Monoterpene ‘Thermometer’ of Tropical Forest-Atmosphere Response of High Temperature Stress
Discovery of a tropical forest biochemical thermometer.
Tropical forests absorb large amounts of atmospheric carbon dioxide (CO2) through photosynthesis, but elevated temperatures suppress this absorption while promoting biochemical emissions of monoterpene. Plant monoterpenes are hypothesized to be involved in thermotolerance of photosynthesis, but observations are scarce and global models assume that tropical monoterpene emissions are dominated by α-pinene. Moreover, models assume that monoterpene emissions composition is insensitive to temperature. Using 13CO2 labeling, this study shows that monoterpene emissions from tropical leaves derive from recent photosynthesis and demonstrate distinct temperature optima for five groups, potentially corresponding to different enzymatic temperature-dependent reaction mechanisms within β-ocimene synthases. As diurnal and seasonal leaf temperatures increased during the Amazonian 2015 El Niño event, leaf and landscape monoterpene emissions showed strong linear enrichments of the highly reactive β-ocimenes (Group 1) at the expense of other monoterpene isomers (Groups 4–5).This high positive sensitivity of Group 1 monoterpenes and negative temperature sensitivity of α-pinene (Group 2), typically assumed to be the dominant monoterpene with moderate reactivity, was not accurately simulated by current global emission models.
Given that β-ocimenes are highly reactive with respect to both atmospheric and biological oxidants, the results suggest that highly reactive β-ocimenes may play important roles in the thermotolerance of photosynthesis by functioning as effective antioxidants within plants and as efficient atmospheric precursors of secondary organic aerosols. Thus, monoterpene composition may represent a new sensitive thermometer of leaf oxidative stress and atmospheric reactivity, and therefore a new tool in future studies of warming impacts on tropical biosphere-atmosphere carbon cycle feedbacks. Plant response to warming may involve a single enzyme or gene (ocimene synthase), insertion into transgenic plants will facilitate quantitative studies on the role of light-dependent monoterpences in oxidative stress responses including thermotolerance of photosynthesis. This presents opportunities for the development of the ‘monoterpene thermometer’ gene in agricultural plants as a sensor of plant oxidative stress during environmental extremes.
Tropical forests are increasingly threatened by increased temperatures that can lead to oxidative stress, but the physiological mechanisms plants use to cope with these conditions remain poorly understood. This study reports the discovery of a tropical forest monoterpene thermometer where the composition of monoterpene emissions changes as a function of temperature. The scientists found a high-temperature sensitivity of the composition of tropical leaf monoterpene emissions across a wide range of temporal (minutes to seasons) and spatial (leaf to ecosystem) scales. As monoterpene emissions increased with temperature, the composition shifted such that highly reactive monoterpenes accounted for a larger fraction of the total under high-temperature stress. This result suggests a biological function of these highly reactive monoterpenes in the tropics. Given their high reactivity to both atmospheric and biological oxidants, the results suggest that monoterpenes play important roles in the thermotolerance of photosynthesis by functioning as effective antioxidants within plants and as efficient atmospheric precursors of secondary organic aerosols, thereby enhancing surface cooling and water recycling. Thus, monoterpene composition may represent a new sensitive ‘thermometer’ of leaf oxidative stress and atmospheric reactivity, and therefore a new tool in future studies of warming impacts on tropical biosphere-atmosphere carbon cycle feedbacks.
Lawrence Berkeley National Laboratory Climate and Ecosystem Sciences Division
This work was supported as part of the GoAmazon 2014/5 and the Next-Generation Ecosystem Experiments (NGEE)–Tropics funded by the Office of Biological and Environmental Research (BER), within the U.S. Department of Energy Office of Science, through contract No. DE-AC02-05CH11231 to Lawrence Berkeley National Laboratory, as part of DOE BER’s Terrestrial Ecosystem Science Program. Additional funding for this research was provided by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
Jardine, K.J., Jardine, A.B., Holm, J.A., Lombardozzi, D.L., Negron-Juarez, R.I., Martin, S.T., Beller, H.R., Gimenez, B.O., Higuchi, N., and Chambers, J.Q. “Monoterpene ‘thermometer’ of tropical forest-atmosphere response to climate warming.” Plant, Cell & Environment 40(3), 441–452 (2017). [DOI:10.1111/pce.12879].