Plant respiration in a changing world

Climate-mediated changes in plant respiration are now accepted as a critical component of the biosphere’s response to global climate change. Each year, whilst producing the energy and carbon intermediates necessary for biosynthesis and cellular maintenance, several times more CO2 is released into the atmosphere by plant respiration than by the burning of fossil fuels (Canadell et al., 2007). Variations in rates of plant respiration (e.g. as a result of climate and/or genotypic differences in energy demand) thus have the potential to affect the functioning of individual plants and ecosystems, and the extent to which atmospheric CO2 will be sequestered by the terrestrial biosphere (King et al., 2006). In recent years, much has been learnt about the importance of plant respiration for ecosystem and Earth-system functioning, the underlying mechanisms responsible for variability in rates of respiration, and the roles played by respiration in helping plants to survive in stressful environments. There has also been growing interest in understanding the extent to which scaling relationships can be used to predict variations in plant respiration (Wright et al., 2006; Reich et al., 2008). However, compared with the relatively comprehensive understanding of photosynthetic metabolism, we lack basic information on key determinants of respiratory rates in photosynthetic and nonphotosynthetic plant organs. Moreover, our ability to predict the scale and magnitude of future rates of respiration remains limited. Dealing with these issues requires a dialogue between researchers working over a wide range of spatial and temporal scales in order to better integrate their combined knowledge and to help reconcile differences in perspectives, approaches and facts. To facilitate this dialogue and to act as a catalyst for future cross-discipline research, the 24th New Phytologist Symposium on ‘Plant respiration and climate change: scaling from mitochondria to the globe’ was held over 3 d at St Hugh’s College, University of Oxford, UK. ‘If we are to predict, more effectively, the effects of climate change on rates of respiration, the international research community needs to formulate a better understanding of the key determinants of respiration in aboveground and belowground organs.’ The symposium brought together, for the first time at an international meeting, biologists and modellers working on respiration at the molecular, cellular, whole-organism and ecosystem/global levels. Over 120 participants from highly diverse backgrounds were attracted to the meeting, with the research interests of participants spanning 16 orders of magnitude (Fig. 1). A total of 25 talks were given over five sessions: Respiratory carbon release over large spatial and temporal scales; Mitochondrial composition and respiratory function; Regulation of respiration in plants and fungal partners; Heterogeneity of respiration in contrasting cell types and tissues; and Respiratory responses to environmental gradients. To facilitate integration, each session comprised talks covering a range of scales and disciplines, and speakers were strongly encouraged to make their talks accessible to the diverse backgrounds of the audience. A feature of the meeting was the opportunity for participants to discuss and debate the issues raised in individual talks. The presentation of over 70 posters and associated discussion periods further extended the opportunity to share ideas. Here, we present some of the emerging and unresolved issues that formed the basis of many lively debates. Elucidating the role of mitochondrial respiration in determining plant responses to climate change, and the role of respiration in determining the scale and magnitude of climate change, requires an integrative dialogue between researchers working over > 16 orders of magnitude, ranging from molecular to global levels. Plant respiration logo courtesy of APPS Lancaster, UK. Despite its central importance to plant, ecosystem and Earth-system functioning, when participants at the 24th New Phytologist Symposium were asked the question: ‘What is respiration?’ there was little consensus in the immediate answers. From a metabolic perspective, several speakers focussed on the catabolic aspects of respiration and the use of respiratory products for biosynthesis and cellular maintenance (e.g. ATP, reducing equivalents and carbon skeletons). Considerable emphasis was placed on understanding specific steps regulating flux through glycolysis, the pentose phosphate pathway, the tricarboxylic acid (TCA) cycle and/or mitochondrial electron transport, with profiling changes of respiratory proteins and metabolites also being common attributes. For others, respiration was viewed largely from the perspective of the ‘CO2 release component’ or the ‘O2 uptake component’, with few attempts to quantify both components simultaneously. Where CO2 and O2 exchange exhibit an asynchronous response (e.g. when light inhibits TCA cycle CO2 release but increases mitochondrial O2 uptake; Hurry et al., 2005), confusion can arise about the direction and magnitude of a reported respiratory response. A further challenge was the extent to which measured rates of CO2 release actually reflect tissue-specific rates of mitochondrial respiration. For example, refixation of respired CO2 by photosynthesis can reduce measured rates of respiratory CO2 release, both in leaves (Loreto et al., 2001; Hurry et al., 2005) and in stems (Teskey et al., 2008). Moreover, Bob Teskey (University of Georgia, USA) showed in his talk that internal movement of respired CO2 away from the cellular source to a remote organ (e.g. transport of root-respired CO2 to stems) could lead to respiration being underestimated at the source, and overestimated in the remote organ. Similarly, the contribution of plants to the release of CO2 by soils was robustly debated (Nina Buchmann, ETH Zurich, Switzerland; Kurt Pregitzer, University of Nevada, USA; Alastair Fitter, University of York, UK), reflecting the complexity of belowground processes controlling overall rates of soil CO2 efflux (including the extent to which plant-derived carbon is respired by mycorrhizal fungi and soil microbes). Finally, there was considerable debate about the carbon sources used by respiration. In many predictive models, an implicit assumption is made that there is a direct coupling between respiration and the use of recently fixed carbon from photosynthesis. However, as reported by Susan Trumbore (Max Planck Institute, Jena, Germany) and others, respiration in leaves, stems and roots often uses a variety of carbon sources, with older pools of stored carbon contributing substantially to respiration in some tissues (particularly roots) (Trumbore, 2006). Collectively, these observations highlight the range of answers that currently exist when challenged with the question: ‘What is respiration?’ Awareness of this lack of consensus and the multitude of ways in which respiration is considered and measured will be essential if our aim of improved communication across discipline boundaries and better integration of respiration research across different scales (Fig. 1) is to be advanced. If we are to predict, more effectively, the effects of climate change on rates of respiration, the international research community needs to formulate a better understanding of the key determinants of respiration in aboveground and belowground organs. There is also a pressing need for a greater degree of understanding of the role of plant mitochondria as ‘metabolic factories’, and their role in helping plants to cope with environmental stress. In both cases, integrating our molecular–biochemical–physiological understanding of mitochondrial responses to their environment is likely to be vital. Achieving this integration, however, remains a major challenge. At the subcellular level, speakers at the meeting outlined several major advances, including the regulatory context of nuclear genes encoding mitochondrial proteins (Jim Whelan, University of Western Australia, Perth, Australia), the analysis of mitochondrial supercomplexes and their role in respiratory function (Hans-Peter Braun, Leibniz Universität, Hannover, Germany), the discovery of regulatory factors controlling rates of glycolysis, the TCA cycle and mitochondrial electron transport (Sandra Oliver, CSIRO, Australia; Guillaume Tcherkez, University Paris-Sud, France; Matthieu Bagard, Université Paris Est Créteil, France; Miquel Ribas-Carbó, Universitat de les Illes Balears, Spain; Jaume Flexas, Universitat de les Illes Balears, Spain; Stephanie Searle, University of Canterbury, New Zealand; Nicolas Taylor, University of Western Australia, Australia), the temporal and spatial heterogeneity of the mitochondrial proteome across plant tissue types (Harvey Millar, University of Western Australia, Australia), regulation of the mitochondrial metabolome (Lee Sweetlove, University of Oxford, UK; Alisdair Fernie, Max Planck Institute, Golm, Germany), taxonomic distribution of the alternative oxidase (Allison McDonald, University of Ontario, Canada) and the importance of mitochondrial metabolism during environmental stress events (David Macherel, Université d’Angers, France; Jaume Flexas, Universitat de les Illes Balears, Spain). At higher scales, speakers also discussed the importance of physiological changes in respiratory metabolism in determining rates of net CO2 exchange at whole-plant and ecosystem levels (Kurt Pregitzer, University of Nevada, USA; Lisa Wingate, University of Cambridge, UK; Margaret Barbour, University of Sydney, Australia; Bob Teskey, University of Georgia, USA). The discussion periods also identified the difficulties in integrating existing and emerging subcellular knowledge with an understanding of the processes taking place at higher scales (whole plant, ecosystem and global). This inability to integrate across scales contrasts with existing modelling of photosynthesis, where development of a mechanistic biochemical framework (Farquhar et al., 1980) subsequently enabled the development of large-scale models that better accounted for climate-dependent variations in photosynthesis (for example in canopy level models (De Pury & Farquhar, 1997) and global vegetation–climate models (Cox et al., 2000; Cox, 2001)). To date, however, no equivalent model has been constructed for plant respiration, partly because of the lack of integrative studies combining knowledge of subcellular processes with whole-tissue physiological responses to climate. Nevertheless, the meeting participants remained confident that we could achieve a more holistic, better-integrated understanding of respiration, so long as there is effective dialogue between researchers working over the spatial scales shown in Fig. 1. One reason for the disjunction across molecular–biochemical–physiological–ecological scales has been the study of diverse natural ecosystems at one end of the spectrum, and the largely restricted application of molecular analysis procedures to model plant species (often grown under artificial, controlled environmental conditions) at the other end of the spectrum. However, with the advent of DNA deep sequencing and other molecular tool advancements, it is increasingly possible to apply many molecular approaches to multiple genotypes of diverse plant species experiencing a wide range of environmental gradients. Moreover, advances in genotyping technology will make whole-genome association mapping of respiratory traits and their environmental responses possible. Opportunities were highlighted for molecular researchers to collaborate with their ecological colleagues at existing field sites to build new, better-integrated data sets from gene expression to ecosystems in natural settings, akin to the work of Andrew Leakey (University of Illinois, USA) on soybean crops in managed free-air CO2 enrichment (FACE) experiments (Leakey et al., 2009). Over the course of the 3-d meeting, two areas emerged as representing road-maps of how a multiscale, process-based understanding of respiration could emerge. The first was the integration of molecular–protein–metabolite–physiology–ecosystem level studies investigating the impacts of sustained changes in growth temperature (i.e. thermal acclimation). Several speakers, including Mark Tjoelker (Texas A&M University, USA) and Peter Reich (University of Minnesota, USA), provided evidence of thermal acclimation in terms of temperature-mediated changes in respiratory flux (O2 uptake and/or CO2 release), with warm-grown plants exhibiting lower rates of plant respiration at a given temperature than their cold-grown counterparts (Atkin & Tjoelker, 2003; Ow et al., 2008). Importantly, physiological observations of acclimation are now being integrated into large-scale models, with important consequences for predicted ecosystem-level CO2 fluxes, both now and in the future. For example, when incorporated into a coupled global climate–vegetation model, accounting for acclimation decreases predicted rates of respiration by 20% in some hot tropical regions (Atkin et al., 2008). The biochemical basis of thermal acclimation is also now better understood, with recent studies highlighting the changes in mitochondrial abundance, protein composition and electron transport rates underpinning the acclimation response (Armstrong et al., 2008). In his talk, Lee Sweetlove (University of Oxford, UK) provided an elegant example of how a combination of experimental and modelling approaches could provide insights into the impacts of acclimation on fluxes through the collection of metabolic pathways that make up the respiratory network. Others provided evidence of a major remodelling of respiratory proteins during the acclimation process (Nicolas Taylor, The University of Western Australia, Australia) and of the contribution of the alternative and cytochrome oxidases to electron transport rates during the acclimation process (Miquel Ribas-Carbó, Universitat de les Illes Balears, Spain; Stephanie Searle, University of Canterbury, New Zealand). Collectively, these talks and recent literature point to a major re-organization of the respiratory system during sustained changes in growth temperature, with important consequences for plant- and ecosystem-level models. The challenge now will be to apply recent advances in the biochemical basis of acclimation to understand why contrasting tissues, species and autotrophic/heterotrophic systems (e.g. soil microbes vs plants) exhibit differing degrees of thermal acclimation in nature, and to assess the adaptive value of thermal acclimation. The second example of integration highlighted in the talks was the recent advancements in our understanding of positional labeling and isotopic discrimination in respiratory metabolism and the use of stable and radioactive isotopes at higher scales (Knohl et al., 2005; Trumbore, 2006; Barbour et al., 2007; Tcherkez et al., 2009). Using data on respiratory discrimination against 13C in leaves, Guillaume Tcherkez (Université Paris-Sud, France) outlined the extent to which leaf respiratory metabolism continues in the light. Subsequently, Margaret Barbour (University of Sydney, Australia) provided an example of how this biochemical understanding can be applied to studies of ecosystem-level CO2 exchange using high-frequency measurements of CO2 concentration and δ13C profiles. In related talks, Lisa Wingate (University of Cambridge, UK) outlined the principles of flux-rate partitioning in forest using data from stable isotope studies conducted at whole-plant and ecosystem scales. A number of talks also described how isotope-labeling experiments can be used to quantify respiratory fluxes at several scales (organ to ecosystem) and to quantify the portion of plant respiration that uses stored and recently fixed photosynthetic products. Using radiocarbon methods, Susan Trumbore (Max Planck Institute, Jena, Germany) provided evidence of respiration in some tissues using carbon substrates fixed from the atmosphere up to several years previously. This finding, if widespread, has important implications for models that currently assume a direct and immediate coupling between photosynthesis and respiration. Many of the talks dealt with fundamental issues of respiratory metabolism over a wide range of scales. Such knowledge is crucial for our understanding of the factors determining current plant growth and performance. However, as Stephen Sitch (University of Leeds, UK) highlighted in his talk on predictive dynamic vegetation and global climate models, such knowledge may be crucial for predicting the scale and magnitude of respiration in a future warmer world and the extent of feedbacks between plant biota and the atmosphere (Sitch et al., 2008). Historically, such models have handled respiration rather crudely, with little or no attempt being made to predict the rates of respiratory CO2 release using process-based approaches or to account for the impact of dynamic responses to factors such as temperature and drought on scaling relationships. In some modelling scenarios, respiration is assumed to represent a constant fraction of photosynthesis, even though we know that the ratio of respiration to photosynthesis often varies (e.g. increasing under drought – Jaume Flexas, Universitat de les Illes Balears, Spain). In other models (e.g. that used by the Hadley Centre; Cox, 2001), rates of respiration at 25°C are linked to variations in tissue nitrogen, with respiration being assumed to be temperature dependent (with a constant Q10 of 2.0 – indicating that no account is made for thermal acclimation). Impacts of drought are also estimated without reference to the consensus emerging from empirical data (Jaume Flexas). Moreover, while the assumption of a strong relationship between respiration (R) and nitrogen (N) is supported by global data sets (Peter Reich, University of Minnesota, USA), variations in R-N scaling often occur (Atkinson et al., 2007;Wright et al., 2006; Atkin et al., 2008). Thus, there is a pressing need for models to move away from reliance on outdated and potentially inaccurate algorithms linking respiration and other plant traits. How should the next generation of dynamic vegetation–climate models better account for spatial and temporal changes in plant respiration? Should efforts be placed on constructing a new process-based model equivalent to that of the Farquhar et al. (1980) biochemical model of photosynthesis? Or should we continue to rely on correlative approaches (e.g. R-N scaling relationships) that better account for the dynamic effects of temperature, light, nutrient availability and drought on respiration? While there was no overwhelming consensus to these questions among meeting participants, all participants agreed that only by strengthening linkages among the different scales shown in Fig. 1 can we more rapidly understand the impacts of climate on respiratory metabolism. We thank Helen Pinfield-Wells and Jill Brooke (New Phytologist Central Office), Joana Zaragoza-Castells, and the staff of St Hugh’s College, University of Oxford, for their expert assistance in organizing and running the 24th New Phytologist Symposium. Also thanks to Rich Norby and Andrew Leakey for their help in running sessions/leading discussions, and to Margaret Barbour, Kevin Griffin and Nicolas Taylor for selecting the best poster awards.

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