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The stimulatory effects of elevated CO2 on plant productivity have been reported for many ecosystems (Ainsworth & Long, 2005), but whether such effects will persist in the face of increasing nutrient limitation is unclear. In nitrogen (N)-limited ecosystems, elevated CO2 has been hypothesized to decrease nutrient availability as the N becomes sequestered in plant and soil pools with slow turnover rates. Alternatively, an elevated CO2 may increase nutrient availability by stimulating N release from soil organic matter (SOM), resulting in positive feedbacks to primary production. Previous reports on the effects of elevated CO2 on N cycling have been variable, with reports of increases, decreases or no change in soil N dynamics under elevated CO2 (Zak et al., 2000). One major source of uncertainty is the degree to which potential changes in root-derived C affect the microbial regulation of soil N availability. In this issue of New Phytologist (pp. 778–786), de Graaf et al. describe a novel approach to examining the effects of elevated CO2 on root-derived inputs of N to soil. Their results support an emerging ‘rhizo-centric’ view, whereby root–microbial interactions may be the central processes in controlling the magnitude and duration of plant productivity responses under elevated CO2.
‘… roots and rhizosphere microbes play a more important role than has been previously considered in mediating soil N availability under elevated CO2.’
By labeling plants with 15N via foliar uptake, de Graaf et al. quantified the magnitude and fate of N from rhizodeposition in wild and cultivated genotypes of wheat and maize exposed to ambient and elevated levels of CO2. Their study reported that rhizodeposition was a strong sink for foliar-applied N in all plants (5–10% of the total uptake from leaves), and that elevated CO2 increased this flux in those plants that also increased in total biomass (e.g. wheat but not maize). Moreover, this study reports that CO2-induced increases in rhizodeposition decreased soil N availability, as greater amounts of root-derived N were immobilized in the rhizosphere of the labeled plants and lesser amounts were taken up by unlabeled, ‘receiver’ plants growing in the same pots.
Increased C fluxes from roots to soil under elevated CO2 have been reported previously but the consequences of such changes for soil N cycling are unclear (Cheng, 1999). de Graaf et al. suggest that greater N immobilization by rhizosphere microbes and decreased N uptake by receiver plants are evidence of enhanced N limitation. However, an alternative interpretation of this is that plants grown under elevated CO2 retain a greater proportion of rhizodeposited N within their rhizosphere. This could be accomplished through CO2-induced increases in rhizosphere microbial biomass as a result of increased root exudation. Such immobilization would not necessarily represent a major loss of N from an individual plant because much of the N would be available for subsequent uptake due to the rapid turnover of the rhizosphere microbial biomass (Paterson, 2003). Furthermore, the loss of root-derived N would likely be minor relative to potential N gains from increased root growth and/or root-induced stimulation of decomposition (Cheng & Kuzyakov, 2005). Both hypotheses are consistent with the data, and suggest that roots and rhizosphere microbes play a more important role than had previously been thought in mediating soil N availability under elevated CO2.
Rhizosphere feedbacks under elevated CO2
Previous conceptual models of plant–microbial interactions under elevated CO2 have focused on bulk soil processes (Fig. 1a). Although such models are appropriate for understanding ecosystem responses in the long term, they do not consider how spatially and temporally dynamic processes occurring in the rhizosphere can influence ecosystem response to elevated CO2. This may explain, in part, why several studies have been unable to account for CO2-induced increases in N in ecosystem budgets (Johnson, 2006). At the Duke Forest free-air carbon dioxide enrichment (FACE) site (North Carolina, USA), the N content of the canopy trees has increased in response to elevated CO2 despite there being no evidence of increased net N mineralization rates in the soil (Finzi et al., 2006). Because net N mineralization is measured in the absence of roots, it is plausible that the unaccounted-for canopy N is derived from enhanced N availability due to rhizosphere processes. A more rhizo-centric view would account for how changes in the intensity of root–microbial interactions under elevated CO2 affect soil N availability and feedbacks to plant productivity (Fig. 1b).
The increased importance of rhizosphere processes under elevated CO2 results from both increased rhizodeposition and changes in rhizosphere N availability. Elevated CO2 can increase rhizosphere C flux through increases in fine root biomass (Norby et al., 1987; Uselman et al., 2000) and/or increases in mass-specific exudation (Phillips et al., 2006). Moreover, elevated CO2 may also induce changes in the chemical composition of exudates (Hodge & Millard, 1998; Phillips et al., 2006). Will such CO2-induced changes in the quantity and chemical quality of exudates influence the microbial processing of soil N? Most root exudates are low molecular weight organic compounds (sugars, amino acids, organic acids) that have traditionally been viewed in light of their effects on P and Fe availability (Marschner, 1995). However, exudates are also the preferred substrates for the rhizosphere microflora (Cheng, 1999), and the rapid assimilation of exudates creates a ‘rhizosphere effect’ around roots where the tight coupling between substrate availability and soil microbial activity is likely to influence soil N availability (Paterson, 2003).
Rhizosphere effects on soil N availability
There are several ways in which roots may increase soil N availability under elevated CO2 (Table 1). First, rhizodeposition may stimulate decomposition through priming effects (Cheng & Kuzyakov, 2005). This has the potential to dramatically increase soil N availability because of the large size of the N pool in SOM. Second, increased C allocation to roots and mycorrhizal fungi under elevated CO2 could increase N availability through increased foraging in soil. Moreover, mycorrhizal fungi (and some plants) may increase N availability through the uptake of organic N (Jones et al., 2005). A third rhizosphere process which may provide a new source of N under elevated CO2 is associative N fixation. Although there have been few reports of increased fixation under elevated CO2, increased rates may occur in the rhizosphere where enhanced substrate availability and low O2 potentials may provide more favorable conditions than in the bulk soil (Dakora & Drake, 2000).
Table 1. Potential rhizosphere effects on soil N availability under elevated CO2
Indicates the magnitude and direction of change (increase +; decrease –) in soil N availability resulting from each process.
Increased SOM decomposition due to priming of rhizosphere microbes
Increased soil exploration, exo-enzyme activity, organic N acquisition
Fine root growth
Increased soil exploration; expansion of rhizosphere extent
Associative N fixation
Increased fixation due to high C availability and low O2 potentials
Grazing of rhizosphere microbes
Increased release of NH4 via the microbial loop
Release of novel compounds
Increased/decreased N due to exudate effects on specific microbial taxa; decreased root competition from allelochemical release
+ or –
Root allocation of metabolites
Increased N immobilization due to higher C : N of root exudates
Increased N loss due to high C availability and low O2 potentials
In addition to accessing new sources of N, rhizosphere processes may accelerate or slow-down N turnover under elevated CO2 (Table 1). The grazing of rhizosphere microflora by soil fauna may accelerate N turnover if increased rhizodeposition stimulates rhizosphere microbes and NH4 release through the microbial loop (Bonkowski, 2004). Second, the production of novel compounds under elevated CO2 could increase or decrease N availability if certain microbial taxa with specific enzymatic capabilities are affected. Finally, CO2-induced increases in the C : N of rhizodeposits may decrease N availability if the roots allocate more C-rich or less N-rich metabolites to root secretions (Paterson, 2003).
Unresolved questions and future research needs
Our present understanding of how rhizosphere processes will affect feedbacks to plant productivity under elevated CO2 is constrained by the lack of appropriate methods. Most studies of CO2 effects on root-derived C have been conducted with small plants growing in an artificial medium (Grayston et al., 1996), and most studies of CO2 effects on N mineralization have been conducted in soil cores from which the roots have been excluded (Zak et al., 2000). Thus, a fundamental challenge in adopting a more rhizo-centric view is that there are few good methods for quantifying rhizosphere processes in intact root–soil systems. This is especially true in the case of root exudation, which has rarely been measured in situ. Such a knowledge gap has limited our understanding of some very basic questions. For example, what are the effects of a root's age, diameter, order or mycorrhizal status on the quantity and chemical quality of exudates? How do abiotic factors such as soil temperature, moisture and fertility affect exudation? Although recent reviews have highlighted our progress in understanding controls on exudation (Jones et al., 2004), more efforts are needed to develop field-based approaches, with the larger goal of integrating the results from field observations with those from highly controlled experimental systems (e.g. growth chambers, FACE sites).
Similarly, relatively few studies have examined the effects of exudate chemistry on soil N transformation rates under rhizosphere-relevant conditions. For example, how much C is needed (and in what chemical form) to stimulate net N mineralization? Does the response depend on the physical, chemical, or biotic properties of the soil? A future research priority should be to develop methods which can better simulate the rhizosphere environment in order to provide a more mechanistic understanding of the fate of root exudates in soil under realistic conditions.
An emerging view in elevated CO2 research is that root–microbial interactions are likely to play an increasingly important role in controlling ecosystem-scale responses to global change. This would argue for a more rhizo-centric view of the interactions between plants and soil microbes, and a better understanding of how roots influence soil N availability. Because today's rhizosphere is yesterday's (and tomorrow's) bulk soil it is critical to integrate rhizosphere mechanisms into models of bulk soil processes in order to better understand the long-term response of ecosystems to global change.