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First published online September 15, 2009; 10.1104/pp.109.144113 Plant Physiology 151:1009-1016 (2009) © 2009 American Society of Plant Biologists
Will Elevated Carbon Dioxide Concentration Amplify the Benefits of Nitrogen Fixation in Legumes?1Environmental Sciences Department, Brookhaven National Laboratory, Upton, New York 11973 (A.R.); Department of Plant Biology (E.A.A., A.D.B.L.), Department of Crop Sciences (A.R., E.A.A.), and Institute for Genomic Biology (E.A.A., A.D.B.L.), University of Illinois at Urbana-Champaign, Urbana, Illinois 61801; and Photosynthesis Research Unit, United States Department of Agriculture/Agricultural Research Service, Urbana, Illinois 61801 (E.A.A.)
Growth at elevated [CO2] stimulates photosynthesis and increases carbon (C) supply in all C3 species. A sustained and maximal stimulation in productivity at elevated [CO2] requires an enhanced nutrient supply to match the increase in C acquisition. The ability of legumes to exchange C for nitrogen (N) with their N2-fixing symbionts has led to the hypothesis that legumes will have a competitive advantage over nonleguminous species when grown at elevated [CO2]. On balance, evidence suggests that in managed systems, legumes are more responsive to elevated [CO2] than other plants (e.g. Ainsworth and Long, 2005
The majority of species capable of forming a symbiotic relationship with N2-fixing bacteria belong to the Leguminosae family, and most of the roughly 20,000 legume species form a relationship with nodule-inducing bacteria, collectively known as rhizobia. The seeds of legumes have a high protein content, and some are also rich in oil. Consequently, legumes are an important source of protein and calories for humans and animals, exemplified by the fact that 25 countries plant 20% to 57% of their arable land with legumes such as Bambara groundnuts (Vigna subterranea), peas (Pisum sativum), beans (Phaseolus vulgaris), and lentils (Lens culinaris; http://faostat.fao.org/; Fig. 1 ). These include countries using intensive farming practices that produce mainly soybean (Glycine max), as well as developing countries where smallholder and subsistence farmers grow a wide variety of species that contribute to local food security. In addition, legumes are important components of animal forage in both temperate and tropical zones (Kretschmer and Pitman, 2001  ). In the tropics leguminous trees are used in rotation, or in multispecies cropping systems to enhance soil fertility, and as a source of wood. In all row crop, pasture, and agroforestry systems, the ability of legumes to fix N2 reduces the need for chemical fertilizer inputs and provides important economic and environmental benefits (Peoples et al., 1995). Between one-third and one-half of the total N added to agricultural land is attributable to the legume-rhizobia symbiosis (Herridge et al., 2008; http://faostat.fao.org/). The contribution of legume-rhizobia symbioses to N2-fixation natural ecosystems is hard to estimate, but is important to the composition and function of many terrestrial ecosystems, with woody legumes being particularly abundant in the tropics, while herbaceous legumes are widespread at higher latitudes (Vitousek et al., 2002).
The formation of a root nodule is preceded by an elaborate molecular courtship and the controlled infection of the plant host cell by rhizobia. Within the root nodule, a bacteroid, containing differentiated rhizobia, is isolated from the host cell by a peribacteroid membrane. In addition to forming and maintaining the root nodule, the host provides the bacteroid with a supply of C to fuel N2 fixation. Suc is delivered to the root nodule via the phloem where it is cleaved by Suc synthase, enters glycolysis, and ultimately provides malate to the bacteroid. The bacteroid returns NH4+ to the host cell, which is assimilated into Gln. Further metabolism into other N-containing transport compounds uses C skeletons furnished by the host, and in the case of N-rich ureides, takes place in adjacent uninfected host cells. Both amides (Gln and Asn) and uriedes are exported from the root nodule via the xylem (Fig. 2 ). Within the bacteroid, malate is oxidized by the Krebs cycle to provide reductant for the nitrogenase complex and for the respiratory chain that fuels the nitrogenase complex with ATP. The outer layer of the root nodule forms a diffusive barrier that limits the entry of O2 and protects the highly sensitive nitrogenase complex from O2 inhibition. However, this barrier also limits the supply of O2 to the bacteroid respiratory chain. The presence of high concentrations of leghemoglobin in the host cell, which gives active nodules their characteristic pink color, increases the flux of O2 through the cytoplasm and controls the concentration of free O2 available to the respiratory chain in the peribacteroid membrane (Crawford et al., 2000 ; Fig. 2).
The hypothesis that legumes have an advantage over nonleguminous plants in elevated [CO2] is prevalent in the literature (e.g. Soussana and Hartwig, 1996 ; Zanetti et al., 1996; Serraj et al., 1998; Rogers et al., 2006). This hypothesis is well supported by numerous studies that report greater stimulation of photosynthesis and growth of legume species compared to other functional groups (e.g. Reich et al., 2001; Lee et al., 2003; Ainsworth and Long, 2005). Furthermore, experiments comparing nodulating and nonnodulating genotypes within a legume species have found that N fixers are more responsive to elevated [CO2] than nonfixers (Nakamura et al., 1999; Luscher et al., 2000; Ainsworth et al., 2002, 2004). However, there is also significant variation in the magnitude of the response to elevated [CO2] among legume species and genotypes (Reich et al., 2001; West et al., 2005), and legume aboveground primary production was not statistically greater than that of other functional types when averaged across four Free Air CO2 Enrichment (FACE) experiments (Nowak et al., 2004). A recent meta-analysis suggested that elevated [CO2] will have no effect on N2 fixation in many natural terrestrial ecosystems, which are characterized by intact soils, naturally occurring plant communities, and no fertilizer amendments (van Groenigen et al., 2006).
In C3 plants, elevated [CO2] increases photosynthesis and decreases stomatal conductance. All other effects at the plant and ecosystem level stem from these two primary responses and the secondary effects they elicit (Ainsworth and Rogers, 2007 ). In the absence of other nutrient limitations, legumes will be able to capitalize on the benefits of elevated [CO2] by both increasing N2 fixation and by reducing the negative impact of drought on N2 fixation. In addition, legumes will be able to avoid or limit the few deleterious effects of elevated [CO2] by reducing the potential for sink limitation of C acquisition and limiting the reductions in leaf and grain N content that are typically observed in C3 plants grown at elevated [CO2]. Here, we examine the mechanisms that allow legumes to both capitalize on the benefits, and avoid, or limit, the disadvantages of growth at elevated [CO2].
In fertilized crops and pasture species, the hypothesis that greater photoassimilate availability at elevated CO2 supports stimulated N2 fixation is broadly supported (e.g. Soussana and Hartwig, 1996 ; Zanetti et al., 1996; Ross et al., 2004; Rogers et al., 2006; Fig. 3
). FACE experiments with soybean (Glycine max) and clover (Trifolium repens) showed a stimulation in photosynthetic C uptake and leaf carbohydrate content at elevated [CO2] (Ainsworth et al., 2003b; Rogers et al., 2004; Leakey et al., 2009; Fig. 3). Increases in soybean aboveground biomass were not accompanied by reductions in tissue N content, implying that increased C supply was matched by additional N2 fixation at elevated [CO2] (Morgan et al., 2005; Rogers et al., 2006). An increase in the relative contribution of symbiotically fixed N to total plant N at elevated [CO2] has been reported in a number of experiments (e.g. Schortemeyer et al., 2002; Lee et al., 2003), and in clover, the increased relative contribution of symbiotically fixed N2 at elevated [CO2] was a critical factor in maintaining the C to N ratio in the ecosystem as a whole (Zanetti et al., 1996). These experiments provide ample evidence that legumes increase N2 fixation at elevated [CO2].
An increase in N2 fixation at elevated [CO2] could result from an increase in nodule size, nodule number per plant, or an increase in specific nitrogenase activity, i.e. the amount of N2 fixed per unit nodule and time (Fig. 3). Increased nodule biomass per plant is commonly reported in leguminous trees (e.g. Schortemeyer et al., 2002 ) and herbaceous species (e.g. Lee et al., 2003) grown at elevated [CO2]. Changes in both nodule size and nodule number contribute to increased nodule biomass in different species and studies. On the other hand, there is less evidence that specific nitrogenase activity increases at elevated [CO2] (Cen and Layzell, 2004), perhaps because many legumes lack excess specific nitrogenase capacity (Vance and Heichel, 1991).
In contrast to N2 fixation in fertilized agricultural environments, N2 fixation in natural ecosystems is not consistently stimulated by elevated [CO2] (van Groenigen et al., 2006
These apparent nutrient limitations of N2 fixation at elevated [CO2] may not be specific to legumes or physiologically distinct from nutrient limitation in nonleguminous species. Mo limitation, which is largely confined to acidic soils, may impact N2 fixation directly (Hungate et al., 2004 Therefore, the non-N nutrient limitation of the response of legumes to elevated [CO2] is likely a general nutrient limitation of plant growth that is exacerbated at elevated [CO2] where the availability of C, N, and potentially water is improved, rather than a specific nutrient requirement of legumes grown at elevated [CO2].
Reductions in leaf N content and or increases in C to N ratio are commonly observed in plants grown at elevated [CO2] (Ainsworth and Long, 2005 ). Reduced leaf N content negatively impacts forage quality and can result in additional feeding by protein-limited insects as they attempt to compensate for the reduced leaf N content (Whittaker, 1999). In addition, a lower leaf N content, relative to the enhanced C supply at elevated [CO2], limits the supply of N available for translocation to reproductive tissue during grain fill.
Evidence from mixed semigrassland communities managed as a forage crop showed that leaf N content and C to N ratio were unaffected by growth at elevated [CO2] in legumes, but decreased in nonlegumes (Winkler and Herbst, 2004
Elevated [CO2] will have direct effects on human health and well being through changes in grain quality. Protein content of nonleguminous C3 grains including barley (Hordeum vulgare), wheat (Triticum aestivum), and rice (Oryza sativa) declined by 14% at elevated [CO2] (Taub et al., 2008
The sustained stimulation of C3 photosynthesis by elevated [CO2] increases the availability of carbohydrate and in doing so alters the balance of C and N resources. As a result the plant acclimates, adjusting its photosynthetic, respiratory, and N metabolism to improve performance under elevated [CO2] (Leakey et al., 2009 ). The acclimation of photosynthesis is best understood in the context of the relationship between changes in intercellular [CO2] (ci) and the light-saturated rate of photosynthesis (A), otherwise known as the A-ci curve (Fig. 4
). Differences in the impact of elevated [CO2] on photosynthesis among major plant functional types can explained on the basis of variation in the A-ci relationship (Ainsworth and Rogers, 2007). The distinct effects of elevated [CO2] on leguminous and nonleguminous C3 herbs can be illustrated by comparing the responses of nonleguminous perennial ryegrass (Lolium perenne) and leguminous clover (Fig. 4). Perennial ryegrass grown at elevated [CO2] displayed photosynthetic acclimation with a lower maximum photosynthetic carboxylation capacity (Vc,max) and a lower maximum capacity for electron transport leading to ribulose-1,5-bisP regeneration (Jmax) when compared with plants grown at current [CO2] (Ainsworth et al., 2003a). This results in a less-steep initial slope and lower asymptote on the A-ci curve at elevated [CO2] compared to current [CO2] (Fig. 4A). As a result, leaves measured at an atmospheric [CO2] of 600 µmol mol–1 (corresponding to a ci of approximately 420 µmol mol–1) had lower A if grown at elevated [CO2] (Elev600 in Fig. 4A) compared to plants grown at current [CO2] (Curr600 in Fig. 4A). As a consequence, the stimulation of A at an atmospheric [CO2] of 600 µmol mol–1 relative to 360 µmol mol–1 (corresponding to a ci of approximately 250 µmol mol–1) was less in plants grown at elevated [CO2] compared to plants grown at current [CO2]. In contrast, clover did not photosynthetically acclimate to elevated [CO2], maintaining the same Vc,max and Jmax at current and elevated [CO2] and maximizing the stimulation of A by elevated [CO2] (Fig. 4B; Ainsworth et al., 2003b). Legumes, such as clover, maximize the stimulation of productivity at elevated [CO2] by avoiding photosynthetic acclimation because of their ability to reset the balance of C and N metabolism at elevated [CO2]. Legumes avoid acclimation by allocating some of the additional photosynthate produced at elevated [CO2] to their symbiosis with rhizobia to stimulate N2 fixation. In nonleguminous species where N acquisition cannot be stimulated in this manner, C and N metabolism are balanced by reducing synthesis of Rubisco, which leads to lower Vc,max and A, but also decreases the photosynthetic demand for the limiting nutrient, N, making it available to other sinks (Leakey et al., 2009). These mechanisms maximize the efficiency of resource use for both functional groups, but explain how legumes can gain greater benefit from elevated [CO2] than nonlegumes.
The capacity for legumes to coordinate enhanced assimilation of C and N at elevated [CO2] to avoid down-regulation of photosynthetic capacity and ultimately maximize gains in productivity has been demonstrated across a range of species, environmental conditions, and ecological settings (Ainsworth and Rogers, 2007 ; Leakey et al., 2009). Nevertheless, there are situations where N2 fixation cannot be stimulated in response to greater photosynthate availability at elevated [CO2] because some other factor is limiting. These include the nutrient limitations discussed above, as well as low temperature (Ainsworth et al., 2003b) and potentially drought stress. Unlike the response during warm spring weather (Fig. 4), low temperature was observed to cause photosynthetic acclimation to elevated [CO2] in clover (Ainsworth et al., 2003b). It seems likely that when some environmental factor prevents stimulation of N2 fixation at elevated [CO2], excess photosynthate is likely to accumulate and lead to photosynthetic acclimation, but direct evidence of this mechanism in operation is needed.
Drought is a major limitation to crop production and causes a marked inhibition of N2 fixation in legumes. This is particularly important in arid regions where legumes are also major food crops (Fig. 1). In some species, N2 fixation is especially sensitive to even modest soil drying and reductions in N2 fixation are observed before effects on transpiration or photosynthesis are apparent (Serraj et al., 1999 ). Despite considerable attention, the causes of drought-induced inhibition of N2 fixation are still not well understood. There are a number of mechanisms proposed to account for the reduction in N2 fixation under drought stress: (1) oxygen limitation, (2) C shortage, (3) regulation by N metabolism, and (4) oxidative damage of cellular components in the nodules (Serraj et al., 1999; Galvez et al., 2005; Ladrera et al., 2007; Marino et al., 2007; Naya et al., 2007). A detailed review of these mechanisms is beyond the scope of this Update. However, given that elevated [CO2] has previously been reported to ameliorate drought-induced reductions in N2 fixation through a number of these mechanisms, we consider recent work in this area.
The supply of C to the bacteroid can limit N2 fixation. Plants growing at elevated [CO2] should be able to enhance C supply to the nodule through increased photosynthesis. However, the drought-induced C shortage in the bacteriod occurs downstream of Suc supply. It is correlated with a crash in host cell Suc synthase activity (Fig. 2), an accumulation of Suc, and a decline in malate content (Galvez et al., 2005
Drought-associated decreases in N2 fixation have been linked to increases in ureides, amides, and other amino acids in the leaf and nodule, and there is evidence for both a systemic and local feedback on N2 fixation that is associated with N metabolites (Serraj et al., 1999
Elevated [CO2] perhaps has the most potential to help protect N2 fixation from moderate drought by maintaining higher soil moisture content. There is overwhelming evidence that growth at elevated [CO2] reduces stomatal conductance (gs; Fig. 3), and that this instantaneous response of stomates to CO2 is maintained with time (Leakey et al., 2009
Current evidence suggests there are three key features of the response of legumes to elevated [CO2]: (1) unlike other nonleguminous C3 plants, only legumes have the potential to maximize the benefit of elevated [CO2] by matching stimulated photosynthesis with increased N2 fixation; (2) this potential can only be realized in the absence of limitations on productivity such as nutrient deficiency, low temperature, or drought; (3) rising [CO2] may offer some protection from drought-induced decreases in N2 fixation, which will be become more prevalent with projected changes in precipitation intensity and frequency that are projected to accompany the rise in [CO2]. However, despite the considerable importance of legumes to both agriculture and the function of natural ecosystems, there are still key knowledge gaps. There have been very few long-term studies of the response of field-grown legumes to elevated [CO2]. This greatly limits characterization of the environmental conditions under which N2 fixation can or cannot be stimulated at elevated [CO2]. The feedback effects of nutrient limitation on N2 fixation and photosynthesis have not been quantified. Only a single leguminous food crop (soybean) has been the subject of a fully open-air CO2 enrichment experiment, and this study has not yet reported the effects of elevated [CO2] on N2 fixation. No study we are aware of has quantitatively assessed the flow of C to nodules at current and elevated [CO2]. These and other challenges create the prospect of many new and exciting findings in this subject area.
We thank Joe Nivens for the soybean illustration and Craig Yendrek for comments on an earlier version of the manuscript. Received July 2, 2009; accepted September 2, 2009; published September 15, 2009.
1 This work was supported in part by the U.S. Department of Energy Office of Science (grant no. DE–AC02–98CH10886 to A.R. and Brookhaven National Laboratory). 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Alistair Rogers (arogers{at}bnl.gov). www.plantphysiol.org/cgi/doi/10.1104/pp.109.144113 * Corresponding author; e-mail arogers{at}bnl.gov.
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IMPORTANCE OF LEGUMES
THE SYMBIOSIS
