ReviewShort-chain oxygenated VOCs: Emission and uptake by plants and atmospheric sources, sinks, and concentrations
Introduction
Over the last few years great emphasis has been placed on emissions of volatile organic compounds (VOCs) by plants. Their presence in the air affects atmospheric chemistry: reactions with OH radicals and NOx produce ozone (Atkinson, 2000), a secondary oxidant pollutant in the troposphere. Furthermore, VOCs also react with ozone to form OH radicals and can form aerosol particles (Matsunaga et al., 2003; Goldstein et al., 2004; Holzinger et al., 2005) that can act as cloud condensation nuclei (Kavouras et al., 1998) with climatic implications (Peñuelas and Llusià, 2003).
Emitted VOCs can represent up to 10% of the carbon fixed by plants (Llusià and Peñuelas, 2000; Peñuelas and Llusià, 2004) and their multiple roles in plant physiology have been widely studied. They seem to provide protection against high temperatures (Singsaas and Sharkey, 1998; Peñuelas and Llusià, 2002), high irradiation (Peñuelas and Munne-Bosch, 2005), and oxidation stress (Velikova et al., 2005). As well, they also act as herbivore deterrents, as attractants of pollinators and the enemies of herbivores (Pichersky and Gershenzon, 2002), as plant–plant communication cues (Peñuelas et al., 1995), and as plant ‘safety valves’ (Rosenstiel et al., 2004). The release of VOCs by plants after wounding or stress and, specially, the release of methanol and hexenals in connection with lipoxygenase activity (Fukui and Doskey, 1998; Fall et al., 1999; Heiden et al., 2003; Peñuelas et al., 2005) are currently widely under study.
Most of the interest in VOCs has to date been focused on isoprenoids (isoprene, monoterpenes, and sesquiterpenes), and less studies have dealt with short-chain oxygenated compounds (oxVOCs) such as formaldehyde, acetaldehyde, acetone, methanol, ethanol, and formic and acetic acids. These compounds were formerly grouped together under the generic name of ‘other VOCs’ and were thus split into two categories: (i) other reactive VOCs with lifetimes of less than one day (including formaldehyde and acetaldehyde) and (ii) other less reactive VOCs with lifetimes of more than one day (including methanol, ethanol, formic acid, acetic acid, and acetone) (Guenther et al., 1995).
Emissions of many of these oxygenated compounds, because there are analytical difficulties associated with their sampling and analysis, were identified only recently, and many of them were previously thought to have only a limited role in atmospheric chemistry (Fall, 1999). Nowadays, however, growing importance is being attached to the study of these compounds. A large amount of carbon (150–500 Tg C y−1) fluxes from the Earth's surface into the atmosphere in the form of oxygenated species. There is evidence of the presence of highly abundant global sources of oxVOCs, although their origin is not as yet exactly clear (Singh et al., 2001, Singh et al., 2004). These sources are either direct—primary—or indirect—secondary—and can be either biogenic or anthropogenic.
Some analytical problems have been solved with the use of proton transfer reaction-mass spectrometry (PTR-MS) (described by Lindinger et al., 1998). This technique allows for real-time or on-line (without preconcentration) monitorization of emissions at concentrations as low as pptv (1 pptv=1 part in 1012 by volume) and so the responses of plant emissions to environmental changes can be detected almost instantaneously. It has been used in measures of direct leaf emissions (Fall et al., 1999; Karl et al., 2002a; Peñuelas et al., 2005) and atmospheric mixing ratios (Sanhueza et al., 2001; Warneke et al., 2003; Filella and Peñuelas, 2006), as well as coupled to micrometeorological techniques like eddy covariance (Karl et al., 2001a, Karl et al., 2001b), proving to be a powerful tool.
In this paper we review current knowledge of emissions of oxVOCs by plants and the factors that control them (Fig. 1), and also provide an overview of sources, sinks, and concentrations found in the atmosphere. These are areas of study that are still not fully understood and are yet to be fully deciphered. The exchange of oxVOCs between plants and the atmosphere has been studied (i) in various plant species or communities, (ii) using different approaches and objectives, (iii) with different sampling and analytical techniques, and (iv) under wide-ranging field and laboratory conditions. The papers cited in our review reflect the whole spectrum of situations that have led authors to reach conclusions that in some cases may seem even to be contradictory. For instance, some authors have proposed that oxVOCs emissions are mainly physiologically controlled, while others consider that the principal control mechanisms are physicochemical. In fact, control by physicochemical processes does not preclude biochemical control (or vice versa) and it is very likely that both mechanisms are involved. However, the lack of knowledge regarding processes involved prevents us from clarifying exactly what is conditioning the exchange of a certain compound and when, how, and why it is doing so.
Short-chain oxVOCs can be emitted or taken up by plants. The direction of the exchange is thought to be at least partly determined by the atmospheric mixing ratios, since gases move along the concentration gradient between the inner part and the outside part of the leaf. Another physicochemical property that influences oxVOC atmospheric exchange is solubility. These compounds all have in common high water solubility, as shown by their Henry's law constants (H) that range in magnitudes from 10−2 (formic acid) to 101 (acetaldehyde) Pa m3 mol−1 under standard conditions. These figures are low in comparison with those of highly volatile isoprene and monoterpenes, both of which have constants in the order of 103 Pa m3 mol−1 (Sander, 1999). In highly water-soluble compounds exchange is more affected by stomatal conductance, with the degree of stomatal sensitivity varying with H (Niinemets and Reichstein, 2003b). Thus, physicochemical characteristics such as low volatility or diffusion of some VOCs may also control emissions and interact with physiological limitations (Niinemets and Reichstein, 2003a, Niinemets and Reichstein, 2003b; Niinemets et al., 2004).
Aside from stomatal regulation, the exchange of oxVOCs can also be physiologically controlled by metabolic activity rates and both of these processes are affected by internal (genetic traits, developmental stage, phenology, water content, etc.) and environmental (light, temperature, relative humidity, herbivory, and pollution stresses, wind speed, etc.) conditions. The oxVOCs formation mechanisms within the plant are known in some cases, although often our knowledge of these processes is not as detailed as would be desirable. Furthermore, unknown processes contributing to the VOC pool within the plant might be at work. The metabolic pathways working in the opposite direction, that is, those that determine the fate of the uptaken oxVOCs within plants, also warrant further study.
Uptake can occur by means of the absorption of gas-phase oxVOCs through the stomata into the mesophyll or via adsorption into the cuticle as a result of dry (gas-phase) or wet (liquid-phase) deposition. Although entry through the stomata is the most commented upon, studied, and—possibly—important way of absorption of short-chained oxVOCs, the diffusion of adsorbed oxVOCs through aqueous pores of the cuticle may also play an important role in absorption, as has been described recently for inorganic and organic ions (Schreiber, 2005; Schönherr, 2006). This could happen, for example, after rain, on dew-wetted leaves, or by means of the transpired water vapour recondensed on the leaf surface (Burkhardt et al., 1999). On the other hand, if not absorbed, the oxVOCs adsorbed on the cuticle may be revolatilized, for example with the evaporation of dew in the morning, as a result of a decrease in atmospheric concentration caused by photochemical activity or through the action of air turbulence (wind). As well, oxVOCs may react with other atmospheric chemical species on the cuticle itself.
In addition to adsorbed and absorbed oxVOCs, in certain studies uptake estimates may include oxVOC scavenging resulting from the reactions of the oxVOCs with other reactive VOCs freshly emitted by plants. This would specially be the case in measurements carried out within canopies or above communities, although the low reactivity of the short-chained oxVOCs may render this process quantitatively unimportant and ozone chemistry may turn out to be the main factor responsible for scavenging newly emitted reactive VOCs such as isoprenoids (Goldstein et al., 2004; Holzinger et al., 2005).
The emission of oxVOCs from within the leaf may occur along the same pathways as the uptake, that is, via the stomata and the cuticle, the former being again the most studied pathway and probably the most important in quantitative terms. However, more research is needed to elucidate the importance of each pathway and their respective roles and mechanisms in both the release and the deposition of oxygenated VOCs.
Emitted and revolatilized oxVOCs enter the atmospheric compartment in which they can react with ozone molecules, OH radicals, other VOCs, and nitrogen oxides. Otherwise, they may be degraded by ultra-violet (UV) radiation. Such transformations, however, are slow due to the low reactivity of short-chain oxVOCs, a fact that is illustrated by their relatively long half-lives ranging from a few hours (aldehydes) to 15 days (acetone). A long-range transport of oxVOCs on the wind is thus likely to occur and hence influence the atmospheric chemistry of distant regions.
The low reactivity of these compounds is derived from the fact that short-chained oxVOCs are themselves products of photolysis and the chemical reactions of a vast diversity of other VOCs present in the atmosphere. Currently, this secondary photochemical production from VOCs is thought to be the main atmospheric source of oxVOCs. Another related issue that needs further investigation is the balance between biogenic emission and photochemical production: sometimes the maximum reported emissions of oxVOCs take place when secondary atmospheric production is likely also to be at a maximum, e.g. at midday or in the afternoon when stomatal conductance, photosynthetic rate, transpiration, irradiation, and temperatures are high, and thus plant metabolic activity and oxVOCs volatilization are also high. However, if atmospheric mixing ratios control the gas exchange, and photochemical production increases the mixing ratios, then oxVOCs emissions should be hindered. Photochemical destruction of oxVOCs may partly offset photochemical production, although the long lifespan and low reactivity of oxVOCs may in fact ensure that this effect is of little import. These processes are not well understood and future research may well unravel some of these uncertainties.
In general, plants synthesize C1 oxVOCs during many growth and developmental processes such as seed maturation, cell expansion, cell wall degradation, leaf abscission, and senescence of plant tissues. C2 oxVOCs seem mainly related to responses to changes in the environment, above all during periods of stress (Kreuzwieser et al., 1999b). In this detailed overview, we will group the short-chained oxVOCs into acids, acetone, aldehydes and alcohols. Usually, the compounds within each group—especially aldehydes and acids—have been studied together due to the similarities in the sampling and analytic techniques involved.
Section snippets
Acids
Formic (HCOOH) and acetic (CH3COOH) acids are the most prominent organic acids emitted by vegetation (Kesselmeier and Staudt, 1999). In C3 plant leaves in the light, formic acid can be generated in its deprotonated form—formate—by the non-enzymatic decarboxylation of glyoxylate formed in photorespiration (Igamberdiev et al., 1999; Kesselmeier and Staudt, 1999; Hanson and Roje, 2001). In the dark, in nonphotosynthetic tissues and in C4 species its origin is not clear. In these cases, formic acid
Acetone
Acetone (CH3COCH3) is the simplest existing ketone. Within plant tissues, acetone can be produced by the cyanogenic pathway (activated to deter herbivores), leading to the production of hydrogen cyanide (HCN) and—as a byproduct—acetone. Another way in which acetone may be formed is via acetoacetate decarboxylation, a well-known reaction that occurs in certain soil bacteria and animals. For a detailed description of these pathways see Fall (2003).
In direct plant emission measurements (Table 3),
Aldehydes
The short-chain aldehydes emitted by plants are the C1 formaldehyde (HCHO) and the C2 acetaldehyde (CH3CHO). The formaldehyde origin within plants remains unclear. It seems to be a product of methanol oxidation, although its actual biochemical basis in plants is not known and other possible origins such as 5,10-methylene-tetrahydrofolate dissociation, glyoxylate decarboxylation or oxidative demethylation reactions have been proposed (Hanson and Roje, 2001). Acetaldehyde formation is known to be
Alcohols
The short-chain alcohols emitted by plants are methanol (CH3OH) and ethanol (CH3CH2OH). Methanol is a product of the demethylation of pectin during cell wall formation (biochemical details reviewed by Fall, 2003). Ethanol is produced in fermentative reactions when energy is obtained from glucose.
As in the case of acids, the high solubility of these alcohols ensures that their release is stomata-dependent (Macdonald and Fall, 1993; Nemecekmarshall et al., 1995; Schade and Goldstein, 2002) and
Final remarks
All these short-chain oxygenated VOCs have some common characteristics which set them apart from other widely studied VOCs such as isoprene and monoterpenes. For example, it is noticeable that their higher water solubility (low gas-aqueous phase partitioning coefficient, H) partly relates their emission to transpiration and makes it sensitive to changes in stomatal conductance. Compared to isoprenoids, they have a long atmospheric lifespan and so can affect tropospheric chemistry far from where
Acknowledgements
Our research was partly supported by ISONET (Marie Curie network contract MC-RTN-CT-2003 504720) from the European Union, by grants REN2003-04871, CGL2004-01402/BOS and CGL2006-04025/BOS from the Spanish Government, by a 2004 grant from the Fundación BBVA, and by a SGR 2005-00312 grant from AGAUR (Generalitat de Catalunya). Roger Seco gratefully acknowledges a FPI fellowship (BES-2005-6989) from MEC (Spanish Government).
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