Root carbon flux: measurements versus mechanisms
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Measurements of the flux of CO2 from biologically active tissues, ground surfaces and landscapes provide a quantitative basis for addressing processes controlling the net movement of carbon (C) between the atmosphere and global land surfaces (Baldocchi et al., 1996; Edwards & Hanson, 1996; Hanson et al., 2000). Net C-flux data from tissues or landscapes are also typically used as the basis for inferring causal mechanisms responsible for the accumulation and reallocation of C within ecosystems under variable environmental conditions. Such processes include the following.
- • The fixation of atmospheric C through photosynthesis.
- • The fate and transport of C compounds within ecosystems.
- • The utilization of C within whole plants.
- • The movement of C from autotrophic sources to its utilization by heterotrophic organisms within soils.
In this issue of New Phytologist, Aubrey & Teskey (pp. 35–40) report new and quantitatively unexpected results suggesting that common assumptions developed from net CO2-flux measurements from both ground and root-tissue measurements may dramatically underestimate the actual metabolic rates of below-ground plant tissues (fine, coarse and structural roots plus associated mycorrhizal fungi). Their results raise a number of questions about C-cycling processes within plants with potentially important implications about how we model C uptake, allocation and respiration in the context of changing environmental conditions.
‘…the data of Aubrey and Teskey might spur discussions regarding long-standing assumptions for relationships between C fluxes observed at the tissue level and the mechanisms responsible.’
Mechanistic implications for plant carbon processes
Aubrey & Teskey’s conclusions suggest that the traditional quantification or conceptualization of total root respiration (i.e. the amount of CO2 diffusing from root tissues into the soil or into a measured humidified air volume) underestimates the actual C metabolism carried out by below-ground plant tissues. This conclusion is mechanistically consistent with previous reports of the redistribution of tissue-respired CO2 by the transpiration stream and the transport of soil-derived CO2 through plants (Ford et al., 2007; Teskey & McGuire, 2007; Teskey et al., 2008). That is, the upward movement of dissolved CO2 in the transpiration stream has come to be expected. However, the magnitude of the internal C movement from below-ground tissues to above-ground plant parts, as calculated by Aubrey & Teskey, is surprisingly large. The magnitude of the flow of C to and from below-ground tissues, suggested by their calculations, raises important questions about our understanding of the transport, allocation and utilization of assimilates in root tissues.
- • Are we routinely underestimating the C needed to sustain below-ground tissues?
- • Will the capacity of phloem transport of assimilates to roots need to be re-evaluated in the context of these new estimates of below-ground tissue metabolism?
- • How do root tissue anatomy and environmental conditions (temperature and moisture) interact to affect CO2 diffusion into and out of roots?
In the context of above-ground plant metabolism, additional interesting research questions are suggested.
- • Where does this CO2 leave the plant (stems, branches, leaves)?
- • If a large fraction of the CO2 passes up the transpiration stream into foliage, does it have a quantitatively significant impact on the amount of CO2 substrate available for gross photosynthesis?
If the answer to the last question is yes, calculations of the commonly described and quantified relationship between assimilation and internal CO2 concentrations supporting the Farquhar photosynthesis model (Farquhar et al., 1980) might need to be reconsidered or modified. New realizations about the magnitude of CO2 sources feeding the photosynthetic process would not affect published photosynthetic relationships for leaves as intact organs, but they could have implications for the energetics of C movement through biochemical pathways.
Personal communications with D. Aubrey during the preparation of this commentary indicated that the authors believed that much of the excess CO2 which moved vertically in the transpiration stream was probably released through plant stems and branches or potentially re-assimilated in photosynthetically active stem tissues before reaching the plant canopy. They acknowledge the potential for a portion of internally transported CO2 to reach the canopy, but the relative proportions of transpiration-stream CO2 released or re-assimilated is as yet unknown.
We do not resolve these questions in the current commentary. We only highlight how the data of Aubrey & Teskey might spur discussions regarding long-standing assumptions for relationships between C fluxes observed at the tissue level and the mechanisms responsible. Aubrey & Teskey’s research will probably spawn similar observations in other plant types across a range of environmental conditions with the purpose of fully characterizing the nature of unexplored C fluxes and metabolic rates of below-ground plant tissues. We look forward to the results of those studies.
Implications for soil or ecosystem carbon flux?
Syntheses of net C-flux data have been employed to summarize daily to annual C gains or losses for important ecosystems (e.g. Curtis et al., 2002; Luyssaert et al., 2007), which in turn serve as the basis for evaluating the functioning of terrestrial ecosystems in the context of Earth’s C cycle through time (e.g. Thornton et al., 2007). Do the conclusions of Aubrey & Teskey undermine these quantitative assessments? The answer is no.
Aubrey & Teskey’s results have important implications for understanding internal plant physiological mechanisms, but they do not lead to the need for a reassessment of ecosystem net C-exchange capacities. Such C budgets are constrained by empirical flux observations normalized to ground areas or tissue area or to mass relationships that would not change with altered understanding of C-utilization mechanisms within plants. Aubrey & Teskey’s findings may, however, have implications for the interpretations of how and why flux rates change from year-to-year or with season of the year.
Better terminology will enhance our understanding of mechanisms
An enhanced and accurate understanding of the true nature of tissue metabolic activity is essential for understanding how plant and soil microorganisms process C and how energy flows through ecological systems. Unfortunately, the understanding of underlying mechanisms is typically based on measurements executed at coarse scales, which probably mask significant internal or unseen complexities. Consideration of the conclusions and observations of Aubrey & Teskey underscores the need for careful evaluation of the use of ‘mechanistic’ terminology to describe what are really only fluxes from target organs, organisms, or ecological surfaces; these fluxes are, in turn, assumed to be dominated by one or more physiological processes. Aubrey & Teskey indirectly make the case for the restricted use of the term ‘root respiration’ for direct measures of root metabolism of C-based substrates into CO2.
A more commonly abused term is ‘soil respiration’. It is fair to conclude that the majority of scientists recognize that soil CO2 efflux results from contributions of CO2 from a complex combination of the activity of autotrophs and a wide variety of heterotrophic organisms, but we nonetheless default to the collective use of the term. Why? Soil respiration is commonly used because it has been convenient to apply to simple and often strong relationships between ground-level effluxes of CO2 and temperature. Gu et al. (2004, 2008) provide clear evidence that a variety of short-term processes confound such empirical relationships, which justifies the general conclusion that it is inappropriate to attribute mechanisms to complex flux processes without adequate justification. Perhaps it is finally time to dispense with the common use of ‘soil respiration’ or tissue and stem respiration in favor of terms better clarifying what we really measure – CO2 efflux from the defined surface or surfaces. Conversely, the term CO2 efflux should be reserved for CO2 exiting the surfaces of interest.
The results of Aubrey & Teskey remind us to stay attentive to new approaches and methods for evaluating commonly held assumptions about the nature and magnitude of physiological processes. In our opinion, their results further imply that the extrapolation of empirical relationships between CO2 flux and environmental drivers embedded within supposedly mechanistic ecosystem models could lead to inappropriate conclusions about the relationship between energy flow and C flux. Climate change response and feedback models are a special case where the use of coarse scale observations and potentially incorrect mechanisms could mislead mitigation and adaptation plans of the future.
We look forward to future published work on plant and ecosystem C-cycle mechanisms, employing new methods with the capacity to resolve processes within boxes that were previously black. We applaud Aubrey & Teskey for pushing the boundaries of measurements for the potential resolution of important mechanisms.