The world's soils store more carbon than is present in biomass and in the atmosphere. New experimental evidence suggests that the delivery of fresh plant-derived carbon to the subsoil stimulates microbial activity and results in mineralization of thousand-year-old carbon. This supports the recent proposal that the conservation of organic carbon at depth results from a lack of energy for decomposers. This large pool of deep carbon is unlikely to respond to future changes in temperature if no fresh carbon is supplied, limiting the predicted positive feedback between global warming and soil organic carbon decomposition. The results imply that management practices that increase the distribution of fresh carbon along the soil profile (such as deep ploughing and the use of drought-resistant crops with extensive root systems) will stimulate loss of this ancient buried carbon. It is shown that the supply of fresh plant-derived carbon to deep soil layers stimulated the microbial mineralization of carbon that is thousands of years old, and is suggested that a lack of supply of fresh-carbon may prevent the decomposition of the organic carbon pool in deep soil layers in response to future changes in temperature. The world’s soils store more carbon than is present in biomass and in the atmosphere1. Little is known, however, about the factors controlling the stability of soil organic carbon stocks2,3,4 and the response of the soil carbon pool to climate change remains uncertain5,6. We investigated the stability of carbon in deep soil layers in one soil profile by combining physical and chemical characterization of organic carbon, soil incubations and radiocarbon dating. Here we show that the supply of fresh plant-derived carbon to the subsoil (0.6–0.8 m depth) stimulated the microbial mineralization of 2,567 ± 226-year-old carbon. Our results support the previously suggested idea7 that in the absence of fresh organic carbon, an essential source of energy for soil microbes, the stability of organic carbon in deep soil layers is maintained. We propose that a lack of supply of fresh carbon may prevent the decomposition of the organic carbon pool in deep soil layers in response to future changes in temperature. Any change in land use and agricultural practice that increases the distribution of fresh carbon along the soil profile1,8,9 could however stimulate the loss of ancient buried carbon.

Stability of organic carbon in deep soil layers controlled by fresh carbon supply

Understanding the origin of the carbon (C) stabilised in soils is crucial in order to device management practices that will foster Caccumulation in soils. The relative contributions to soilC pools of roots vs. shoots is one aspect that has been mostly overlooked, although it appears a key factor that drives the fate of plant tissueC either as mineralized CO2 or as stabilized soil organic matter (SOM). Available studies on the subject consistently indicate that rootC has a longer residence time in soil than shootC. From the few studies with complete datasets, we estimated that the mean residence time in soils of root-derived C is 2.4times that of shoot-derived C. Our analyses indicate that this value is biased neither by an underestimation of root contributions, as exudation was considered in the analysis, nor by a priming effect of shoot litter on SOM. Here, we discuss the main SOM stabilisation mechanisms with respect to their ability to specifically protect root-derived SOM. Comparing in situ and incubation experiments suggests that the higher chemical recalcitrance of root tissues as compared to that of shoots is responsible for only a small portion, i.e. about one fourth, of the difference in mean residence time in soils of root-derived vs. shoot-derivedC. This suggests that SOM protection mechanisms other than chemical recalcitrance are also enhanced by root activities: (1)physico-chemical protection, especially in deeper horizons, (2)micrometer-scale physical protection through myccorhiza and root-hair activities, and (3)chemical interactions with metal ions. The impact of environmental conditions within deeper soil layers on rootC stabilisation appear difficult to assess, but is likely, if anything, to further increase the ratio between the mean residence time of root vs. shootC in soils. Future advances are expected from isotopic studies conducted at the molecular level, which will help unravel the fate of individual shoot and root compounds, such as cutins and suberins, throughout soil profiles.

Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation

The rhizosphere is a complex environment where roots interact with physical, chemical and biological properties of soil. Structural and functional characteristics of roots contribute to rhizosphere processes and both have significant influence on the capacity of roots to acquire nutrients. Roots also interact extensively with soil microorganisms which further impact on plant nutrition either directly, by influencing nutrient availability and uptake, or indirectly through plant (root) growth promotion. In this paper, features of the rhizosphere that are important for nutrient acquisition from soil are reviewed, with specific emphasis on the characteristics of roots that influence the availability and uptake of phosphorus and nitrogen. The interaction of roots with soil microorganisms, in particular with mycorrhizal fungi and non-symbiotic plant growth promoting rhizobacteria, is also considered in relation to nutrient availability and through the mechanisms that are associated with plant growth promotion.

Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms

Five main biogenic sources of CO2 efflux from soils have been distinguished and described according to their turnover rates and the mean residence time of carbon. They are root respiration, rhizomicrobial respiration, decomposition of plant residues, the priming effect induced by root exudation or by addition of plant residues, and basal respiration by microbial decomposition of soil organic matter (SOM). These sources can be grouped in several combinations to summarize CO2 efflux from the soil including: root-derived CO2, plant-derived CO2, SOM-derived CO2, rhizosphere respiration, heterotrophic microbial respiration (respiration by heterotrophs), and respiration by autotrophs. These distinctions are important because without separation of SOM-derived CO2 from plant-derived CO2, measurements of total soil respiration have very limited value for evaluation of the soil as a source or sink of atmospheric CO2 and for interpreting the sources of CO2 and the fate of carbon within soils and ecosystems. Additionally, the processes linked to the five sources of CO2 efflux from soil have various responses to environmental variables and consequently to global warming. This review describes the basic principles and assumptions of the following methods which allow SOMderived and root-derived CO2 efflux to be separated under laboratory and field conditions: root exclusion techniques, shading and clipping, tree girdling, regression, component integration, excised roots and in situ root respiration; continuous and pulse labeling, 13 C natural abundance and FACE, and radiocarbon dating and bomb- 14 C. A short sections cover the separation of the respiration of autotrophs and that of heterotrophs, i.e. the separation of actual root respiration from microbial respiration, as well as methods allowing the amount of CO2 evolved by decomposition of plant residues and by priming effects to be estimated. All these methods have been evaluated according to their inherent disturbance of the ecosystem and C fluxes, and their versatility under various conditions. The shortfalls of existing approaches and the need for further development and standardization of methods are highlighted. q 2005 Elsevier Ltd. All rights reserved.

Sources of CO2 efflux from soil and review of partitioning methods

▪ Abstract Feedback between plants and the soil is frequently invoked on the basis of evidence of mutual effects. Feedback can operate through pathways involving soil physical properties, chemical and biogeochemical properties and processes, and biological properties, including the community composition of the microbiota and soil fauna. For each pathway, we review the mechanistic basis and assess the evidence that feedback occurs. We suggest that several properties of feedback systems (for example, their complexity, specificity, and strength relative to other ecological factors, as well as the temporal and spatial scales over which they operate) be considered. We find that the evidence of feedback is strongest for plants growing in extreme environments and for plant-mutualist or plant-enemy interactions. We conclude with recommendations for a more critical appraisal of feedback and for new directions of research. Let us not make arbitrary conjectures about the greatest matters. Heraclitus (1)

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Feedback in the plant-soil system

Plant species and soil fertility presumably control rhizosphere effects on soil organic matter (SOM) decomposition, but qualitative and quantitative descriptions of such controls are still sparse. In this study, rhizosphere effects of soybean [Glycine max (L.) Merr.] and spring wheat (Triticum aestivum L.) on SOM decomposition were investigated at four phenological stages under three levels of fertilization in a greenhouse experiment using natural 13 C tracers. The magnitude of the rhizosphere effect ranged from 0% to as high as 383% above the decomposition rate in the no-plant control, indicating that the rhizosphere priming can substantially intensify decomposition. The rhizosphere priming effect was responsible for a major portion of the total soil C efflux. Cumulative soil C loss caused by rhizosphere effects during the whole growing season equated to the amount of root biomass C for the soybean treatment, and 71% of root biomass C for the wheat treatment. Different plant species produced significantly different rhizosphere priming effects. The overall rhizosphere priming effect of soybean plants was significantly higher than for wheat plants. Plant phenology significantly influenced the rhizosphere priming effect. Little rhizosphere effect occurred in both wheat and soybean treatments initially. The priming effect of the wheat rhizosphere reached 287% above the no-plant control at the flowering stage and declined significantly afterward. The priming effect of the soybean rhizosphere peaked at 383% above the no-plant control during the late vegetative stage and remained at high levels onward. Contrary to many published reports, NPK fertilization did not significantly modify the rhizosphere priming effect.

Rhizosphere Effects on Decomposition

Using a natural abundance 13 C method, soil organic matter (SOM) decomposition was studied in a C3 plant – ‘C4 soil’ (C3 plant grown in a soil obtained from a grassland dominated by C4 grasses) system and a C4 plant – ‘C3 soil’ (C4 plant grown in a soil taken from a pasture dominated by C3 grasses) system. In C3 plant – ‘C4 soil’ system, cumulative soil-derived CO2–C were higher in the soils planted with soybean (5499 mg pot −1 ) and sunflower (4484 mg pot −1 ) than that in ‘C4 soil’ control (3237 mg pot −1 ) without plants. In other words, the decomposition of SOM in soils planted with soybean and sunflower were 69.9% and 38.5% faster than ‘C4 soil’ control. In C4 plant – ‘C3 soil’ system, there was an overall negative priming effect of live roots on the decomposition of SOM. The cumulative soil-derived CO2–C were lower in the soils planted with sorghum (2308 mg pot −1 )a nd amaranthus (2413 mg pot −1 ) than that in ‘C3 soil’ control (2541 mg pot −1 ). The decomposition of SOM in soils planted with sorghum and amaranthus were 9.2% and 5.1% slower than ‘C3 soil’ control. Our results also showed that rhizosphere priming effects on SOM decomposition were positive at all developmental stages in C3 plant – ‘C4 soil’ system, but the direction of the rhizosphere priming effect changed at different developmental stages in the C4 plant – ‘C3 soil’ system. Implications of rhizosphere priming effects on SOM decomposition were discussed.

Rhizosphere priming effects on the decomposition of soil organic matter in C4 and C3 grassland soils

Two plant–soil systems, C3 plant - `C4 soil' (obtained from a grassland dominated by C4 grasses) and C4 plant - `C3 soil' (obtained from a pasture dominated by C3 grasses), were used in this study to monitor the dynamics of rhizosphere respiration (root-derived CO2-C) at different plant developmental stages. In C3 plant - `C4 soil' system, CO2-C derived from soybean roots increased significantly from vegetative stage (55.69 mg C d−1 pot−1) to flowering stage (132.18 mg C d−1 pot−1), and it declined thereafter (83.37-111.63 mg C d−1 pot−1). However, no significant change of CO2-C derived from sunflower roots was observed at different plant developmental stages (67.05–77.66 mg C d−1 pot−1). CO2-C derived from soybean (Glycine max (L) Merr) roots was significantly higher than that derived from sunflower (Helianthus annuus) roots except for that at vegetative stage. In C4 plant - `C3 soil' system, CO2-C derived from sorghum roots was significantly higher at flowering stage (169.51 mg C d−1 pot−1) than at other stages (75.89–113.26 mg C d−1 pot−1). CO2-C derived from amaranthus roots was the highest at vegetative stage (88.88 mg C d−1 pot−1) and it declined significantly thereafter (23.42–53.47 mg C d−1 pot−1). CO2-C derived from sorghum (Sorghum bicolor) roots was significantly higher than that from amaranthus (Amaranthus hypochondriacus) roots except for that at vegetative stage. In conclusion, rhizosphere respiration varied not only with plant species but also with plant phenology. With the soil volume used in our pots, the overall percentages of cumulative root-derived CO2-C to total soil respiration were 61.22, 61.14, 81.84 and 67.37% for soybean, sunflower, sorghum and amaranthus, respectively. Specific rhizosphere respiration was also discussed and was used as an index of root activity and vitality.

Rhizosphere respiration varies with plant species and phenology: A greenhouse pot experiment

Summary •T ree root respiration utilizes a major portion of the primary production in forests and is an important process in the global carbon cycle. Because of the lack of ecologically relevant methods, tree root respiration in situ is much less studied compared with above-ground processes such as photosynthesis and leaf respiration. • This study introduces a new 13 C natural tracer method for measuring tree root respiration in situ . The method partitions tree root respiration from soil respiration in buried root chambers. • Rooting media substantially influenced root respiration rates. Measured in three media, the fine root respiration rates of longleaf pine were 0.78, 0.27 and 0.18 mg CO 2 carbon mg − 1 root nitrogen d − 1 at 25 ° C in the native soil, tallgrass prairie soil, and sand‐vermiculite mixture, respectively. Compared with the root excision method, the root respiration rate of longleaf pine measured by the field chamber method was 18% higher when using the native soil as rooting medium, was similar in the prairie soil, but was 42% lower if in the sand‐vermiculite medium. • This natural tracer method allows the use of an appropriate rooting medium and is capable of measuring root respiration nondestructively in natural forest conditions.

Measuring tree root respiration using 13C natural abundance : rooting medium matters

In the present study, ‘natural 13 C tracer method’ was used to partition the belowground respiration into rhizosphere respiration and soil microbial respiration to test the hypothesis that defoliation affects rhizosphere respiration and rhizosphere priming effect on decomposition of soil organic matter (SOM). A C3 plant species, Helianthus annuus (sunflower), was grown in ‘C4’ soil in microcosms so that the CO2 evolved from plant-soil system can be partitioned. Four levels of defoliation intensities were established by manual clipping. CO2 evolved from plant-soil system was trapped during 0–4 h after defoliation (HAD), 5–22 HAD and 23–46 HAD using a closed circulating system, respectively. We found that both rhizosphere respiration and soil microbial respiration of the clipped plants were either unchanged or significantly enhanced compared to unclipped plants at 45% defoliation level during all sampling intervals. Soil microbial respiration increased significantly at all defoliation levels during 0–4 HAD, however, both rhizosphere respiration and soil microbial respiration decreased significantly during 5–22 HAD or 23–46 HAD when 20% or 74 clearly demonstrated that the defoliation treatments modified the rhizosphere priming effect on SOM decomposition. The total cumulative rhizosphere priming effects on SOM decomposition during 0–46 HAD were 146%, 241%, 204% and 205% when 0%, 20%, 45% and <74%.

Defoliation affects rhizosphere respiration and rhizosphere priming effect on decomposition of soil organic matter under a sunflower species: Helianthus annuus

Shenglei Fu

Papers

Rhizosphere Effects on Decomposition

Rhizosphere priming effects on the decomposition of soil organic matter in C4 and C3 grassland soils

Rhizosphere respiration varies with plant species and phenology: A greenhouse pot experiment

Measuring tree root respiration using 13C natural abundance : rooting medium matters

Defoliation affects rhizosphere respiration and rhizosphere priming effect on decomposition of soil organic matter under a sunflower species: Helianthus annuus