Abstract
Plants emit a substantial amount of biogenic volatile organic compounds (BVOCs) into the atmosphere having significant effects on atmospheric chemistry, physics, and the organisms. In this chapter, important facts about BVOCs’ production mechanism, storage, and emissions due to various abiotic and biotic factors have been discussed. The role of BVOCs in defense system through plant signaling has also been discussed. The chapter continues with the discussions about the importance of BVOCs in the formation of tropospheric ozone and secondary organic aerosols and ultimately strengthens our understanding about global change research.
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5.1 Introduction
Generally, any organic compound having vapor pressure high enough under normal conditions to be vaporized into the atmosphere is termed as a volatile organic compound (VOC). VOCs emitted by plants are widely known as biogenic volatile organic compounds (BVOCs). BVOCs are classified according to their structure and biosynthetic origin (Pichersky et al. 2006). BVOCs represent a group of organic trace gases (except carbon dioxide and monoxide) released into the atmosphere from the plants and soils. Biogenic VOCs include isoprenoids (isoprene and monoterpenes) as well as alkanes, alkenes, carbonyls, esters, ethers, alcohols, and acids. The lifetime of BVOCs in the atmosphere varies from minutes to several days (Kesselmeier and Staudt 1999).
Isoprene (C5H8) is the most widely studied single BVOC which accounts for >90 % of the total BVOC emissions of a particular plant species (Blande et al. 2007). The total annual isoprene emissions account for 440–660 TgC (Guenther et al. 2006), which is a large fraction of annual global BVOC emissions (700–1000 TgC) (Laothawornkitkul et al. 2009). Isoprene belongs to the biochemical class of terpenoids; other BVOCs under the same class are monoterpenes (C10H16) and sesquiterpenes (C15H24). BVOCs produced by plants are involved in plant reproduction (by attracting pollinator), growth, wound healing, development, and defense against herbivores. They are also involved in a communication process between plants and insects, within plants, and within plant communities (Pichersky and Gershenzon 2002; Peñuelas et al. 1995; Shulaev et al. 1997) (Fig. 5.1). BVOCs can also protect plants against high temperatures. But, on the other hand, BVOC emissions increase with warming and might produce both negative and positive feedback on global warming through aerosol formation as well as direct and indirect greenhouse effects (Fig. 5.2).
Several authors have reported that plants re-emit a substantial fraction of their assimilated carbon into the atmosphere as BVOCs that can affect chemical and physical properties of the atmosphere (Peñuelas and Llusià 2001; Kesselmeier and Staudt 1999).
A large fraction of carbon can be lost during BVOC emission and it was estimated to be around ~10 % of the total carbon stored by plants through photosynthesis (Peñuelas Llusià 2003). Apart from abovementioned functions, there is another function of BVOCs that has dragged scientist attention given global warming. Recently, it is found that production and emission of certain BVOCs such as isoprene and monoterpenes, which contribute a large fraction of total BVOCs, confer protection against high temperature. There are various factors responsible for BVOC emissions and biological and physicochemical processes (Figs. 5.1 and 5.2). Several internal (biochemical and genetic) and external factors control emission rates of different BVOCs by altering their synthesis, diffusion, or vapor pressure to the atmosphere. The external factor includes abiotic (light, wind, water availability, temperature, and ozone) and biotic (animal, plant, and microorganism interactions) factors (Fig. 5.2). The complex net of these factors and their interactions and the different responses of the different BVOCs produce large qualitative and quantitative and spatial and temporal variability of emissions and frequent deviations from current standard emission models, mostly based on temperature and light response (Peñuelas and Llusià 2001). Plant emissions of BVOCs have strong relevance for plant physiology and plant ecology, atmospheric chemistry, and climate.
5.2 BVOC Emissions: Why and How
It is now well reported by several authors that a wide variety of volatile non-methane organic compounds (referred to hereafter as biogenic volatile organic compounds (BVOCs)) are emitted into the atmosphere from vegetation (Fall et al. 1999; Geron et al. 2000; Guenther et al. 1995, 2000; Fuentes et al. 2000). BVOCs are stored in specialized structures like glandular trichomes, glands, and resin ducts/resin canals (Turner et al. 2000; Franceschi et al. 2005) and are tightly separated by the surrounding cells by an impermeable layer, generally cuticular cells (Gershenzon et al. 2000). On the other hand, if plants have no storage structures for BVOCs, they have some temporary pools/nonspecific storage (observed in both conifers and broad-leaved trees) in mesophyll that freely diffuse out of the leaf along their concentration gradient. The only determining factor for this process of gas diffusion is stomatal conductance.
5.2.1 Mechanism of BVOC Emission
The mevalonic acid (MVA) pathway and the 2-deoxyxylulose 5-phosphate/2-methylerythritol 4-phosphate (MEP) pathway (Fig. 5.3) are the two metabolic routs responsible for DMAPP formation. Leucine metabolism is another pathway which works as a source of isoprenoids. The source of DMAPP within the chloroplast is the MEP pathway (Rohmer et al. 1993). The MEP pathway begins with pyruvate and glyceraldehyde 3-phosphate (Rohmer et al. 1993) and involves skeletal rearrangement to make the branched chain and finally ends with isoprene (Arigoni et al. 1997). In the MEP pathway, each carbon in the starting intermediate costs three ATPs plus two NADPH if at the redox level of a triose phosphate with CTP equivalent to ATP. According to Lichtenthaler and coworkers, this pathway is responsible for most of the isoprenoids made in plastids (Lichtenthaler et al. 1997). It is proved that this pathway is responsible for isoprene synthesis (Schwender et al. 1997; Zeidler et al. 1997). The MEP pathway is more efficient (cost is only six carbon atoms, 20 ATPs, and 14 NADPH) as compared to the MVA pathway (cost is nine carbon atoms, 24 ATPs, and 14 NADPH).
5.2.2 Role of Isoprene Synthase
Plants emit isoprene produced from DMAPP by isoprene synthase (enzyme) (Silver and Fall 1991) which works at a relatively high pH and needs Mg2+ (Schnitzler et al. 1996; Silver and Fall 1995) which is present inside chloroplasts (Mgaloblishvili et al. 1979; Wildermuth and Fall 1996, 1998). Wildermuth and Fall (1998) also found some isoprene synthase activity bound to thylakoid membranes. Isoprene synthase activity is found to be soluble (Wildermuth and Fall 1996, 1998). The membrane-bound form of isoprene synthase activity appeared to have the same kinetics as the soluble form. Whether the soluble form is converted to the bound form or vice versa and what effect this might have on the activity of isoprene synthase is not known. Thylakoid-bound isoprene synthase activity could be stimulated threefold by the addition of GTP and palmitoyl CoA (Wildermuth 1997). The conversion of DMAPP to isoprene is catalyzed by isoprene synthase. Perhaps isoprene is a product of the breakdown of higher isoprenoids in E. coli. In bacteria (Bacillus subtilis), isoprene emission occurs during different phases of growth (Wagner et al. 1999).
5.3 Atmospheric Chemistry and Physics of BVOCs
5.3.1 Production of Tropospheric Ozone
According to Fehsenfeld et al. (1992) and Thompson (1992), isoprene emission from plants plays a significant role in atmospheric chemistry (Fig. 5.2). BVOCs such as isoprene can alter atmospheric chemistry affecting the residence times of gases that contribute to the greenhouse effect. Isoprene oxidation in the atmosphere can give rise to ozone and smog if nitrogen oxides are present in the atmosphere (Daum et al. 2000; Haagen-Smit 1952). In the high-isoprene emission zone, like a zone with extensive tropical forest, isoprene oxidation can account for up to 71 % of the reduction in OH (compared to only 11 % for CO oxidation and 5 % for CH4 oxidation) (Grosjean 1995). Hence, it is very important to understand the role of BVOCs in atmospheric chemistry (Thompson et al. 1992; Fehsenfeld et al. 1992). BVOC emissions can indirectly increase the concentrations of other important greenhouse gases such as methane resulting in reduced atmospheric oxidation capacity due to depletion of OH radicals (Lelieveld et al. 2008). Hydroxyl radicals are very reactive oxidants and act as the atmospheric detergent (Lelieveld et al. 2008). After the study of chemistry and transport model by Wang et al. (1998), it is clear that global emissions of BVOCs, particularly isoprene, can cause a 15 % increase in the background levels of O3 and a 20 % decrease in the mean OH concentrations (Wang et al. 1998). Another study suggested that global VOC emissions (isoprene as a large fraction) cause an 18 % increase in the global tropospheric O3 concentration, a 16 % decrease in the global OH concentrations, and a 20 % increase in the tropospheric lifetime of CH4 (Poisson et al. 2000). Even the NOx spatial distribution and deposition are affected by BVOC interactions.
The oxidation of BVOCs by OH in the presence of sufficient NOx leads to the formation of O3 in the troposphere by disruption of the photochemical steady state of O3 (i.e., allows the oxidation of NO to NO2 without removal of an O3 molecule) and so causes elevated O3 concentrations. NOx emissions may result from fossil fuel combustion, fertilizer application, and biomass burning, as well as natural production by lightning. As tropospheric photochemistry is highly nonlinear with respect to the emissions of O3 precursors, modeling is required to determine the effects of BVOC emissions on O3 concentrations in the troposphere (Fowler et al. 2008).
At night, NOx is present in the atmosphere as NO2. According to Monson and Holland (2001), sunlight photolyzes NO2 which leads to the formula of one molecule of ozone per one molecule of NO2. In the absence of hydrocarbons, the total NOx level determines the amount of ozone in the atmosphere.
This cycle is continued as long as there are C–H bonds available which enable the formation of ozone. At a very high NOx level, one isoprene molecule can result in multiple molecules of ozone. But at a low NOx level, isoprene emission can reduce ozone level via different set of reactions (Trainer et al. 1987). Isoprene also plays a role in the growth of aerosols in the atmosphere. Though aerosol’s yield per molecule in the atmosphere is much lower than for monoterpenes, due to its large emission, isoprene became a significant source of secondary organic aerosol (Claeys et al. 2004; Edney et al. 2005; Kroll et al. 2005, 2006; Ng et al. 2006; Olcese et al. 2007). The resulting changes in climate may affect BVOC emission rates, providing a positive feedback in the climate system. The oxidation of BVOCs also contributes atmospheric CO (Hatakeyama et al. 1991; Fehsenfeld et al. 1992; Bergamaschi et al. 2000; Griffin et al. 2007) which impacts the oxidative capacity of the atmosphere similar to isoprene through acting as a sink for OH (Logan et al. 1981). Thereby, the oxidation of CO is a source or sink of O3, depending on the NOx availability. Atmospheric oxidation of BVOCs can also result in the formation of peroxyacetyl nitrates (PANs) (Fehsenfeld et al. 1992). PANs have longer residence time and can be transported to a larger distance. PANs are a source of NOx when they are thermally decomposed in warmer air (Fehsenfeld et al. 1992; Poisson et al. 2000), contributing a high level of NOx in the regime without local NOx emissions which ultimately lead to higher O3 levels in remote areas.
5.3.2 Secondary Aerosol Formation
According to various laboratory and field studies, BVOCs are a significant source of secondary organic aerosol (SOA) (Fig. 5.1) (Leaitch et al. 1999; Joutsensaari et al. 2005). Through the mechanism SOA formation via BVOC oxidation is still not fully explained (Kulmala 2003), but it is understood that BVOC oxidation results in lower vapor pressure compounds which triggers their condensation on preexisting atmospheric molecules (Joutsensaari et al. 2005). Terpenes and sesquiterpenes contribute more significant amounts of SOA as compared to isoprene (Claeys et al. 2004; Leaitch et al. 1999; Meskhidze and Nenes 2006). Atmospheric aerosols are considered to have direct effects on climate as they scatter solar radiation. Secondarily they also have indirect effects such as cloud condensation nuclei, changing cloud albedo, and the degree of cloud cover. The possibility that SOA formation from BVOC emissions cools the Earth and so a moderate temperature is dependent on BVOC emission from plants – and other similar feedbacks in Earth’s system – is the focus of much current research. Hence, there is the potential for feedback between BVOC emissions, SOA, and climate.
5.4 Factors Affecting BVOC Emission
5.4.1 Taxonomic Characteristics
Trees are traditionally considered to be the key BVOC emitters. Isoprene, monoterpenes, and sesquiterpenes are emitted from many plants and they appear to have an adaptive role in protecting plants from abiotic stress. However, only some plant species emit isoprene. For example, taxonomic groups as distinct as mosses and oak trees emit isoprene, but in groups as closely allied as mosses and hornworts or oak and maple trees, both are emitters (mosses and oaks) and non-emitters (hornworts and maples) (Lerdau and Gray 2003; Hanson et al. 1999). Monson et al. (2013) studied various isoprene-emitting genera with high taxonomic diversity, such as the Fabaceae (old name: Leguminosae). Mosses (Hanson et al. 1999), ferns (Tingey et al. 1987), gymnosperms, and angiosperms (http:www.es.lancs.ac.uk/cnhgroup/iso-emissions.pdf for comprehensive list) consist of members emitting BVOCs and not emitting BVOCs. Isoprene synthases (IspSs) are the enzyme which catalyzes the conversion of DMAPP to isoprene. IspSs have been sequenced from several plant species such as the Populus species (Sasaki et al. 2005; Miller et al. 2001) and kudzu (Pueraria lobata) (Sharkey et al. 2005). According to Bohlmann et al. (1998), IspSs belong to the TSP-b family of terpene synthases, also code for monoterpene and sesquiterpene synthases in angiosperms. But these are absent in gymnosperms. Isoprene synthase genes analyzed so far have been found to have high-sequence homology with certain monoterpene synthase genes (Miller et al. 2001; Sharkey et al. 2005) and even a bifunctional acyclic monoterpene synthase/isoprene synthase gene (Sharkey et al. 2013). A small change in the gene sequences can easily alter both substrate and product specificity of IspS genes (El Tamer et al. 2003; Tholl 2006; Kampranis et al. 2007). North American oaks all emit isoprene, but many European oaks do not. Instead, among European oaks a variety of behaviors is found. Some clades emit isoprene, some emit monoterpenes in a light dependent manner, and some emit very little terpene (Loreto et al. 1998a, b; Csiky and Seufert 1999; Kesselmeier and Staudt 1999).
5.4.2 Temperature
BVOC emissions are highly temperature dependent because higher temperature increases the rate of chemical reaction and cellular diffusion and increases the vapor pressure of volatile compounds (Lerdau et al. 1994; Tingey et al. 1991; Sharkey and Yeh 2001; Fuentes et al. 1999). The emission rates of BVOCs are analyzed by their synthesis rates and physicochemical parameters like solubility, volatility, and diffusivity (Niinemets et al. 2004; Kesselmeier and Staudt 1999; Laothawornkitkul et al. 2009). BVOC emission rates are highly controlled by both external and internal factors. Although there are large uncertainties in the magnitude of emission rates of BVOCs, a recent estimate for North America (Guenther et al. 2000) suggests that of an estimated 84 TgCyear_1 of BVOC emissions, 30 % are isoprene, 25 % are terpenoid compounds, and 40 % are non-terpenoid compounds including methanol, hexene derivatives, and 2-methyl-3-buten-2-ol.
BVOCs follow the Henry’s law constant (KH) and they partition between gas and liquid phases in the plants. Leng et al. (2013) reported that the measured KH values for isoprene, limonene, α-pinene, and linalool at 298 K were 0.036, 0.048, 0.029, and 21.20 mol L−1 atm−1, respectively. They also reported that diffusion of these BVOCs follow the first-order kinetics for rate of loss and diffusion coefficients of all the species as a function of temperature. Temperature affects the evaporation and release of a minimal part of the pools of BVOCs that leaks out the impermeable cell layer. Herbivory, strong winds, and forest fires are the other strong factors responsible for BVOC emissions (Litvak and Monson 1998). High humidity also plays a significant role in BVOC emission from the structures of plants containing BVOC pools.
The enzymes which are responsible to catalyze the synthesis of BVOCs can be easily controlled or influenced by temperature. Emissions of volatile terpenes have a Q10 = 2–4 at temperatures variable between 20 and 40 °C (Monson et al. 1992). Thus the elevation in atmospheric temperature is a direct effect of terpenes formed through enzymatic action.
5.4.2.1 Thermotolerance
Sharkey and Singsaas (1995) were the first researchers who reported that isoprene plays a significant role in thermotolerance function. Singsaas et al. (1997) showed that adding isoprene to an air stream (or nitrogen gas) that passed over these leaves could increase the temperature at which damage occurred from as low as 35 °C to as high as 45 °C. Thermotolerance was also mentioned with special reference to monoterpene emissions from Quercus ilex (oak species) by Loreto et al. (1998a, b). Several studies have reported the positive link between isoprene and photorespiration (Peñuelas and Llusià 2002). According to one study, “Thermotolerance of leaf discs from four isoprene-emitting species is not enhanced by exposure to exogenous isoprene” (Logan and Monson 1999) and was of substantial concern. They found that leaf disks’ chlorophyll fluorescence held in darkness or light plus nitrogen did not increase until 45 °C, irrespective of whether isoprene was in the air stream. In their experiments the control leaf pieces did not exhibit photosynthetic damage below 45 °C. Measurements of the temperature where CO2 uptake fell to zero were not reported in the study.
Two advancements were added in definitive experiments. First was the refinement of the thermotolerance hypothesis and the second was the use of fosmidomycin, the inhibitor that eliminates isoprene production without affecting photosynthesis. With these improvements, much stronger evidence for the thermotolerance hypothesis has been obtained (Sharkey et al. 2001). The study reported that the isoprene synthesis provides tolerance of short high-temperature episodes. The molecules similar to isoprene were also tested to find out the basic requirements for thermotolerance. One rule was apparent in the results. The compounds taken into consideration were alkenes (1,3-butadiene, 1-butene, and cis 2-butene) that provided thermotolerance though alkanes (n-butane, iso-butane, and 2-methyl-butan) did not; they even increased the damage caused by heat (Sharkey et al. 2001).
5.4.3 Soil Moisture
Soil moisture is one of the important factors responsible for BVOC emission from plants. Soil moisture is significantly correlated with BVOC (isoprene and monoterpene) emission (Gray et al. 2014). Several authors studied the global BVOC emission model with soil moisture. Guenther et al. (2006) estimated a 7 % decrease in isoprene emission due to soil moisture’s effect, while Muller et al. (2008) calculated a 20 % decrease. The lower soil moisture can induce stomatal closure, which can reduce the production and emission of BVOCs coming directly from temporary storage pools inside the leaves (McBean et al. 2005).
5.5 BVOC Emission and Global Warming
Climate models suggest that, during the twenty-first century, the mean global temperature will increase by 1–6 °C (with a best estimate of 2–3 °C) (IPCC 2007). BVOC emissions are altered by varying their temperature; their emissions increase with temperature to a certain limit, beyond which enzyme degradation and physiological responses to heat stress affect the emission pattern (Guenther et al. 1993).
Emissions of BVOCs are always run along a vapor pressure gradient from the cellular level (containing relatively high concentrations) to the surrounding air of leaves (containing relatively low concentrations) due to transport. Temperature increases the emission rates of most BVOCs exponentially by enhancing the enzymatic activities of synthesis, by elevating the BVOC vapor pressure, and by decreasing the resistance of the diffusion pathway (Tingey et al. 1991). Penuelas and Llusia (2003) have suggested that increasing mean global temperatures by 2–3 °C could enhance global BVOC emissions by 25–45 %. The dependency of BVOC emission rates on temperature can be further explained with G93 algorithm, given by Guenther et al. (1993), where the emission rate of monoterpene can be expressed as:
where E and E s are measured emission rates and basal emission rates at a standard temperature, i.e., 30 °C, respectively. T and T s are measured and standard temperatures, respectively. β is an empirical coefficient (depends on species of vegetation and compounds emitted. With the similar model at a local temperature regime (4 °C) for Douglas fir trees, Constable et al. (1999) found a predicted increase in emission of 52 %, 46 %, and 41 % for α-pinene, β- pinene, and Δ-3 carene, respectively. Whereas isoprene emission is modeled as:
where E is the isoprene emission rate at temperature T and PAR flux L, E S is the emission rate measured at standard temperature TS and PAR (1000 mmol m−2 s−1), and the scaling factors CT and CL are defined by:
where, C T1 (95,000 J mol−1), C T2 (230,000 J mol−1), T m (41 °C), α (0·0027), and C L1 (1·066) are parameters calculated from experiments made on some BVOC-emitting plant species (Guenther et al. 1993). R is the gas constant (8·134 J K−1 mol−1).
Applying the algorithms of emission response to temperature (Llusià and Peñuelas 2000; Tingey et al. 1991; Peñuelas and Llusia 2003) calculated global warming over the past 30 years and found that BVOCs increased global emissions by 10 % and a further 2–3 °C rise in the mean global temperature, which is predicted to occur this century (Houghton et al. 2001), could increase BVOC global emissions by an additional 30–45 %.
At a very high temperature, isoprene emission declines dramatically. It is possible that extreme temperature rises will eventually cause a decrease in isoprene emissions, irrespective of other changes to ecosystems.
Global warming can also indirectly influence global- and regional-scale BVOC emissions by altering vegetation species composition and vegetation characteristics (Wilmking et al. 2004; Starfield and Chapin 1996). Simulation model studies predict forest dieback at a lower latitude such as Amazonia (Cox et al. 2004). However, the models predicted that boreal forests will be exposed northward in a global warming scenario (Chapin et al. 2000; Kittel et al. 2000). The increase in boreal forests may increase BVOC emissions for species such as Populus sp. and Picea sp. (Lerdau and Slobodkin 2002). However, forests at lower altitudes may reduce BVOC emission, probably having no impact on global budgets.
5.6 BVOCs and Plant Signaling (Plant–Plant and Plant–Insect Herbivory)
Several authors discussed about the BVOC emissions and their role in many abiotic stress tolerance, including thermotolerance of photosynthesis and reduced oxidative stress (Sun et al. 2013; Singsaas et al. 1997; Loreto et al. 1998; Sharkey and Singsaas 1995; Possell and Loreto 2013; Llusià et al. 2005).
As per the authors of the recent twenty-first century, BVOCs are essential components for communication within a plant, between plants, and between a plant and an insect (Trowbridge and Stoy 2013; Dicke and Baldwin 2010; Duhl 2008; Baldwin et al. 2002). In plant–herbivore interactions, the volatiles can act as attractants or repellents to herbivores (Laothawornkitkul et al. 2008). For instance the α-pinene (monoterpene) released by wounded Pinus sylvestris L. (Scotch pine) acts as an attractant to Hylobius abietis (large pine weevil), and thus, previous damage of a conifer can increase herbivory damage. However, by repelling limonene attraction of H. abietis can be reduced (Nordlander 1991). According to Mithen (2001), heat-stressed Brassica nigra (black mustard) plants may become attractive to specialized feeders of Brassicaceae (older name, Cruciferae) due to the increasing emissions of allyl isothiocyanate (organosulfur compound and responsible for the pungent taste of the Cruciferae family). Arimura et al. (2001) found that BVOCs emitted from Tetranychus (spider mite)-infested lima bean/butter bean (Phaseolus lunatus L.) can activate genes encoding pathogenesis-related proteins and phenylalanine ammonia-lyase in leaves of noninfested neighboring plants, and GLVs can serve as signal compounds in plant–plant communication (Arimura et al. 2001). Later on it was found that such kind of sharing of information (between plants) depends on the diffusion and convection of the BVOC information between a sender and a receiver plant (Baldwin et al. 2002).
5.7 Conclusion
BVOCs played an important role in atmospheric chemistry and were also involved in the several mechanisms of plant physiology like plant signaling. Any biotic or abiotic stress is responsible for BVOC emission from plants. The overall effect of increasing BVOC emissions will depend on the positive and negative feedback mechanism. These emissions are released in support of defense mechanisms from plant species. This chapter signifies about the important component of atmospheric sciences as well as plant physiology, i.e., BVOCs which are still under progress; very less attention has been put toward this mechanism. The important environmental issue of global warming is also influenced by BVOCs. BVOCs also played an important role in the production of tropospheric ozone, aerosol formation, and ultimately SOA. In short, this chapter concludes with the fact that precursors play an important role in the production of secondary pollutants and these precursors like BVOCs take part in climate change issues.
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Sonwani, S., Saxena, P., Kulshrestha, U. (2016). Role of Global Warming and Plant Signaling in BVOC Emissions. In: Kulshrestha, U., Saxena, P. (eds) Plant Responses to Air Pollution. Springer, Singapore. https://doi.org/10.1007/978-981-10-1201-3_5
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