Temperature Response of Isoprene Emission in Vivo Reflects a Combined Effect of Substrate Limitations and Isoprene Synthase Activity: A Kinetic Analysis

Abstract

The responses of isoprene emission rate to temperature are characterized by complex time-dependent behaviors that are currently not entirely understood. To gain insight into the temperature dependencies of isoprene emission, we studied steadystate and transient responses of isoprene emission from hybrid aspen (Populus tremula 3 Populus tremuloides) leaves using a fast-response gas-exchange system coupled to a proton-transfer reaction mass spectrometer. A method based on postillumination isoprene release after rapid temperature transients was developed to determine the rate constant of isoprene synthase (IspS), the pool size of its substrate dimethylallyldiphosphate (DMADP), and to separate the component processes of the temperature dependence of isoprene emission. Temperature transients indicated that over the temperature range 25°C to 45°C, IspS was thermally stable and operated in the linear range of its substrate DMADP concentration. The in vivo rate constant of IspS obeyed the Arrhenius law, with an activation energy of 42.8 kJ mol 21 . In contrast, steady-state isoprene emission had a significantly lower temperature optimum than IspS and higher activation energy. The reversible temperature-dependent decrease in the rate of isoprene emission between 35°C and 44°C was caused by decreases in DMADP concentration, possibly reflecting reduced pools of energetic metabolites generated in photosynthesis, particularly of ATP. Strong control of isoprene temperature responses by the DMADP pool implies that transient temperature responses under fluctuating conditions in the field are driven by initial DMADP pool size as well as temperature-dependent modifications in DMADP pool size during temperature transients. These results have important implications for the development of process-based models of isoprene emission.

Facing the Future: Effects of Short-Term Climate Extremes on Isoprene-Emitting and Nonemitting Poplar

“…S4) during HDSs were higher than at the leaf level (30°C, leaf temperature). As temperature is the main driver of ISOPRENE SYNTHASE (ISPS) enzyme activity, the strong increase in the isoprene emission during HDSs is probably a combined function of enhanced ISPS activity and higher substrate availability (Rasulov et al, 2010). Drought can also promote isoprene emission, albeit with a concomitant decrease in photosynthesis Tattini et al, 2014), probably as a result of decreased c i (Table I).…”

“…In terms of C and energy, isoprene biosynthesis is a costly investment for the plant Ghirardo et al, 2011) and is biochemically Rasulov et al, 2010;Way et al, 2011;Monson et al, 2012) and transcriptionally (Mayrhofer et al, 2005;Wiberley et al, 2009) under the control of environmental factors such as light, temperature, and [CO 2 ]. Isoprene synthesis is light dependent (Loreto and Sharkey, 1993); however, emissions can become uncoupled from photosynthesis under stress that impairs net CO 2 assimilation (A) and makes plants rely on alternative (old) C sources (Affek and Yakir, 2003;Brilli et al, 2007;Ghirardo et al, 2011;Trowbridge et al, 2012).…”

Estimations of isoprenoid emission capacity from enclosure studies: measurements, data processing, quality and standardized measurement protocols

“…Although smaller well-mixed chambers generally reach a steady-state rapidly, within seconds to minutes (Rasulov et al, 2010 for the use of an ultra-fast system in isoprene measurements), care needs to be taken to allow the leaf BVOC concentrations and physiological status to equilibrate with chamber conditions after leaf enclosure. This is needed as mono-and sesquiterpenes can be non-specifically stored within the leaves and leaf surface after synthesis (Niinemets et al, 2010c;Niinemets and Reichstein, 2002).…”

Bisphosphonate Inhibitors Reveal a Large Elasticity of Plastidic Isoprenoid Synthesis Pathway in Isoprene-Emitting Hybrid Aspen

“…Foliage net assimilation and transpiration rates were measured with an ultrafast gas exchange system that is particularly suitable for measurements of transient leaf physiological responses (system half time of approximately 0.15 s; Laisk et al, 2002;Rasulov et al, 2010). The system has a circular (cross-sectional area of 8.04 cm 2 ) thermostatted clip on-type leaf cuvette.…”