regrowth
Medicago sativa shoot regrowth was enhanced by both N and CO₂ (Table 1; N and CO₂ effects). Effects of both CO₂ and N on shoot and whole plant regrowth became greater with time (Table 1; D x C and D x N interactions), so at 20 d both shoot and whole-plant regrowth was greatest in plants grown at high N and high CO₂ (HN/HC), lowest for plants grown at LN/LC, and intermediate for the other two combinations of N and CO₂ (Fig. 1 and 2) . Similar treatment separations were seen in crown and root dry weights (Fig. 3 and 4) . Root and crown regrowth was initially greatest for plants grown under HN/HC, and then appeared to both decrease and then recover sooner than the other treatments in response to defoliation. These responses may have been due in part to mobilization of reserve compounds, as elevated CO₂ increased both the rate and total amounts of TNC for mobilization in M. sativa (Skinner et al., 1999). However, regrowth in completely defoliated plants relies totally on storage compounds for only a few days, and then depends increasingly on metabolites generated from the newly formed photosynthetic surfaces (Richards and Caldwell, 1985). Nodules were apparent on roots of M. sativa at all harvests. Although not measured, the nodules appeared noticeably larger and more abundant under elevated CO₂, indicating that enhanced regrowth may have been due in part to increased N fixation (Zanetti et al., 1996). Stimulation of photosynthesis was also a likely contributor to enhanced growth at elevated CO₂ (Bazzaz, 1990; Bowes, 1991).

View larger version (20K): [in this window] [in a new window]   Fig. 1. Changes in shoot dry weight of M. sativa, P. smithii, and B. gracilis when grown under high/low (H/L) CO2 and N regimes during the 20 d following defoliation. The vertical bars represent ± standard error of the mean

View larger version (23K): [in this window] [in a new window]   Fig. 2. Changes in whole plant dry weights of M. sativa, P. smithii, and B. gracilis when grown under high/low (H/L) CO2 and N regimes during the 20 d following defoliation. The vertical bars represent ± standard error of the mean

View larger version (24K): [in this window] [in a new window]   Fig. 3. Changes in crown dry weight of M. sativa, P. smithii, and B. gracilis when grown under high/low (H/L) CO2 and N regimes during the 20 d following defoliation. The vertical bars represent ± standard error of the mean

View larger version (23K): [in this window] [in a new window]   Fig. 4. Changes in root dry weight of M. sativa, P. smithii, and B. gracilis when grown under high/low (H/L) CO2 and N regimes during the 20 d following defoliation. The vertical bars represent ± standard error of the mean

Similar to results obtained for P. smithii and M. sativa, N treatment significantly enhanced regrowth of B. gracilis (Table 1). Unlike the C₃ species, elevated CO₂ reduced regrowth at HN in this C₄ grass (Fig. 1 and 2, Table 1; D x N x C interaction).

The reduction in regrowth in B. gracilis at elevated CO₂ is curious. Elevating CO₂ above present ambient concentrations is often thought to have little direct effect on the photosynthetic metabolism in C₄ species, although small photosynthetic enhancements have been observed in B. gracilis when when CO₂ concentrations were doubled (LeCain and Morgan, 1998; Morgan et al., 1994). There is little information concerning why regrowth in a C₄ grass should be significantly reduced under CO₂ enrichment. Defoliation may decrease the capability of forages to respond to CO₂ (Hebeisen et al., 1997; Schapendonk et al., 1997). This could result simply from the removal of the photosynthetic surface upon which the CO₂-induced growth response depends. In the case of frequently defoliated plants, formation of smaller tillers may reduce CO₂ responses through a reduction in sink strength (Hebeisen et al., 1997). But it may also be due to lowered respiration under elevated CO₂. Regrowth of defoliated vegetation is initially driven solely by respiration in the mobilization and utilization of reserves. Numerous studies have shown that elevated CO₂ reduces specific respiration rates in plants (Amthor, 1997; Gonzàlez-Meler et al., 1996; Wullschleger et al., 1994). Although there is little information on how elevated CO₂ might affect respiration involved in plant regrowth, reduced respiration may sometimes down-regulate regrowth processes analogous to elevated CO₂ down-regulating photosynthesis. This may have especially important consequences for C₄ species with less potential to respond positively to CO₂ than C₃ species, and may explain why in the present study only B. gracilis exhibited reduced regrowth at elevated CO₂.

Biomass Partitioning
For all species, root:shoot ratio decreased during the regrowth period (Fig. 5 ; calculated with shoots' including crown tissues), a consequence of mobilization of reserves for above-ground growth, and restoration of the photosynthetic tissues. Root:shoot ratios were sometimes greater under the LN regime. In M. sativa, greater root:shoot ratios under LN were detected only in plants grown at LC (P < 0.05). At HC, root:shoot ratios were similar between N treatments, and similar as well to ratios observed in HN/LC plants. Root:shoot ratios were generally greater in B. gracilis grown at LN, but, in contrast, no consistent treatment trends were observed in P. smithii. Thus, the end result of treatment combinations on biomass partitioning was inconsistent, although where root:shoot ratios shifted, it was toward higher ratios under LN treatments, suggesting an increased distribution of biomass to roots in accordance with achieving a functional balance of tissue N.

View larger version (23K): [in this window] [in a new window]   Fig. 5. Root:shoot ratio of M. sativa, P. smithii, and B. gracilis when grown under high/low (H/L) CO2 and N regimes during the 20 d following defoliation. The vertical bars represent ± standard error of the mean

Metabolites and Partitioning
Several measures of whole-plant C and N were analyzed for N and CO₂ treatment effects (Table 3). Concentrations of TNC, as well as the proportion of labile C (C_lab; TNC - storage carbohydrates) to N_lab were almost always greater in each species at HC compared with LC, suggesting that photosynthetic enhancements in all three species grown at elevated CO₂ were sufficient to elevate carbohydrate concentrations. Concentrations of whole-plant N were generally less for plants grown at HC, especially when expressed on a plant dry weight (DW) basis. The effect of CO₂ on N was sometimes less evident when expressed on a structural dry weight (SDW) basis or in terms of N_lab, indicating that part of the CO₂-induced drop in plant N concentration was due to carbohydrate dilution. Concentrations of N appeared greater under LN in M. sativa compared with the two grass species, and the effect of N treatment on whole-plant N concentrations was more evident in the grasses. While no data were collected to indicate whether N fixation was significant enough in these M. sativa plants to affect their response to CO₂, it does seem likely that their N-fixing capacity, although limited in seeding-year plants, may have been an important factor in the different responses observed for the grasses and M. sativa.

Our motivation in evaluating several measures and proportions of labile C and N compounds was that such metabolite pools may be more closely related to partitioning responses than more traditionally and easily measured attributes like total plant tissue N concentration (Campagna and Margolis, 1989; Stulen and den Hertog, 1993). Our results did not fully support this notion. Although strong negative correlations were observed between k and the ratio of sucrose to N_lab, this was the only attribute involving carbon that was significantly related to k. All others were nonsignificant. Several measures of whole-plant N that were unrelated to C or C forms were significantly correlated with k, including the strongest correlation which was established between k and total-plant N expressed on a SDW basis. The lack of any treatment effects on k in the N-fixer, M. sativa, lends indirect support for the importance of N in controlling partitioning. On balance, this experiment confirms the importance of N and N metabolites in plant partitioning responses, but does not provide strong correlative evidence linking C metabolites to partitioning. This lack of evidence does not negate the importance of such C metabolite pools and their proportions in regulating plant biomass partitioning. Proof of links between metabolites measured at one or just a few points in time with growth events that occur over weeks may be difficult to accomplish. While it seems feasible that labile forms of metabolites may regulate plant partitioning responses, a very limited number of whole plant or even organ-level metabolite analyses may be insufficient to reveal more localized metabolite responses that could be involved in regulating organ relative growth responses. Indeed, there is good evidence that source and sink concentrations of sucrose are important in the regulation of plant biomass partitioning (Farrar and Gunn, 1996).

	CONCLUSIONS

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Our results indicate that increasing atmospheric CO₂ concentrations are likely to have important impacts on productivity and biomass partitioning in forage grasses and legumes, and that differential responses among the functional groups will undoubtably affect their performance in the field. Because this study was conducted on first-year growth of perennial forage plants in a growth chamber environment with well-watered plants, some care needs to be exercised in extrapolating these results to the field environment. But some important conclusions that pertain to the field environment can be made. The finding that regrowth and plant biomass partitioning responses to CO₂ were different among the C₃ and C₄ grasses and legume, and in accordance to our hypotheses, lends support to the usefulness of functional groupings as a strategy for understanding and summarizing plant responses to CO₂. The particular results of this study, that C₃ plants demonstrated a positive CO₂-induced regrowth response, whereas regrowth of the C₄ grass was less at elevated CO₂, and that N limitations appeared to have less effect on CO₂ responses of the legume compared with the non-N fixing grasses, indicate important generalities that could be important in the field, but need to be understood in the context of the environment. For instance, we know CO₂ enhancement can stimulate growth of C₄ grasses, especially in water-limited environments because of increased water use efficiency (e.g., Owensby et al., 1999). On the other hand, there are examples of studies in which elevated CO₂ did not elicit growth responses in second- and third-year M. sativa (Bunce, 1995). So the use of functional group knowledge needs to be applied carefully, because of environmental interactions with CO₂, many of which are still poorly understood. Our results also indicate that changes in plant biomass partitioning from CO₂ enrichment may be considered in terms of the balanced growth concept. Strong relationships between various plant N attributes in the grasses and biomass partitioning responses in this study indicate that whole plant measures of plant N will likely be useful for modeling and interpretive applications in situations in which plants are subjected to variable N or elevated CO₂. Finally, because of their capability to fix N, CO₂ enrichment may not be as likely to lead to increased partitioning below-ground in legumes compared with grasses, and productivity may be more responsive to elevated CO₂ compared with grasses, especially in N-limited, semi-arid rangelands where the water relations benefit of elevated CO₂ is likely to be important. Field studies in which legumes can be grown in competition with other species will be needed to confirm this.

	ACKNOWLEDGMENTS

 
We thank Barry Weaver, Dean Ackerman, Dan LeCain, Jennifer Martin, Patience Russell, and Ernie Taylor for technical assistance, and Gary Richardson for statistical advice.

	NOTES

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¹ Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

Received for publication February 4, 2000.

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