Owen K. Atkin

Thermal acclimation and the dynamic response of plant respiration to temperature

Temperature-mediated changes in plant respiration (R) are now accepted as an important component of the biospheres response to global climate change. Here we discuss the underlying mechanisms responsible for the dynamic response of plant respiration to short and long-term temperature changes. The Q(10) is often assumed to be 2.0 (i.e. R doubles per 10 degrees C rise in temperature); however, the Q(10) is not constant (e.g. it declines near-linearly with increasing temperature). The temperature dependence of Q(10) is linked to shifts in the control exerted by maximum enzyme activity at low temperature and substrate limitations at high temperature. In the long term, acclimation of R to temperature is common, in effect reducing the temperature sensitivity of R to changes in thermal environment, with the temperature during plant development setting the maximal thermal acclimation of R.

Plant phenotypic plasticity in a changing climate

Climate change is altering the availability of resources and the conditions that are crucial to plant performance. One way plants will respond to these changes is through environmentally induced shifts in phenotype (phenotypic plasticity). Understanding plastic responses is crucial for predicting and managing the effects of climate change on native species as well as crop plants. Here, we provide a toolbox with definitions of key theoretical elements and a synthesis of the current understanding of the molecular and genetic mechanisms underlying plasticity relevant to climate change. By bringing ecological, evolutionary, physiological and molecular perspectives together, we hope to provide clear directives for future research and stimulate cross-disciplinary dialogue on the relevance of phenotypic plasticity under climate change.

The hot and the cold: unravelling the variable response of plant respiration to temperature

When predicting the effects of climate change, global carbon circulation models that include a positive feedback effect of climate warming on the carbon cycle often assume that (1) plant respiration increases exponentially with temperature (with a constant Q10) and (2) that there is no acclimation of respiration to long-term changes in temperature. In this review, we show that these two assumptions are incorrect. While Q10 does not respond systematically to elevated atmospheric CO2 concentrations, other factors such as temperature, light, and water availability all have the potential to influence the temperature sensitivity of respiratory CO2 efflux. Roots and leaves can also differ in their Q10 values, as can upper and lower canopy leaves. The consequences of such variable Q10 values need to be fully explored in carbon modelling. Here, we consider the extent of variability in the degree of thermal acclimation of respiration, and discuss in detail the biochemical mechanisms underpinning this variability; the response of respiration to long-term changes in temperature is highly dependent on the effect of temperature on plant development, and on interactive effects of temperature and other abiotic factors (e.g. irradiance, drought and nutrient availability). Rather than acclimating to the daily mean temperature, recent studies suggest that other components of the daily temperature regime can be important (e.g. daily minimum and / or night temperature). In some cases, acclimation may simply reflect a passive response to changes in respiratory substrate availability, whereas in others acclimation may be critical in helping plants grow and survive at contrasting temperatures. We also consider the impact of acclimation on the balance between respiration and photosynthesis; although environmental factors such as water availability can alter the balance between these two processes, the available data suggests that temperature-mediated differences in dark leaf respiration are closely linked to concomitant differences in leaf photosynthesis. We conclude by highlighting the need for a greater process-based understanding of thermal acclimation of respiration if we are to successfully predict future ecosystem CO2 fluxes and potential feedbacks on atmospheric CO2 concentrations.

The crucial role of plant mitochondria in orchestrating drought tolerance

BACKGROUND Around the world, the frequency and intensity of droughts is increasing as a result of global climate change, with important consequences for the growth and survival of agricultural and native plant species. Understanding how plants respond to water stress is thus crucial for predicting the impacts of climate change on the crop productivity and ecosystem functioning. In contrast to the large number of studies assessing drought impacts on photosynthesis, relatively little attention has been devoted to understanding how mitochondrial respiratory metabolism is altered under water stress conditions. SCOPE This review provides an overview of the impacts of water stress on mitochondrial respiration (R), combining studies at the whole-plant, individual organ, cellular and organelle levels. To establish whether there are clear patterns in the response of in vivo R to water stress, a wide range of root, leaf and whole-plant studies are reviewed. It is shown that water stress almost always inhibits R in actively growing roots and whole plants. However, in fully expanded, mature leaves the response is more variable, with water stress reducing R in near two-thirds of reported studies, with most of the remainder showing no change. Only a few studies reported increases in leaf R under severe water stress conditions. The mechanisms responsible for these variable responses are discussed. Importantly, the fact is highlighted that irrespective of whether drought increases or decreases respiration, overall the changes in R are minor compared with the large decreases in photosynthetic carbon gain in response to drought. Based on recent work highlighting the link between chloroplast and mitochondrial functions in leaves, we propose a model by which mitochondrial R enables survival and rapid recovery of productivity under water stress conditions. Finally, the effects of water stress on mitochondrial function, protein abundance and overall metabolism are reviewed.

Interdependence between chloroplasts and mitochondria in the light and the dark

2. Interactions between organelles depends on metabolite exchange . . . . . . . . . . . . . . . . . . . . 236 2.1. ATP exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236 2.2. Transport of reducing equivalents across membranes . . . . . . . . . . . . . . . . . . . . . . . . 237 2.3. Exchange of carbon compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238

Photosynthesis, Carbohydrate Metabolism and Respiration in Leaves of Higher Plants

The relationships between photosynthesis, carbohydrate metabolism and respiration in leaves of C3 plants are reviewed. We first provide an overview of how mitochondrial respiration relies on, and responds to, the supply of photosynthetic products in the light. The pathways by which the various substrates (glycine, oxaloacetate, malate and/or pyruvate) enter the mitochondria and are oxidized, are discussed. We also provide an overview of the pathways of mitochondrial electron transport, with particular attention being paid to the non-phosphorylating alternative oxidase (AOX). We then discuss what is known about leaf respiration rates in light versus darkness (both O2 consumption and CO2 release). The extent to which mitochondrial O2 consumption continues in the light is highly variable, being inhibited, not affected or even stimulated in various reports. On the other hand, non-photorespiratory mitochondrial CO2 release (R) is invariably inhibited by light (5–80% inhibition). R is sensitive to the lowest irradiance values, and is inhibited rapidly. Three methods via which R in the light is measured are outlined and mechanisms via which light might inhibit R are discussed. The effect that light to dark transitions have on respiration are also discussed: we distinguish the initial, photorespiratory post-illumination burst (PIB) from the post-illumination rise in respiration (LEDR, light-enhanced-dark-respiration) which occurs following the PIB. The chapter also considers the demand for mitochondrially-derived ATP for photosynthesis and carbohydrate metabolism and the potential role of respiration during over-reduction of the chloroplast is highlighted. Mitochondrial respiration appears to be critical for the provision of ATP necessary for energy demanding processes in the light. Moreover, there is growing evidence that respiration helps a plant cope with excess photosynthetic redox equivalents, which otherwise can result in photo-oxidative stress.

Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial‐age atmospheric CO2 and growth temperature

Our study assessed the impact of a wide range of industrial-age climate scenarios on leaf respiration (R) in Eucalyptus saligna. Well-watered or sustained drought-treated plants were grown in glasshouses differing in atmospheric CO₂ concentration ([CO₂]) (280, 400 and 640 μl l⁻¹) and temperature (26 and 30°C). Rates of R in darkness (R(dark) ) and light (R(light) ), photosynthesis (A) and related leaf traits (mass : area relationships, and nitrogen, phosphorus, starch and sugar concentrations) were measured. Light inhibited R in all cases (R(light) < R(dark) ) (well-watered: 40%; drought-treated: 73%). Growth [CO₂] and temperature had little impact on area-based rates of R(dark) or R(light) , with R(light) exhibiting minimal thermal acclimation. By contrast, sustained drought resulted in reduced R(dark), R(light) and A, with the inhibitory effect of drought on A and R(light) (c. 50-70%) greater than that on R(dark) (c. 15%). Drought effects were fully reversible after watering. Variability in R(light) appeared to be dependent on the underlying rate of R(dark) and associated Rubisco activity. Collectively, our data suggest that there is an asynchronous response of leaf carbon metabolism to drought, and a tighter coupling between R(light) and A than between R(dark) and A, under both past and future climate scenarios. These findings have important implications for ecosystem/global models seeking to predict carbon cycling.

The art of growing plants for experimental purposes: a practical guide for the plant biologist

Every year thousands of experiments are conducted using plants grown under more-or-less controlled environmental conditions. The aim of many such experiments is to compare the phenotype of different species or genotypes in a specific environment, or to study plant performance under a range of suboptimal conditions. Our paper aims to bring together the minimum knowledge necessary for a plant biologist to set up such experiments and apply the environmental conditions that are appropriate to answer the questions of interest. We first focus on the basic choices that have to be made with regard to the experimental setup (e.g. where are the plants grown; what rooting medium; what pot size). Second, we present practical considerations concerning the number of plants that have to be analysed considering the variability in plant material and the required precision. Third, we discuss eight of the most important environmental factors for plant growth (light quantity, light quality, CO2, nutrients, air humidity, water, temperature and salinity); what critical issues should be taken into account to ensure proper growth conditions in controlled environments and which specific aspects need attention if plants are challenged with a certain a-biotic stress factor. Finally, we propose a simple checklist that could be used for tracking and reporting experimental conditions.

Leaf Respiration in Light and Darkness (A Comparison of Slow- and Fast-Growing Poa Species).

We investigated whether leaf dark respiration (nonphotorespiratory mitochondrial CO2 release) is inhibited by light in several Poa species, and whether differences in light inhibition between the species are related to differences in the rate of leaf net photosynthesis. Four lowland (Poa annua L., Poa compressa L., Poa pratensis L., and Poa trivialis L.), one subalpine (Poa alpina L.), and two alpine (Poa costiniana Vick. and Poa fawcettiae Vick.) Poa species differing in whole plant relative growth rates were grown under identical controlled conditions. Nonphotorespiratory mitochondrial CO2 release in the light (Rd) was estimated according to the Laisk method. Photosynthesis was measured at ambient CO2 partial pressure (35 Pa) and 500 [mu]mol photons m-2 s-1. The rate of photosynthesis per unit leaf mass was positively correlated with the relative growth rate, with the slow-growing alpine Poa species exhibiting the lowest photosynthetic rates. Rates of both Rd and respiration in darkness were also substantially lower in the alpine species. Nonphotorespiratory CO2 release in darkness was higher than Rd in all species. However, despite some variation between the species in the level of light inhibition of respiration, no relationship was observed between the level of inhibition and the rate of photosynthesis. Similarly, the level of inhibition was not correlated with the relative growth rate. Our results support the suggestion that rates of leaf respiration in the light are closely associated with rates in darkness.

Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration

We examined the effect of short- and long-term changes in temperature on gene expression, protein abundance, and the activity of the alternative oxidase and cytochrome oxidase pathways (AOP and COP, respectively) in Arabidopsis thaliana. The AOP was more sensitive to short-term changes in temperature than the COP, with partitioning to the AOP decreasing significantly below a threshold temperature of 20 degrees C. AOP activity was increased in leaves, which had been shifted to the cold for several days, but this response was transient, with AOP activity subsiding (and COP activity increasing) following the development of leaves in the cold. The transient increase in AOP activity in 10-d cold-shifted leaves was not associated with an increase in alternative oxidase (AOX) protein or AOX1a transcript abundance. By contrast, the amount of uncoupling protein was significantly increased in cold-developed leaves. In conjunction with this, transcript levels of the uncoupling protein-encoding gene UCP1 and the external NAD(P)H dehydrogenase-encoding gene NDB2 exhibited sustained increases following growth in the cold. The data suggest a role for each of these alternative non-phosphorylating bypasses of mitochondrial electron transport at different points in time following exposure to cold, with increased AOP activity being important only in the early stages of cold treatment.