Mary A. Heskel

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity’s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.

Bringing the Kok effect to light: A review on the integration of daytime respiration and net ecosystem exchange

Net ecosystem exchange (NEE) represents the difference between carbon assimilated through photosynthesis, or gross primary productivity (GPP), and carbon released via ecosystem respiration (ER). NEE, measured via eddy covariance and chamber techniques, must be partitioned into these fluxes to accurately describe and understand the carbon dynamics of an ecosystem. GPP and daytime ER may be significantly overestimated if the light inhibition of foliar mitochondrial respiration, or “Kok effect,” is not accurately estimated and further integrated into ecosystem measurements. The light inhibition of respiration, a composite effect of multiple cellular pathways, is reported to cause between 25-100% inhibition of foliar mitochondrial respiration, and for this reason needs to be considered when estimating larger carbon fluxes. Partitioning of respiration between autotrophic and heterotrophic respiration, and applying these scaled respiratory fluxes to the ecosystem-level proves to be difficult, and the integration of light inhibition into single and continuous measures of ecosystem respiration will require new interpretations and analysis of carbon exchange in terrestrial ecosystems.

Evolutionary Change in Continuous Reaction Norms

Understanding the evolution of reaction norms remains a major challenge in ecology and evolution. Investigating evolutionary divergence in reaction norm shapes between populations and closely related species is one approach to providing insights. Here we use a meta-analytic approach to compare divergence in reaction norms of closely related species or populations of animals and plants across types of traits and environments. We quantified mean-standardized differences in overall trait means (Offset) and reaction norm shape (including both Slope and Curvature). These analyses revealed that differences in shape (Slope and Curvature together) were generally greater than differences in Offset. Additionally, differences in Curvature were generally greater than differences in Slope. The type of taxon contrast (species vs. population), trait, organism, and the type and novelty of environments all contributed to the best-fitting models, especially for Offset, Curvature, and the total differences (Total) between reaction norms. Congeneric species had greater differences in reaction norms than populations, and novel environmental conditions increased the differences in reaction norms between populations or species. These results show that evolutionary divergence of curvature is common and should be considered an important aspect of plasticity, together with slope. Biological details about traits and environments, including cryptic variation expressed in novel environmental conditions, may be critical to understanding how reaction norms evolve in novel and rapidly changing environments.

Convergence in the temperature response of leaf respiration across biomes and plant functional types.

Significance A major concern for terrestrial biosphere models is accounting for the temperature response of leaf respiration at regional/global scales. Most biosphere models incorrectly assume that respiration increases exponentially with rising temperature, with profound effects for predicted ecosystem carbon exchange. Based on a study of 231 species in 7 biomes, we find that the rise in respiration with temperature can be generalized across biomes and plant types, with temperature sensitivity declining as leaves warm. This finding indicates universally conserved controls on the temperature sensitivity of leaf metabolism. Accounting for the temperature function markedly lowers simulated respiration rates in cold biomes, which has important consequences for estimates of carbon storage in vegetation, predicted concentrations of atmospheric carbon dioxide, and future surface temperatures. Plant respiration constitutes a massive carbon flux to the atmosphere, and a major control on the evolution of the global carbon cycle. It therefore has the potential to modulate levels of climate change due to the human burning of fossil fuels. Neither current physiological nor terrestrial biosphere models adequately describe its short-term temperature response, and even minor differences in the shape of the response curve can significantly impact estimates of ecosystem carbon release and/or storage. Given this, it is critical to establish whether there are predictable patterns in the shape of the respiration–temperature response curve, and thus in the intrinsic temperature sensitivity of respiration across the globe. Analyzing measurements in a comprehensive database for 231 species spanning 7 biomes, we demonstrate that temperature-dependent increases in leaf respiration do not follow a commonly used exponential function. Instead, we find a decelerating function as leaves warm, reflecting a declining sensitivity to higher temperatures that is remarkably uniform across all biomes and plant functional types. Such convergence in the temperature sensitivity of leaf respiration suggests that there are universally applicable controls on the temperature response of plant energy metabolism, such that a single new function can predict the temperature dependence of leaf respiration for global vegetation. This simple function enables straightforward description of plant respiration in the land-surface components of coupled earth system models. Our cross-biome analyses shows significant implications for such fluxes in cold climates, generally projecting lower values compared with previous estimates.

Seasonality of foliar respiration in two dominant plant species from the Arctic tundra: response to long-term warming and short-term temperature variability

Direct measurements of foliar carbon exchange through the growing season in Arctic species are limited, despite the need for accurate estimates of photosynthesis and respiration to characterise carbon cycling in the tundra. We examined seasonal variation in foliar photosynthesis and respiration (measured at 20°C) in two field-grown tundra species, Betula nana L. and Eriophorum vaginatum L., under ambient and long-term warming (LTW) conditions (+5°C), and the relationship of these fluxes to intraseasonal temperature variability. Species and seasonal timing drove most of the variation in photosynthetic parameters (e.g. gross photosynthesis (Agross)), respiration in the dark (Rdark) and light (Rlight), and foliar nitrogen concentration. LTW did not consistently influence fluxes through the season but reduced respiration in both species. Alongside the flatter respiratory response to measurement temperature in LTW leaves, this provided evidence of thermal acclimation. The inhibition of respiration by light increased by ~40%, with Rlight : Rdark values of ~0.8 at leaf out decreasing to ~0.4 after 8 weeks. Though LTW had no effect on inhibition, the cross-taxa seasonal decline in Rlight : Rdark greatly reduced respiratory carbon loss. Values of Rlight : Agross decreased from ~0.3 in both species to ~0.15 (B. nana) and ~0.05 (E. vaginatum), driven by decreases in respiratory rates, as photosynthetic rates remained stable. The influence of short-term temperature variability did not exhibit predictive trends for leaf gas exchange at a common temperature. These results underscore the influence of temperature on foliar carbon cycling, and the importance of respiration in controlling seasonal carbon exchange.

Differential physiological responses to environmental change promote woody shrub expansion.

Direct and indirect effects of warming are increasingly modifying the carbon-rich vegetation and soils of the Arctic tundra, with important implications for the terrestrial carbon cycle. Understanding the biological and environmental influences on the processes that regulate foliar carbon cycling in tundra species is essential for predicting the future terrestrial carbon balance in this region. To determine the effect of climate change impacts on gas exchange in tundra, we quantified foliar photosynthesis (Anet), respiration in the dark and light (RD and RL, determined using the Kok method), photorespiration (PR), carbon gain efficiency (CGE, the ratio of photosynthetic CO2 uptake to total CO2 exchange of photosynthesis, PR, and respiration), and leaf traits of three dominant species – Betula nana, a woody shrub; Eriophorum vaginatum, a graminoid; and Rubus chamaemorus, a forb – grown under long-term warming and fertilization treatments since 1989 at Toolik Lake, Alaska. Under warming, B. nana exhibited the highest rates of Anet and strongest light inhibition of respiration, increasing CGE nearly 50% compared with leaves grown in ambient conditions, which corresponded to a 52% increase in relative abundance. Gas exchange did not shift under fertilization in B. nana despite increases in leaf N and P and near-complete dominance at the community scale, suggesting a morphological rather than physiological response. Rubus chamaemorus, exhibited minimal shifts in foliar gas exchange, and responded similarly to B. nana under treatment conditions. By contrast, E. vaginatum, did not significantly alter its gas exchange physiology under treatments and exhibited dramatic decreases in relative cover (warming: −19.7%; fertilization: −79.7%; warming with fertilization: −91.1%). Our findings suggest a foliar physiological advantage in the woody shrub B. nana that is further mediated by warming and increased soil nutrient availability, which may facilitate shrub expansion and in turn alter the terrestrial carbon cycle in future tundra environments.

Thermal acclimation of shoot respiration in an Arctic woody plant species subjected to 22 years of warming and altered nutrient supply

Despite concern about the status of carbon (C) in the Arctic tundra, there is currently little information on how plant respiration varies in response to environmental change in this region. We quantified the impact of long-term nitrogen (N) and phosphorus (P) treatments and greenhouse warming on the short-term temperature (T) response and sensitivity of leaf respiration (R), the high-T threshold of R, and associated traits in shoots of the Arctic shrub Betula nana in experimental plots at Toolik Lake, Alaska. Respiration only acclimated to greenhouse warming in plots provided with both N and P (resulting in a ~30% reduction in carbon efflux in shoots measured at 10 and 20 °C), suggesting a nutrient dependence of metabolic adjustment. Neither greenhouse nor N+P treatments impacted on the respiratory sensitivity to T (Q10 ); overall, Q10 values decreased with increasing measuring T, from ~3.0 at 5 °C to ~1.5 at 35 °C. New high-resolution measurements of R across a range of measuring Ts (25-70 °C) yielded insights into the T at which maximal rates of R occurred (Tmax ). Although growth temperature did not affect Tmax , N+P fertilization increased Tmax values ~5 °C, from 53 to 58 °C. N+P fertilized shoots exhibited greater rates of R than nonfertilized shoots, with this effect diminishing under greenhouse warming. Collectively, our results highlight the nutrient dependence of thermal acclimation of leaf R in B. nana, suggesting that the metabolic efficiency allowed via thermal acclimation may be impaired at current levels of soil nutrient availability. This finding has important implications for predicting carbon fluxes in Arctic ecosystems, particularly if soil N and P become more abundant in the future as the tundra warms.

Breaking the cycle: how light, CO2 and O2 affect plant respiration

In 1953, Sir Hans Krebs won the Nobel Prize for his classic work elucidating the metabolic steps by which citrate is metabolized within the mitochondria and drives energy recovery from stored carbohydrates. Through an elegant series of reactions fed from a common substrate, the tricarboxylic acid cycle (TCA) creates carbon compounds of various sizes and configurations to support a multitude of metabolic reactions (Krebs 1936). Contemporaneously, physiologists like Bessel Kok, concentrating on photosynthetic metabolism, suggested an in vivo linkage between photosynthesis and respiration that was sensitive to environmental conditions, particularly light (Kok 1948). Many talented scientists from the fields of molecular biology, biochemistry, physiology, and ecology have continued to examine this linkage and the effect of light on it (Hurry et al. 2005). Significant progress has integrated and advanced our knowledge of the biochemical and physiological controls of respiratory metabolism, and now it is well established that even low levels of light can not only decrease respiratory CO2 release but can also cause the long-studied clockwise Krebs cycle to be decidedly non-cyclical (Fig. 1, ‘light’). On pages 2208–2220 of the December issue, Guillaume Tcherkez et al. (2012) use emerging technologies, developing theories and clever experimental manipulations to further advance our knowledge of the structure, function and control of respiratory metabolism in the light.The result is a clearer understanding of the tricarboxylic acid pathway (TCAP – not cycle!) and specifically the dynamic effects of atmospheric CO2 and O2 on respiratory metabolism. Changes in the atmospheric CO2 and/or O2 partial pressure are likely to influence respiratory metabolism during illumination in a variety of ways, though underlying functional controls of these effects are not yet clear. Elevated CO2 conditions can stimulate carboxylation and can decrease oxygenation of ribulose-1,5-bisphosphate (RuBP) in photosynthesis, altering the energy balance and efficiency of carbon fixation and the rate of triose-phosphate production (Sage, Sharkey & Seemann 1990). Kok’s observation of lower mitochondrial CO2 efflux in the light has often been interpreted as a decreased demand for respiratory products when photosynthesis could more directly supply ATP, reductants and reduced sugars. However, increased rates of carbon fixation in elevated CO2 environments have been shown to vary in their influence on the degree of light inhibition of respiration, with studies reporting decreases (Wang et al. 2001; Shapiro et al. 2004) or little effect (Sage et al. 1990; Ayub et al. 2011; Crous et al. 2012). While acknowledging previous interpretations of mechanistic controls on the light inhibition of respiration, Tcherkez et al. view the complexity of plant metabolism in the light under different gaseous environments as a ‘persisting conundrum’ and tackle this issue using an arsenal of techniques. Key to their work is the development of tools to quantitatively follow the flow of individual carbon atoms among the various pools of the TCAP. Such detailed tracing allows for modelling of the probability and kinetics of individual reactions and provides qualitative links to isotopic fluxomics (Tcherkez et al. 2009). The last decade has seen a strong theoretical advancement in our understanding of mitochondrial metabolism in illuminated photosynthetic cells (Hurry et al. 2005; NunesNesi, Sweetlove & Fernie 2007; Leakey et al. 2009). As light impacts the redox state of cells and organelles, the regulation of various enzyme systems leads the TCAP ‘cycle’ to become decidedly less cyclical, opening the sequence of reactions to provide parallel but linked metabolic pathways (Fig. 1). In the dark, Krebs’ classical clockwise view is maintained, and citrate metabolism fed from glycolysis creates carbon substrates, releases CO2 as various intermediates are oxidized and supplies reductant to drive the formation of ATP by the electron transport chain/oxidative phosphorylation. By contrast, in illuminated photosynthetic cells (right panel), TCAP activity is fed directly from stored citrate, bypassing the incorporation of acetyl-coenzyme A, and is used primarily to drive the formation of glutamine/ glutamate rather than participating in the full cycle. Moreover, triose phosphates from the Calvin cycle can feed the formation of phosphoenolpyruvate, which itself can be carboyxlated, and the resulting oxaloacetate can be then transformed into malate or fumarate in the ‘left-hand’ side of the opened cycle. Using a stable isotope pulse-chase experiment, Tcherkez et al. show that the rate of respiration in the light is unaffected by short-term (hours) manipulations of [CO2] and further conclude that CO2 evolution from the TCAP accounts for only 20% of the total decarboxylations. Correspondence: K. L. Griffin. E-mail: griff@ldeo.columbia.edu Plant, Cell and Environment (2012) doi: 10.1111/pce.12039 bs_bs_banner

Reply to Adams et al.: Empirical versus process-based approaches to modeling temperature responses of leaf respiration

Reply to Adams et al. : Empirical versus process-based approaches to modeling temperature responses of leaf respiration

Small flux, global impact: Integrating the nuances of leaf mitochondrial respiration in estimates of ecosystem carbon exchange

The balance of photosynthesis and respiration, their responses to a changing environment, and predictive models of these responses continue to be an active body of research. While photosynthesis is robustly described by a longstanding, scalable biochemical model (Farquhar et al., 1980), a similar mechanistic model of respiration remains an ongoing challenge. Respiration encompasses multiple cellular processes in the mitochondria and cytosol that drive energy and carbon skeleton production for plant growth and maintenance. Through glycolysis (cytosol), the tricarboyxlic acid (TCA) cycle (mitochondrial matrix), the electron transport chain/oxidative phosphorylation (mitochondrial inner membrane), and other associated pathways, metabolic products of photosynthesis are transformed into energy in the form of ATP, oxygen is consumed, and carbon dioxide is produced. Unlike its metabolic foil, photosynthesis, mitochondrial respiration takes place in all plant tissues, in all cells, at all times. Its ubiquity as an energy source in plants, its role promoting and maintaining efficient photosynthesis, and its contribution to the terrestrial carbon cycle warrant accurate quantification for scaling leaflevel fluxes of carbon. New strategies for measuring and modeling plant respiration across systems and scales are necessary to robustly characterize how carbon flows through terrestrial environments. Developments in measurement techniques, comprehensive fieldbased data sets, and crossscale research collaborations are directly addressing environmental sensitivities and biochemical nuances and, in turn, advancing how respiration is considered at the leaf and ecosystem levels. This essay covers current areas of plant respiration research and their integration into the broader terrestrial carbon cycle.