Impact of elevated temperature and ozone on the emission of volatile organic compounds and gas exchange of silver birch (Betula pendula Roth)
Highlights
► Warming increased VOC emission and photosynthesis and reduced stomatal conductance. ► O3 elevation decreased VOC emission and photosynthesis. ► Increased substrate availability may partly explain enhanced VOC emission. ► Stomatal conductance did not regulate VOC emission.
Introduction
Increasing temperature and rising ozone (O3) levels seriously affect many natural ecosystems worldwide (IPCC, 2007, The Royal Society, 2008). Over the last 100 years, rising concentrations of greenhouse gases due to burning of fossil fuels and deforestation have led to approximately 0.74 °C increase in the mean global temperature, and it has been predicted to further rise by up to 2–5 °C in this century, the increase being even greater at the northern latitudes (IPCC, 2007). Tropospheric O3 is one of the major global air pollutants with current background concentrations in the northern Hemisphere being approximately 20–45 ppb. Its impact is expected to become even more important in the future due to increasing emissions of O3 precursors, nitrogen oxides (NOx) and volatile organic compounds (VOCs), in the atmosphere (Vingarzan, 2004, Sitch et al., 2007, The Royal Society, 2008). Both O3 and elevated temperature can disturb plant growth and production mainly by causing oxidative stress in the leaf apoplast, and especially processes involved in photosynthesis are sensitive to these stresses (Kangasjärvi et al., 2005, Sharkey, 2005, Wittig et al., 2007).
Plants emit a considerable percentage, even 10%, of the carbon fixed by photosynthesis back into the atmosphere as VOCs, including isoprene, mono- and sesquiterpenes and a number of compounds derived from the lipoxygenase pathway (green leaf volatiles, GLVs), isoprene and monoterpenes being the most prominent ones (Kesselmeier and Staudt, 1999, Atkinson and Arey, 2003, Peñuelas and Llusià, 2003, Holopainen, 2004). At a global scale, the emissions of VOCs from plants greatly exceed the emissions from the anthropogenic sources (Guenther et al., 2000, Peñuelas and Llusià, 2003). In general, the emission of VOCs from vegetation seems to depend on climatic conditions as well as on plant species and genotype, and time of the day and season (Kesselmeier and Staudt, 1999, Laurila et al., 1999, Grote and Niinemets, 2008).
The variability in VOC emissions results from complex interactions between the plant and its environment (Kesselmeier and Staudt, 1999, Dudareva et al., 2006). From the ecological point of view, plant-derived VOCs play multiple roles in communication and protection of plants against several abiotic and biotic stresses (Holopainen, 2004, Laothawornkitkul et al., 2009). Isoprene and monoterpenes, in particular, have been shown to provide protection against elevated temperature (Loreto et al., 1998, Peñuelas et al., 2005, Velikova and Loreto, 2005, Velikova et al., 2009) and O3 (Loreto and Velikova, 2001, Loreto et al., 2004, Calfapietra et al., 2008, Vickers et al., 2009), possibly by stabilizing thylakoid membranes of the chloroplasts and by acting as antioxidants, thus reducing oxidative stress in the leaves. In general, the studies have focused on the impacts of substantially high temperatures and O3 concentrations on plant VOCs, whereas less attention has been paid to plant responses to more realistic O3 or, especially, temperature elevations. Emission of VOCs from plants is known to increase with temperature, and the global warming over the past 30 years could have already increased global biogenic VOC emissions by 10%, and a predicted 2–3 °C rise in the mean global temperature could further increase plant-emitted VOCs by 30–45% (Peñuelas and Llusià, 2003, Rennenberg et al., 2006, IPCC, 2007). Continuously increasing tropospheric O3 levels may potentially either increase or decrease VOC emissions (Loreto et al., 2004, Fares et al., 2006, Fares et al., 2010, Calfapietra et al., 2008, Peñuelas and Staudt, 2010). Global warming and increasing emissions of greenhouse gases also have potential to influence future O3 levels e.g. by modifying the rates of O3 production and destruction in the atmosphere and by affecting the transport processes of O3 and its precursors (The Royal Society, 2008, Laothawornkitkul et al., 2009). Moreover, many volatile compounds emitted by vegetation are highly reactive and participate in atmosphere chemical processes, such as formation of O3 (Ryerson et al., 2001, Atkinson and Arey, 2003) and secondary organic aerosols (Yu et al., 1999, VanReken et al., 2006, Virtanen et al., 2010). Therefore, biogenic VOC emissions should be considered in air pollution and climate change scenarios.
Silver birch (Betula pendula Roth), a widely distributed and economically important tree species in the northern Hemisphere, is capable of emitting an array of mono- and sesquiterpenes (Zhang et al., 1999, Hakola et al., 2001, Vuorinen et al., 2005, Ibrahim et al., 2010). In Scandinavia, silver birch is growing at the extreme limits of its range, where the impacts of climate change, particularly climate warming, on forest ecosystems are already evident (Hemery et al., 2008). Birch is known to be relatively sensitive to O3, but variation exists between genotypes (Prozherina et al., 2003, Yamaji et al., 2003, Oksanen et al., 2007). A recent study, conducted with one of the birch clones used in the present study, revealed that gas exchange, a commonly used sensitivity indicator, was significantly influenced by elevated temperature and O3, i.e. warming enhanced net photosynthesis, whereas stomatal conductance was significantly and photosynthesis slightly reduced by elevated O3 (Riikonen et al., 2009). Moreover, VOC emission, a possible defense mechanism, was notably increased in European aspen (Populus tremula L.) exposed to elevated temperature for one growing season at the same experimental site as used in the current study (Hartikainen et al., 2009). Against this background, the aim of the present open-air exposure experiment was to determine the impact of moderately elevated O3 and temperature, alone and in combination, on VOC emission and gas exchange of four clones of silver birch under 2-year exposure. In 2007, VOC emissions of two clones of silver birch were studied, and in 2008, the experiment was expanded to cover all four clones and three different time occasions during the growing season. In addition to VOC emission analysis, measurements of net photosynthesis, stomatal conductance and expression of genes involved in VOC synthesis were carried out in 2008. Genes encoding 1-deoxy-d-xylulose 5-phosphate synthase (DXS), 1-deoxy-d-xylulose 5-phosphate reductoisomerase (DXR) and isopentenyl diphosphate (IPP) isomerase were selected for mRNA expression studies. DXS and DXR are important in producing the first intermediates specific to plastidial methylerythritol 4-phosphate (MEP) pathway, thus mediating the initiation of the entire plastidial terpene synthesis pathway. IPP isomerase mediates the conversion of IPP (produced in the MVA pathway) to dimethylallyl diphosphate (DMAPP), which is the precursor of isoprenoids (Hoeffler et al., 2002, Nagegowda, 2010). An inverse relationship between VOC emission and mRNA expression of DXS, DXR and IPP isomerase in birch was found in a previous chamber study with increased night-time temperatures (Ibrahim et al., 2010). This finding will be corroborated in the present study in field conditions.
Our hypotheses were: (1) elevated temperature increases VOC emissions, (2) elevated O3 decreases VOC emissions, (3) elevated temperature modifies O3 responses of silver birch, or vice versa, (4) alterations in photosynthesis, stomatal conductance and mRNA expression of DXS, DXR and IPP isomerase explain changes in VOC emissions, (5) birch clones differ in their responses to elevated O3 and temperature, and (6) variation in VOC emission during the growing season appears.
Section snippets
Study site, plant material and growth conditions
Four silver birch (B. pendula Roth) clones (12, 14, 15 and 25), originating from Laukansaari biodiversity birch stand (Punkaharju, 61°41′ N, 29°20′ E, 76 m a.s.l.) (Laitinen et al., 2000) and representing typical silver birch populations in central Finnish forests, were grown in an open-field experimental area at the University of Kuopio (Häikiö et al., 2007, Karnosky et al., 2007) in central Finland (62°53′ N, 27°37′ E, 80 m a.s.l.) over two growing seasons. Silver birch is reproducing sexually,
VOC emissions
Monoterpenes α-pinene, sabinene, β-myrcene, cis-ocimene + limonene (analyzed separately in 2007), 1,8-cineole, γ-terpinene, linalool and allo-ocimene, as well as homoterpene (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) were emitted in both years, but β-pinene emission from birch saplings was detected only in 2007. Correspondingly, sesquiterpenes α-copaene, aromadendrene and δ-cadinene were emitted in both years, but in 2008 also longifolene, α-humulene and caryophyllene oxide were found in the
Impact of elevated temperature and O3 on VOC emission
In this 2-year study on silver birch, a notable effect of slightly elevated temperature on VOC emission and gas exchange was demonstrated in an ecophysiologically relevant field experiment. The impact of O3 on VOC emission was less pronounced, and significant interactions between O3 and temperature elevation were not observed. Generally, VOC emission is known to increase with rising temperature (Singsaas et al., 1999, Loreto et al., 2006, Filella et al., 2007). The present study on birch showed
Conclusions
Our study indicates that rising temperature enhances VOC emissions from silver birch, although the unpredictability of the extent of impending climatic changes still causes considerable uncertainty in VOC emission estimations from boreal forests. Chronic low level O3 stress appears to decrease, rather than increase, VOC emission. The temperature related increase in VOC emission, particularly terpenes, is potentially related to increase carbon resources due to enhanced photosynthesis at elevated
Acknowledgements
This study was supported by the Academy of Finland (project 109933) and the Finnish Graduate School in Environmental Science and Technology (EnSTe). We thank Timo Oksanen (University of Eastern Finland, Department of Environmental Science, Kuopio) for his technical support in programming and maintaining the open-air O3 fumigation and warming treatment systems, staff in the Research Garden of the University of Eastern Finland (Kuopio) for their help of practical issues at the field site and
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Present address: The Finnish Forest Research Institute, Suonenjoki Research Unit, FI-77600 Suonenjoki, Finland.