Papers included in the Virtual Special Issue are indicated by their citations set in bold type.
Introduction to a Virtual Special Issue: probing the carbon cycle with 13C
Article first published online: 2 SEP 2009
© The Authors (2009). Journal compilation © New Phytologist (2009)
Volume 184, Issue 1, pages 1–3, October 2009
How to Cite
Norby, R. J. (2009), Introduction to a Virtual Special Issue: probing the carbon cycle with 13C. New Phytologist, 184: 1–3. doi: 10.1111/j.1469-8137.2009.03020.x
- Issue published online: 2 SEP 2009
- Article first published online: 2 SEP 2009
- biotic interactions;
- carbon cycle;
- carbon pools and fluxes;
- global environmental change;
- plant metabolism and biochemistry;
- plant–soil interactions;
- stable isotope of carbon (13C)
The uptake and metabolism of carbon (C) by plants, and its subsequent partitioning to the soil microbial community and the atmosphere, have long been fundamental topics in plant biology and ecological research. Carbon cycling research is especially prominent now as a key component in our efforts to better understand and predict the trajectory and consequences of global environmental change. The stable isotope of C, 13C, has seen increased use as an important tool for understanding and quantifying C pools and fluxes in terrestrial ecosystems. In this Virtual Special Issue, we bring together 20 recent papers from New Phytologist that use 13C to explore plant and ecosystem C cycling. They cover a wide range of biological questions: basic plant metabolism and biochemistry, gaseous exchanges with the atmosphere, and plant–soil and biotic interactions. Together, this collection of papers shows how powerful 13C has become as a research tool, and how creative and sophisticated researchers have become in exploiting its use.
Andrew Benson recounted the exciting history of the rapid discovery of the path of C in photosynthesis when the newly created radioisotope of C, 14C, saw its first use in plant biology in the 1940s (Benson, 2002). Several decades later, 14C was used in investigations of C allocation in trees in forest ecosystems (McLaughlin & McConathy, 1979). However, safety and regulatory concerns have limited the application of 14C, especially in the field environment. Background levels of 14C that resulted from atmospheric testing of nuclear weapons have been very useful in ecological studies (Carbone & Trumbore, 2007), but such analysis is expensive and not widely available. The short-lived radioisotope, 11C, was used in photosynthesis research before 14C became available (Benson, 2002), but it has seen only limited use (Minchin & Thorpe, 2003) because of its very short half-life and the specialized facility its use requires. By contrast, new tools for analysis of 13C (Barbour et al., 2007) have made approaches using the stable C isotope much more widely available to many researchers.
In their Tansley review, Bowling et al. (2008) discuss the implications of systematic variation in the C isotopic composition (δ13C) in ecosystem C pools and fluxes for C cycling studies. They emphasized the importance of understanding the sources of variation related to plant metabolism and environmental influences, and how that variation is critical for interpreting ecosystem processes and the temporal and spatial variability in the isotopic composition of the atmosphere. A detailed systems approach is required to understand the metabolic pathways and fractionation between 12C and 13C that occurs during metabolism (Barbour & Hanson, 2009), and the differences in metabolic pathways between plant organs can help explain the diel and seasonal variation in δ13C measured at the ecosystem scale (Wingate, 2008). Bathellier et al. (2008) investigated the changes in isotopic signature during plant development in different plant organs of Phaseolus vulgaris. They concluded that the differences between organs were related to respiration and respiratory fractionation. In continuing studies with P. vulgaris, Bathellier et al. (2009) concluded that unless the 13C photosynthetic fractionation varies at the leaf level, the root δ13C signal hardly changes under a range of natural environmental conditions. Hence, more detailed understanding of respiratory fractionation is needed to interpret isotopic evidence at larger scales. Gessler et al. (2009) analyzed the 13C content of respired CO2 from leaves, stems and roots of Ricinus communis and related the diel variation in 13C enrichment of respiratory CO2 to intensive phosphoenolpyruvatecarboxylase-catalysed CO2 refixation in stems and roots. Carbone & Trumbore (2007) and Priault et al. (2009) interpreted 13C patterns resulting from labelling or from diurnal variation in metabolism in terms of functional group variation in allocation. Dueck et al. (2007) used a laser-based approach with 13C-labelled plants to show that there is no evidence for substantial aerobic methane emission by terrestrial plants.
Environmental influences on the 13C content of leaves and other organs within and among plant species are related in part to the initial uptake of 13CO2. Diffusion through stomata causes a discrimination against the heavier 13CO2 molecule relative to 12CO2, and the resulting δ13C in leaves can be used to estimate the balance between stomatal conductance and assimilation rate (DaMatta et al., 2008) or mesophyll resistance (Flexas et al., 2007). Sekiya & Yano (2008) explored how environmental variations, specifically the availability of soil phosphorus, water and atmospheric CO2, could affect the relationship between δ13C and stomatal density. They concluded that there was a linear relationship across all examined environments. Cernusak et al. (2007) hoped to identify indicators of differences in transpiration efficiency among tropical tree species. Although variation in transpiration efficiency was correlated with leaf N concentration and 18O enrichment, transpiration efficiency was correlated with δ13C only within a species, not across species. This contrasts with the clear and long-established difference in δ13C between C3 and C4 plants (Bender, 1971). Descolas-Gros & Scholzel (2007) exploited the C3–C4 difference to differentiate modern pollen into C3 and C4 groups based on δ13C, which should be an aid to interpretation of quaternary and older fossil sediments.
The long-term fate of C in ecosystems depends on whether it is stored in living biomass or in soils (Hyvönen et al., 2007), so the processes controlling the partitioning of C to soil must be understood. In a Tansley review on soil microbial processes that mediate soil C balance, Paterson et al. (2009) discuss how quantitative isotope labelling and partitioning methods contribute to our understanding of the C-cycling processes in soil. They discuss many of the techniques that are employed for introducing a 13C label, including pulse labelling, growing C3 plants in soil from a C4 cropping system (Hancock et al., 2007), use of a 13C-depleted CO2 source in free-air CO2 enrichment (FACE) experiments and the addition of 13C-labelled microbial substrates. Högberg et al. (2008) applied a pulse label of 13CO2 to a forest patch and demonstrated the close temporal coupling between tree canopy photosynthesis and a significant fraction of soil activity in forests. Using a tunable diode laser absorption spectrometer for high-resolution monitoring of δ13C in soil respiration, Bahn et al. (2009) similarly demonstrated a tight coupling in the plant–soil system and the importance of plant metabolism for soil CO2 fluxes in a grassland ecosystem. A 13C pulse-labelling experiment with Quercus rubra seedlings subjected to foliar herbivory led Frost & Hunter (2008) to conclude that C exudation from roots was an actively regulated component of below-ground C allocation. At a finer scale, Paterson et al. (2007) employed compound-specific isotope ratio mass spectrometry to show that utilization of 13C-labelled root exudate compounds was an important driver of microbial group abundance in organic soils.
Fine-root turnover is an important source of C flux into soil (Iversen et al., 2008), and fine-root dynamics are an important controller of the efflux of C from soil (Vargas & Allen, 2008). Distinct C isotope signatures (δ13C from 13C-depleted CO2 sources used in FACE experiments and 14C from atmospheric weapons testing) have been used to quantify fine-root turnover (Gaudinski et al., 2001; Matamala et al., 2003), but the estimates often disagree with estimates obtained from minirhizotron observations. Guo et al. (2008) explain this discrepancy through a model based on root branch order. Fungi also contribute to soil respiration, although as discussed by Bostrom et al. (2008), uncertainty about the mechanism causing the difference in 13C enrichment between fungi and plant material continues to constrain the use of stable isotopes in below-ground C-cycling studies. The detailed analysis of δ13C in respired CO2 and sporocarps of different ectomycorrhizal and saprophytic fungal groups in Bostrom et al. (2008) should help to assess hypotheses about the isotopic fractionation that occurs during microbial decomposition of soil organic matter and observations of increasing δ13C with soil depth (Taylor, 2008). Carbon isotopic analysis (13C and 14C) has also been useful for resolving uncertainties in the plant–fungal relationships in orchids (Zimmer et al., 2007, 2008; Cameron et al., 2008) and Pyroleae species (Hynson et al., 2009).
This Virtual Special Issue focuses on the use of 13C, but stable isotopes of other ecologically important elements, particularly deuterium (Keppler et al., 2007), 18O (Gessler et al., 2007) and 15N (Cameron & Seel, 2007; Pons et al., 2007), are also valuable for studying metabolic processes, fluxes and trophic-level interactions in plants and ecosystems. Combined analysis of 13C with other stable isotopes can be especially revealing (Descolas-Gros & Scholzel, 2007; Cernusak et al., 2007; Högberg et al., 2008; Taylor, 2008). As Barbour & Hanson (2009) concluded, ‘The potential for using techniques involving stable isotopes to help understand terrestrial C cycling has been recognized for many years, and it is time for this potential to be realized.’ This collection of papers demonstrates that the potential is indeed coming to reality.
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- 2007. A new measurement technique reveals rapid post-illumination changes in the carbon isotope composition of leaf-respired CO2. Plant Cell and Environment 30: 469–482. , , , , .
- 2008. Divergence in δC13 of dark respired CO2 and bulk organic matter occurs during the transition between heterotrophy and autotrophy in Phaseolus vulgaris plants. New Phytologist 177: 406–418. , , , , , .
- 2009. Metabolic origin of the δC13 of respired CO2 in roots of Phaseolus vulgaris. New Phytologist 181: 387–399. , , , , , .
- 1971. Variations in the 13C/12C ratios of plants in relation to the pathway of carbon dioxide fixation. Phytochemistry 10: 1239–1244. .
- 2002. Following the path of carbon in photosynthesis: a personal story. Photosynthesis Research 73: 29–49. .
- 2008. Can isotopic fractionation during respiration explain the 13C-enriched sporocarps of ectomycorrhizal and saprotrophic fungi? New Phytologist 177: 1012–1019. , , .
- 2008. Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytologist 178: 24–40. , , .
- 2008. Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytologist 180: 176–184. , , , .
- 2007. Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing. New Phytologist 174: 412–419. , .
- 2007. Contribution of new photosynthetic assimilates to respiration by perennial grasses and shrubs: residence times and allocation patterns. New Phytologist 176: 124–135. , .
- 2007. Large variation in whole-plant water-use efficiency among tropical tree species. New Phytologist 173: 294–305. , , , .
- 2008. In field-grown coffee trees source-sink manipulation alters photosynthetic rates, independently of carbon metabolism, via alterations in stomatal function. New Phytologist 178: 348–357. , , , , , , .
- 2007. Stable isotope ratios of carbon and nitrogen in pollen grains in order to characterize plant functional groups and photosynthetic pathway types. New Phytologist 176: 390–401. , .
- 2007. No evidence for substantial aerobic methane emission by terrestrial plants: a 13C--labelling approach. New Phytologist 175: 29–35. , , , , , , , , , et al.
- 2007. Mesophyll conductance to CO2 in Arabidopsis thaliana. New Phytologist 175: 501–511. , , , , , .
- 2008. Herbivore-induced shifts in carbon and nitrogen allocation in red oak seedlings. New Phytologist 178: 835–845. , .
- 2001. The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129: 420–429. , , , , , .
- 2007. Oxygen isotope enrichment of organic matter in Ricinus communis during the diel course and as affected by assimilate transport. New Phytologist 174: 600–613. , , , .
- 2009. On the metabolic origin of the carbon isotope composition of CO2 evolved from darkened light-acclimated leaves in Ricinus communis. New Phytologist 181: 374–386. , , , , , , , .
- 2008. Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytologist 177: 443–456. , , , , , , .
- 2007. Plant growth, biomass partitioning and soil carbon formation in response to altered lignin biosynthesis in Populus tremuloides. New Phytologist 173: 732–742. , , , , , .
- 2008. High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytologist 177: 220–228. , , , , , , , , , et al.
- 2009. Isotopic evidence of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae). New Phytologist 182: 719–726. , , , .
- 2007. The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytologist 173: 463–480. , , , , , , , , , et al.
- 2008. CO2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest. New Phytologist 179: 837–847. , , .
- 2007. Stable hydrogen isotope ratios of lignin methoxyl groups as a paleoclimate proxy and constraint of the geographical origin of wood. New Phytologist 176: 600–609. , , , , , , , , .
- 2003. Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302: 1385–1387. , , , , .
- 1979. Temporal spatial patterns of carbon allocation in the canopy of white oak. Canadian Journal of Botany-Revue Canadienne de Botanique 57: 1407–1413. , .
- 2003. Using the short-lived isotope 11C in mechanistic studies of photosynthate transport. Functional Plant Biology 30: 831–841. , .
- 2007. Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist 173: 600–610. , , , , .
- 2009. Through the eye of the needle: a review of isotope approaches to quantify microbial processes mediating soil carbon balance. New Phytologist 184: 19–33. , , .
- 2007. Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytologist 173: 154–167. , , , .
- 2009. Pronounced differences in diurnal variation of carbon isotope composition of leaf respired CO2 among functional groups. New Phytologist 181: 400–412. , , .
- 2008. Stomatal density of cowpea correlates with carbon isotope discrimination in different phosphorus, water and CO2 environments. New Phytologist 179: 799–807. , .
- 2008. Missing links –δC13 anomalies between substrates and consumers. New Phytologist 177: 845–847. .
- 2008. Environmental controls and the influence of vegetation type, fine roots and rhizomorphs on diel and seasonal variation in soil respiration. New Phytologist 179: 460–471. , .
- 2008. Weighty issues in respiratory metabolism: intriguing carbon isotope signals from roots and leaves. New Phytologist 177: 285–287. .
- 2007. Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytologist 175: 166–175. , , , , , .
- 2008. The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytologist 178: 395–400. , , .