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Because fluxes of carbon (C) from soils to the atmosphere represent some of the largest biologically mediated C fluxes on Earth (Giardina et al., 2005), an understanding of the plant mediation of these fluxes has global relevance for the C cycle. For example, a 10% change in global terrestrial soil CO2 efflux could double or completely ameliorate anthropogenic CO2 emissions (Schlesinger & Andrews, 2000). Plants may affect CO2 efflux from soils by mediation of both autotrophic (e.g. root respiration) and heterotrophic (e.g. litter decomposition) processes. Thus, inter- and intra-specific differences in plant function have the potential to significantly influence soil CO2 efflux and global C cycles. Although inter-specific and plant diversity influences on soil CO2 efflux have been widely examined (e.g. Raich & Tufekcioglu, 2000; Johnson et al., 2008; Dias et al., 2010; Metcalfe et al., 2011), intra-specific influences have only been acknowledged recently (see Fischer et al., 2007).
Forest trees have been increasingly recognized as drivers of soil CO2 efflux in terrestrial forest ecosystems (Högberg et al., 2001; Janssens et al., 2001; Dias et al., 2010; Högberg, 2010). Although traditionally, respiration from heterotrophic organisms in soils (primarily microbial respiration) has been emphasized, more recent analyses have suggested that autotrophic activity below ground (primarily plant root respiration) may dominate net soil CO2 efflux from terrestrial forest ecosystems. New techniques have allowed for the quantification of the amount of net soil CO2 efflux that can be attributable to both sources, and direct autotrophic respiration may account for as much as 40–60% of net soil CO2 efflux (Högberg et al., 2001; Janssens et al., 2001; Bond-Lamberty et al., 2004; Högberg, 2010). Autotrophic organisms further influence soil CO2 efflux indirectly through afterlife effects of rhizospheric exudates (Kuzyakov, 2002), rhizospheric priming effects on soil C (Bader & Cheng, 2007; Cheng, 2009), controls on root and leaf turnover, and decomposition (Bowden et al., 1993; Metcalfe et al., 2011). Regardless of heterotrophic vs autotrophic CO2 sources, plant species can influence substantially bulk C transfer rates to the atmosphere, a phenomenon with clear linkages to global climate change and global C budgets (Schlesinger & Andrews, 2000; Giardina et al., 2005).
Both autotrophic and heterotrophic CO2 efflux from soils are probably sensitive to plant genetic variation, which can affect the quantity and quality of plant organic matter (e.g. Lojewski et al., 2009), exudates (Phillips et al., 2003) and litter (Schweitzer et al., 2004; LeRoy et al., 2007). Understanding the genetic basis to CO2 flux is important because genetic sources of variation are generally not included in ecosystem C flux models, genetic variation implies that selection processes could affect ecosystem C flux and this knowledge may assist our understanding of how plant breeding can interact with ecosystem C cycles. Nevertheless, our understanding of plant genetic influences on net soil CO2 efflux in natural systems is limited (see Fischer et al., 2007). Few studies have attempted to quantify the effect of genetic variation in a common tree on belowground C fluxes in forested ecosystems (but see Rae et al., 2004, 2007). Well-understood genetic-based patterns in aboveground productivity should be expressed below ground when belowground growth is coupled to aboveground growth, particularly as net soil CO2 efflux can be driven so strongly by autotrophic sources (Högberg, 2010). For example, more productive genotypes probably have higher soil CO2 efflux beneath their canopies.
One model system for the investigation of plant genetic effects on soil C flux is Populus in the Intermountain West, USA (Whitham et al., 2012). Fischer et al. (2006) showed a relationship between genetic molecular markers and fine root production of Populus fremontii, P. angustifolia and their natural hybrids in a common garden of mature trees. Similarly, Fischer et al. (2007) found that natural riparian forest stands dominated by P. fremontii, P. angustifolia and their hybrids along the Weber River, Utah, differed in fine root production, soil CO2 efflux and belowground C allocation. Because the flux differences were detected along a hybridization gradient, genetic-based differences among tree genotypes were implicated as a major causal agent (Fischer et al., 2007). Further, Lojewski et al. (2009) found that tree molecular composition predicted aboveground productivity of trees consistently in natural stands and in four common gardens. The additional heterotrophic contributions to net soil CO2 efflux are also important, and these fluxes may be related indirectly to tree genetics (e.g. via afterlife effects; Whitham et al., 2012). For instance, Schweitzer et al. (2008, 2012) found that soil microbial community structure in the same stands was predictable by genotype. Similarly, Madritch & Hunter (2002, 2003) and Madritch et al. (2006) found genetic-based patterns in leaf decomposition and bulk soil respiration in Quercus spp. (oaks) and Populus tremuloides (aspen) that was attributed to tree genetic identity and diversity. Recent research has also investigated the molecular basis of biomass allocation in Populus, Pinus and Eucalyptus spp. (Li et al., 1991; Retzlaff et al., 2001; Ngugi et al., 2003; Rae et al., 2004, 2007; Wu et al., 2004; Wullschleger et al., 2005). For example, Wullschleger et al. (2005) identified 31 quantitative trait loci (QTLs) associated with whole-tree biomass C allocation in synthetically crossed juvenile Populus trees. Although this work collectively represents advances in the understanding of root mass pools (Wullschleger et al., 2005) and tree–soil–microbial linkages, this work has not been extended to an understanding of integrated annual belowground tree C fluxes in natural systems.
Here, we build on previous studies in the wild (Fischer et al., 2007), utilizing a common garden environment to explore the genetic-based variation and molecular predictability of belowground C flux among two riparian tree species (Populus spp.) and their natural hybrids (collectively referred to as cross types). We hypothesized that, in a common garden, belowground C flux under tree canopies would differ in a manner that would be predictable on the basis of tree molecular variation. We also predicted that our findings would be consistent with patterns identified in the wild (Fischer et al., 2007). Specifically, we hypothesized: higher soil CO2 efflux in the lowland species P. fremontii relative to P. angustifolia and their hybrids; that soil CO2 efflux would vary among genotypes within each species and hybrid cross type; and that across the hybridization gradient, more genetically similar trees would have similar C fluxes than genetically dissimilar trees.
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Our data suggest that genetic differences at the cross type level across a hybridizing complex can have large effects on belowground ecosystem C flux. Although patterns in net soil CO2 efflux represent patterns attributable to both autotrophic and heterotrophic respiration, patterns in our index of TBCAsingle-tree may be the result of belowground C flux in the form of root growth, root respiration and complex rhizosphere fluxes (including mycorrhizae). For both soil CO2 efflux and TBCAsingle-tree, our findings broadly support predictable genetic-based patterns in belowground C fluxes previously found in natural Populus stands (Fischer et al., 2007). Soil CO2 efflux and belowground C allocation were higher in low-elevation P. fremontii, but high-elevation P. angustifolia exhibited much higher fluxes proportional to aboveground productivity. This pattern in proportional allocation below ground was similar to patterns in fine root production described in the same system (Fischer et al., 2006, 2007). Because our data were generated from within a common garden environment, they suggest that patterns in the wild (Fischer et al., 2007) are reflective of genetic-based mechanisms that are stable in a common environment (sensuLojewski et al., 2009). Our Mantel analyses also suggest that C flux below ground can be predicted on the basis of molecular similarities in trees. These similarities were most easily detected with the genetic differences between species, but significant and weaker effects were found among genotypes within hybrid cross types. Overall, genetic predictability of soil C fluxes was measurable, with soils under trees with a similar molecular composition (across all cross types) displaying similarity in C exchange with the atmosphere.
Our data for soil CO2 efflux demonstrate high and variable rates of soil CO2 efflux in our system. For example, the variation in average soil CO2 efflux in our study, ranging from c. 900 to 1400 g m−2 yr−1, is roughly equivalent to differences between soil CO2 efflux in northern temperate vs tropical systems in a recent review (Davidson et al., 2002). The high values in our study are reflective of the high productivity in these riparian systems characterized by fast growth in riparian trees. The magnitude of the differences highlights that differences in soil CO2 efflux based on plant overstory genetics are not only detectable, but may also be large.
Recent work in other natural ecosystems has similarly demonstrated patterns in leaf decomposition and CO2 fluxes that suggest that tree genetic-based regulation of soil C flux may be widespread. Madritch & Hunter (2002, 2003) found differences in leaf decomposition and soil CO2 efflux that were predictable on the basis of oak leaf phenotype from mixed Quercus spp. (oak) forest stands in Georgia, USA. Intra-generic differences in Quercus spp. fine root morphology and longevity in soils (Espeleta et al., 2009) may also be related to differences in soil CO2 efflux at the intra-generic scale. Similarly, Madritch et al. (2006) demonstrated differences in leaf decomposition and C release to soils which were consistent with P. tremuloides (quaking aspen) genotype identities in natural clonal stands in Wisconsin, USA. Finally, genetic-based differences in C flux have also been found in sea grass-dominated systems (Hughes et al., 2008, 2009; Tomas et al., 2011) and in herbaceous angiosperms (Crutsinger et al., 2006, 2009).
Predictable variation in aboveground C flux occurs in the Populus forests studied across a range of common gardens at different elevations and microclimates (Lojewski et al., 2009). If soil CO2 efflux patterns are autotrophically driven, higher soil CO2 efflux could be the result of higher aboveground productivity (i.e. larger trees respire more below ground; Lojewski et al., 2009), or the cause of aboveground differences in productivity when some genotypes exhibit more advantageous rooting below ground (also see Fischer et al., 2006). Although our study cannot immediately distinguish between this potential cause or effect relationship, our work highlights the need for future studies spanning multiple common gardens, and integrating above- and belowground C flux patterns. Interestingly, our data suggest a switch in which, despite higher overall net soil CO2 efflux and TBCAsingle-tree in two cross types, these same cross types are lowest in TBCAsingle-tree proportional to aboveground productivity. This finding is consistent with potential indirect mechanisms, such as feedbacks on C allocation associated with foliar tannin effects on soils (Fischer et al., 2006, 2007; Pregitzer et al., 2010; Smith et al., 2012). For example, foliar tannin-induced decreases in nutrient availability (Rice & Pancholy, 1973; Northup et al., 1995; Hättenschwiler & Vitousek, 2000; Schweitzer et al., 2004) may result in higher belowground investment in trees, as shown in Fig. 2(c), where P. angustifolia and backcross types (known to be higher in foliar tannins compared with other cross types; Schweitzer et al., 2004) demonstrate higher proportional belowground C allocation. These mechanisms may warrant future research, especially based on the extensive previous research on this topic in cottonwood forests (see Schweitzer et al., 2004; Fischer et al., 2006, 2007; Lojewski et al., 2009).
It is important to highlight that our results for net soil CO2 efflux reflect the influence of both autotrophic and heterotrophic CO2 release. Although our study cannot directly disentangle autotrophic and heterotrophic soil CO2, future studies on plant genetic effects should address differences in these CO2 sources. Previous work has demonstrated that genetic differences in secondary plant chemicals within and among Populus cross types predict microbial soil communities (Schweitzer et al., 2008, 2012), with implications for heterotrophic soil CO2 efflux. Autotrophic and heterotrophic CO2 releases from soils have dramatically different implications for global C cycles. Because heterotrophic C is largely the result of the decomposition of C in soil and detritus pools, high heterotrophic C release may decrease soil C storage, whereas autotrophic C efflux below ground may represent the flux of recently fixed photosynthate associated with respiration (Högberg, 2010). Our findings suggest the possibility for re-enforcing patterns in heterotrophic and autotrophic belowground CO2 efflux, and emphasize that genetic differences among trees can play a large role in determining bulk CO2 transfer to the atmosphere from soils via multiple pathways.
A growing body of work demonstrating the genetic regulation of C pools (Retzlaff et al., 2001; Ngugi et al., 2003; Wu et al., 2004; Wullschleger et al., 2005) has led to interest in the use of woody species for the sequestration of C in terrestrial ecosystems (Jansson et al., 2010). Our data here suggest that soil C fluxes in natural systems are already sensitive to genetic variation, at least at the cross type scale. In our study, variation in soil CO2 fluxes appears to be consistent with belowground C allocation, and is predictable on the basis of the molecular composition of genotypes. Future work may help to untangle how these genetic-based patterns are related to potential genetic-based differences in soil C storage.