Biogenic volatile organic compounds in the Earth system

Review

copy The Authors (2009) New Phytologist (2009) 183 27ndash51 27Journal compilation copy New Phytologist (2009) wwwnewphytologistorg 27

Blackwell Publishing LtdOxford UKNPHNew Phytologist0028-646X1469-8137 copy The Authors (2009) Journal compilation copy New Phytologist (2009)2859101111j1469-8137200902859xApril 2009002751Tansley reviewTansley review Tansley review

Tansley review

Biogenic volatile organic compounds in the Earth system

Jullada Laothawornkitkul Jane E Taylor Nigel D Paul and C Nicholas HewittLancaster Environment Centre Lancaster University Lancaster LA1 4YQ UK

Contents

Summary 27

I Introduction 27

II Regulation of BVOC emission 30

III Roles of BVOCs in the Earth system 32

IV BVOCs in a changing global environment 36

V Synthesis 44

Acknowledgements 44

References 44

Author for correspondenceC N HewittTel +44 (0) 1524 593 931Email nhewittlancasteracuk

Received 9 October 2008Accepted 13 March 2009

Summary

Biogenic volatile organic compounds produced by plants are involved in plantgrowth development reproduction and defence They also function as communicationmedia within plant communities between plants and between plants and insectsBecause of the high chemical reactivity of many of these compounds coupled withtheir large mass emission rates from vegetation into the atmosphere they have signi-ficant effects on the chemical composition and physical characteristics of the atmos-phere Hence biogenic volatile organic compounds mediate the relationship betweenthe biosphere and the atmosphere Alteration of this relationship by anthropogeni-cally driven changes to the environment including global climate change may perturbthese interactions and may lead to adverse and hard-to-predict consequences forthe Earth system

Abbreviations ACC 1-aminocyclopropane-1-carboxylic acid BVOC biogenic vola-tile organic compound FACE free-air CO2 enrichment IPCC IntergovernmentalPanel on Climate Change JA jasmonic acid MeJA methyl jasmonate MPAN per-oxymethacrylic nitric anhydride MeSA methyl salicylate PAN peroxyacetylnitrateSA salicylic acid SOA secondary organic aerosol

I Introduction

The Earth is a single and partially self-regulating system thatconsists of interlinked physical chemical and biologicalcomponents The terrestrial biosphere is one subsystem of thisand by acting as a source of biogenic volatile organic

compounds (BVOCs) to the atmosphere provides a stronglink between the Earthrsquos surface atmosphere and climateMost of these BVOCs are synthesized by one of three majorbiochemical routes the isoprenoid the lipoxygenase or theshikimic acid pathways (Feussner amp Wasternack 2002Dudareva et al 2006 Matsui 2006 Xiang et al 2007

New Phytologist (2009) 183 27ndash51 doi 101111j1469-8137200902859x

Key words atmospheric chemistry biogenic volatile organic compounds (BVOCs) climate change global warming plant defence plant volatiles tritrophic interaction

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Review28

Qualley amp Dudareva 2008) A number of low-molecular-weight (C lt 5) BVOCs are also emitted by plants for examplemethanol ethylene formaldehyde ethanol acetone andacetaldehyde (Kreuzwieser et al 1999 Fall 2003 Arguesoet al 2007) These pathways have been relatively well studiedand the routes of formation are now well understood (Fig 1)However the biochemical regulation and function of most ofthese compounds are not clearly known

BVOCs are released from above- and below-ground plantorgans In general flowers and fruits release the widest varietyof BVOCs with emission rates peaking on maturation(Dixon amp Hewett 2000 Knudsen et al 2006 Knudsen ampGershenzon 2006 Soares et al 2007) but leaves have thegreatest mass emission rates The vegetative parts of woodyplants are more likely to release diverse mixtures of terpenoidsincluding isoprene monoterpenes sesquiterpenes and somediterpenes (Owen et al 2001 Keeling amp Bohlmann 2006)whereas grass species emit relatively large amounts of oxygen-ated BVOCs and some monoterpenes (Kirstine et al 1998Fukui amp Doskey 2000) When plants are damaged theemissions of these compounds may be increased and otherso-called green leaf volatiles (C6 aldehydes and ketones) mayalso be produced (Fall et al 1999 Laothawornkitkul et al2008a) Biotic and abiotic stresses may also induce the pro-duction of some BVOCs such as terpenes methyl jasmonate(MeJA) and methyl salicylate (MeSA) from leaves themagnitude and quality of which depend on the type ofdamage (Takabayashi et al 1994 Seo et al 2001 Mithoferet al 2005 Laothawornkitkul et al 2008a) The majorclasses of BVOCs the major groups of BVOC-emittingplants and estimates of current and future fluxes into theatmosphere are shown in Table 1

The single most important BVOC in the Earth system isprobably isoprene (C5H8 2-methyl-13-butadiene) Its pro-duction and emission by plants were first described bySanadze (1956) and its effect on the physics and chemistry ofthe atmosphere was first described by Went (1960) (Table 2)Notwithstanding the dominance of isoprene the biosphereproduces and emits hundreds if not thousands of reactiveBVOCs into the atmosphere Of these probably a few tens toa hundred specific species have significant and discernibleeffects in the atmosphere Since the 1960s over 1000 peer-reviewed papers have been published on the biosynthesis roleand function of BVOCs in the biosphere and atmosphere Itis now clear that these compounds have important effectswithin plants between plants between plants and otherorganisms and in the atmosphere at the local regional andglobal scales

How and why plants synthesize BVOCs and what are theireffects or functions are of interest to at least three distinctscientific communities Atmospheric chemists are interestedin BVOC emissions in terms of their effects on atmosphericcomposition and on the atmospherersquos chemistryndashclimate systemPlant biologists are interested in the functions of BVOCs in Ta

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he Authors (2009)

New

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29

Fig 1 Simplified description of the metabolic pathways of biogenic volatile organic compound (BVOC) biosynthesis in leaves andor flowers and roots Volatile compounds are shown inside oval-shaped areas and the enzymes responsible for BVOC synthesis are shown in boxes (adapted from Dudareva et al 2006) ACC 1-aminocyclopropane-1-carboxylic acid ADH alcohol dehydrogenase AdoMet S-adenosyl-L-methionine ALDH aldehyde dehydrogenase AOC allene oxide cyclase AOS allene oxide synthase B2H benzoic acid-2-hydroxylase BSMT S-adenosyl-L-methioninebenzoic acidsalicylic acid carboxyl methyltransferase CoA coenzyme A DAHP 3-deoxy-D-arabino-heptulosonate DMAPP dimethylallyl diphosphate FPP farnesyl diphosphate FPPS FPP synthase F6P fructose-6-phosphate GA-3P glyceraldehyde-3-phosphate GGPP geranylgeranyl diphosphate GGPPS GGPP synthase GLU β-glucosidase GPP geranyl diphosphate GPPS GPP synthase HCN hydrogen cyanide HG homogalacturonic acid HNL hydroxynitrile lyase HPL fatty acid hydroperoxide lyase IGL indole-3GP lyase indole-3GP indole 3-glycerol phosphate IPP isopentenyl diphosphate IspS isoprene synthase JA jasmonic acid JMT jasmonic acid carboxyl methyltransferase LOX lipoxygenase MeBA methyl benzoate MeJA methyl jasmonate MEP 2-C-methyl-D-erythritol 4-phosphate MeSA methyl salicylate Met methionine MOX methanol oxidase MVA mevalonate OPDA 12-oxo-phytodienoic acid PAL phenylalanine ammonia lyase PDC pyruvate decarboxylase PEP phosphoenolpyruvate Phe phenylalanine PMEs wall-localized pectin methylesterases SA salicylic acid SAMT S-adenosyl-L-methioninesalicylic acid carboxyl methyltransferase TCA tricarboxylic acid or citric acid TPSs terpene synthases

Tansley review


Review30

the biosphere ie their roles in plant biology and ecologyEntomologists are interested in their role as signalling agents

Several lines of current evidence have demonstrated thetight interconnections that exist between the roles of BVOCsin the biosphere and the atmosphere but there has been littlecommunication between these research areas to date Thisreview therefore aims to summarize and identify gaps in ourcurrent knowledge of BVOCs in the Earth system withparticular emphasis on their functions It also highlights thestrong interlinkages between the roles of BVOCs in the bio-sphere and the atmosphere and hence demonstrates how anintegration of knowledge and resources between the biologicaland atmospheric chemistry research fields is necessary toadvance our understanding of the Earth system

As noted above an enormously wide range of BVOCs aresynthesized and emitted into the atmosphere by plants Com-pounds which may be described as BVOCs but which arespecifically excluded from this review include dimethyl sulphideand methane Dimethyl sulphide is known to be very importantin the Earthrsquos climate system (Charlson et al 1987) but isproduced by oceanic not terrestrial plants Methane is similarlyimportant in the climate system but reports of its directbiosynthesis by terrestrial plants (Keppler et al 2006) remaincontroversial We therefore focus on nonmethane volatileorganic compounds produced by terrestrial plants

II Regulation of BVOC emission

Little is known about the regulation of BVOC synthesis rateswith probably more than 90 of the genes involved in theirbiosynthesis still unidentified There is evidence to suggest

that BVOC biosynthesis is largely controlled at the level of geneexpression microarray analyses show that BVOC biosynthesisgenes are upregulated following herbivory via jasmonic acid( JA) salicylic acid (SA) and ethylene signalling pathways(Hermsmeier et al 2001 Kant et al 2004 Ralph et al2006) The changes in expression of the genes involved inBVOC synthesis positively correlate with their emission ratesand this control leads to the spatial (local and systemic) andtemporal pattern of their emissions (Dudareva et al 2003Arimura et al 2004 Underwood et al 2005) Howeveremissions of many BVOCs are also strongly correlated withenzyme activities under both optimum and stress conditions(Kuzma amp Fall 1993 Loreto et al 2001a Fischbach et al2002) This indicates that transcriptional regulation may notbe the only controlling factor and hence post-transcriptionalpost-translational and enzyme regulatory mechanisms leadingto changes in protein levels or enzyme activities remain to beexplored as a further means of control

The availability of substrate for the final reaction leading toBVOC synthesis is also a crucial rate-limiting factor Someenzymes with broad substrate specificities can generate differenttypes of product depending on the level of supplied substrates(Negre et al 2003 Boatright et al 2004 Pott et al 2004)Genetic manipulation resulting in the redirection of cytosolicor plastidic isoprenoid precursors elevates BVOC productionin transgenic tobacco plants (Wu et al 2006) These studieshighlight the importance of precursor fluxes through the entirebiosynthetic pathway in the regulation of BVOC productionand emission

The emissions of BVOCs from flowers and from undamagedand herbivore-damaged leaves often show distinct diurnal or

Table 2 Keystone publications on the role of biogenic volatile organic compounds (BVOCs) in the atmosphere (1) and biosphere (2)

Finding Reference

Isoprene is emitted from plants Sanadze (1956)1

BVOC emissions from forests can lead to aerosol formation and have environmental effects Went (1960)1

An airborne cue from herbivore-damaged plants induces chemical defence in neighbouring undamaged plants

Baldwin amp Schultz (1983)2

BVOCs emitted from damaged plants Dicke (1986)2

BVOCs contribute to photochemical smog and should be considered when developing air pollutant control strategies

Chameides et al (1988)1

Airborne methyl jasmonate induces plant defence and interplant communication occurs between plants from different species

Farmer amp Ryan (1990)2

First review of role of BVOCs in the atmosphere Fehsenfeld et al (1992)1

Global emission of BVOCs from terrestrial plants is gt 1000 Tg yrndash1 Guenther et al (1995)1

Isoprene emission protects photosynthesis from transient heat stress Sharkey amp Singsaas (1995)12

Plants can actively produce BVOCs in response to herbivory Pareacute amp Tumlinson (1995)2

Induced BVOCs repel herbivores and are produced at night De Moraes et al (1997)2

BVOCs play a role in indirect defence against herbivory in nature Kessler amp Baldwin (2001)2

BVOCs can protect plants from oxidative stress Loreto et al (2001b)12

Isoprene oxidation leads to secondary organic aerosol formation Claeys et al (2004)1

BVOCs prime neighbouring plants against herbivore attacks Engelberth et al (2004)2

Isoprene synthesis can be under circadian control Wilkinson et al (2006)1

Isoprene influences plantndashherbivore interactions and tritrophic interactions Laothawornkitkul et al (2008c) Loivamaki et al (2008)12

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Review 31

nocturnal patterns (Dudareva et al 2005 Wilkinson et al2006 Loivamaki et al 2007) This may be the result ofcircadian regulation of substrate availability transcription orenzyme activity (Yakir et al 2007) As yet there is little infor-mation on the molecular mechanisms of circadian control ofBVOC emissions As different BVOCs may result from differentbiosynthetic pathways it is not yet clear how the controls ofthese pathways are co-ordinated to give rise to a specificmixture of BVOCs

The emission rates of all BVOCs also depend at least inpart on leaf temperature which may influence the availabilityof substrate and the activity of rate-limiting enzymes Howeveremission rates from leaves are not only limited by physiologicalfactors but also by physicochemical constraints caused bytemperature stomatal conductance and leaf structure (Niinemetset al 2004) These limit volatility (determined by gas phasepartial pressure and aqueous and lipid phase concentrations)diffusion through the gas aqueous and lipid phases within theleaves and diffusion from the leaf surface Gas phase diffusionat the leafndashair interface determined by stomatal conductancecan influence significantly the synthesis and emission ofBVOCs with low Henryrsquos law constants such as formic acidformaldehyde and methanol This does not apply to the lesswater-soluble compounds such as isoprene and the nonoxy-genated terpenes (Niinemets et al 2004) the emission ratesof which are independent of stomatal conductance Soil moisture

availability carbon dioxide (CO2) concentration and otherenvironmental stresses including ozone (O3) concentrationmay therefore affect the production and emission of someBVOCs through their effects on stomatal conductance

The photon flux density determines the emission rates ofsome BVOCs This largely depends on the presence of storagecompartments in leaves Some plants such as Pinus AbiesEucalyptus and those in the family Rutaceae store BVOCs inspecialized storage compartments (for example resin ductscavities oil glands or glandular trichomes) whereas others suchas some oaks (Quercus spp) do not (Loreto et al 1998a) In theabsence of such storage compartments only small and tem-porary pools of BVOCs can be nonspecifically stored in planttissue in the lipid phase (nonoxygenated lipophilic BVOCs)or in the aqueous phase (oxygenated lipophobic BVOCs)The absence of these compartments results in emission rates beingclosely coupled to incident light intensity (Staudt amp Bertin1998) In plants with BVOC storage compartments the emis-sions are mostly light independent and are closely coupled toleaf temperature because BVOC volatilization comes fromlarge stored pools (Tingey et al 1980) Some compoundsfor example isoprene are not stored at all and are highly volatiletheir emission rate depends on temperature and light Therelationships between light and temperature control ofbiosynthesis rates intraplant storage capacity and light andtemperature control of emission rates are shown in Fig 2 These

Fig 2 Schematic representation of the relationships between light and temperature controls of biogenic volatile organic compound (BVOC) synthesis rates (I) intraplant storage capacity and light and temperature controls of BVOC emission rates (E) (modified with permission from Grote amp Niinemets 2008) BVOC synthesis rates response to light and temperature based on enzyme kinetic expressions whereas BVOC evaporation from storage pools depends on diffusion resistances and compound physicochemical characteristics Therefore BVOC emissions from large stores (eg most monoterpenes) are not dependent directly on the synthesis rate (I ne E) but on diffusion resistances and compound physicochemical characteristics Hence the photon flux density does not influence the emission rate However BVOC emissions from small storage pools (eg isoprene) depend directly on the synthesis rate (I = E) The cross-sections are for a representative needle of monoterpene-emitting species Pinus radiata (the magnifications shows the resin duct) and for a leaf of isoprene-emitting species Populus tremula (the magnification outlines the chloroplasts where isoprene is synthesized) The scale bars are 01 mm in allcases except for chloroplasts (microm) The images were non-stained (P tremula) or stained with toluidine blue (P radiata)

Tansley review


Review32

relationships are the basis of recently developed models ofBVOC emission rates (for example Grote amp Niinemets 2008)

III Roles of BVOCs in the Earth system

BVOCs play numerous roles in the Earth system and provideinterlinkages between its biological chemical and physicalcompartments as shown schematically in Fig 3

1 Roles of BVOCs in the biosphere

BVOCs as signalling compounds within plants The roles ofMeJA ethylene and MeSA in plants are very diverse and havebeen reviewed extensively (Raskin 1992 Creelman amp Mullet1997 Bleecker amp Kende 2000) Here we focus on their rolesin the regulation of BVOC production

MeJA and related compounds MeJA and JA are ubiquitouslydistributed throughout the plant kingdom and are collectivelycalled jasmonates (Creelman amp Mullet 1997) They areinvolved in inducing the production of fruit ripening-relatedBVOCs including ethylene (Kondo et al 2007 Ziosi et al2008) Jasmonate treatment induces the expression of the1-aminocyclopropane-1-carboxylic acid (ACC) synthasegene (Kondo et al 2007) whereas the internal ethyleneconcentration influences the production of MeJA-mediatedvolatiles (Kondo et al 2005) This suggests that jasmonateand ethylene signalling pathways may interact and modulateBVOC production in a range of fruits

JA-dependent signalling also mediates the synthesis ofBVOCs from vegetative plant parts (van Poecke amp Dicke2002 Ament et al 2004 Girling et al 2008) some of whichcan attract parasitoidspredators of herbivores (Thaler 1999

Fig 3 Schematic diagram summarizing the current understanding of the roles of biogenic volatile organic compounds (BVOCs) in the Earth system BVOCs exert their roles in the biological chemical and physical components of the Earth system and hence provide a connection between the biosphere and the atmosphere The use of three compartments labelled biology chemistry and physics is not intended to imply that chemical and physical processes do not occur within the biosphere SOA secondary organic aerosol night-time

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Review 33

Thaler et al 2002a van Poecke amp Dicke 2002) Whendamaged by herbivory some plants also release the volatilecis-jasmone a compound related to JA and MeJA (Loughrinet al 1995 Lou amp Baldwin 2003 Roumlse amp Tumlinson 2004)Cis-jasmone may be another plant regulator as its exogenousapplication increases plant resistance to aphids (Bruce et al2003a) and elevates plant BVOC production and attractionto the parasitoid Aphidius ervi (Birkett et al 2000 Bruceet al 2003b Bruce et al 2008) It induces the expression ofdefence genes which are independent from those induced byMeJA suggesting that these two compounds may producedistinct signalling cascades (Bruce et al 2008)

Although various studies have shown that JA-dependentsignalling plays a central role in the induction of BVOCemission (Ament et al 2004 Girling et al 2008 Herdeet al 2008) it is unclear which cell types are responsible inmediating this pathway and in what form and how far theJA-dependent signals can travel in plants However morerecent experiments have suggested that amino acid conjugatesof JA especially jasmonoyl-isoleucine are essential in JA-dependent signalling (Staswick 2008)

Ethylene Ethylene can diffuse freely from cell to cell acrossmembranes and is a potent regulator in plants Bothexogenous and post-pollination-derived ethylene downregulatefloral volatile production by mediating the expression andactivity of enzymes involved in BVOC synthesis (Negre et al2003 Underwood et al 2005) This may help plants tomodulate their resource allocation because once flowers arepollinated floral scents have accomplished their role Incontrast with its role in flowers ethylene upregulates volatileproduction in ripening fruits and positively regulates theexpression of various enzymes involved in aroma formation(Yahyaoui et al 2002 Manriacutequez et al 2006) Transgenicfruit with impaired ethylene production produces much lessripening-related volatiles (Bauchot et al 1998) indicatingthat such processes are regulated by developmental factors thatmust be coordinated with ethylene synthesis and perception

Vegetative plant parts may also release ethylene as part of aherbivore wounding response (Arimura et al 2002) In generalethylene enhances BVOC production and emission but thisis dependent on the type of BVOC (Horiuchi et al 2001Schmelz et al 2003ab Arimura et al 2008) Several lines ofevidence have indicated that ethylene and JA synergisticallyregulate BVOC synthesis (Horiuchi et al 2001 Schmelzet al 2003ab Arimura et al 2008) However the interplaybetween JA- and ethylene-dependent signals is not yet clearStaswick amp Tiryaki (2004) have suggested that an unknownenzyme might be responsible for conjugation between JA andACC leading to an inactive JAndashACC conjugate with subse-quent hydrolysis of such a conjugate yielding JA and ACCavailable for the corresponding signalling routes Ethylenemay also regulate the JA pathway by influencing the expressionof allene oxide synthase involved in JA biosynthesis

(OrsquoDonnell et al 1996 Laudert amp Weiler 1998 Sivasankaret al 2000)

MeSA MeSA is the volatile counterpart of SA The SAsignalling cascade is involved in the induction of both localand systemic defences (systemic acquired resistance) to a broadrange of pathogens and some insects (Bostock 1999 Dempseyet al 1999 Vasyukova amp Ozeretskovskaya 2007) The mostrecent grafting study using tobacco plants with different geneticbackgrounds has provided unambiguous evidence that MeSAis the mobile signal that is required for systemic resistanceinduction in tobacco (Nicotiana tabacum) (Park et al 2007)

SA- and JA-dependent signalling are required for defenceactivation against herbivores and pathogens and are generallyknown to function antagonistically (Thaler et al 2002bc)Although JA plays a central role in the production of inducedBVOCs and mediates MeSA production (Ament et al 2004)the presence of SA or SA-derived signals is also required forthe production of herbivore-induced volatiles that mediate anindirect defence response (see below) (van Poecke amp Dicke2002 Girling et al 2008) The balance between the JAethylene and SA signalling cascades seems to help plants todiscriminate the quality and quantity of tissue damage and thuscontrol specific blends of herbivore-induced volatiles (Ozawaet al 2000 Engelberth et al 2001 Girling et al 2008)

Roles of BVOCs in plant reproduction To ensure reproductivesuccess flowering plants release a myriad of BVOCs fromtheir flowers in order to attract pollinators (Wright et al 2005)and to assist them to identify conspecific flowers whilstforaging (Andersson et al 2002) The different BVOC mixturesand their relative abundances make the scent bouquet releasedby a particular flower characteristic of that bloom (Knudsenamp Tollsten 1993 Knudsen et al 2006) This specificity maytherefore be used by pollinators to distinguish a particularflower within a single species and across plant species and leadthem to specific food sources (Andersson et al 2002 Schiestlamp Ayasse 2002 Wright et al 2005)

There is strong evidence indicating that flowers competefor pollinator visitors (Basra 2006) Exogenous application ofisoprene promotes early flowering of barley oilseed rape andArabidopsis (Terry et al 1995) These observations have led tothe hypothesis that isoprene emission may disrupt pollinationin competing plants and so confer competitive advantage toisoprene emitters Further studies are required to test this inexperimental and natural systems

Following pollination fruits also produce a range ofBVOCs that change according to their developmental andripening stages (Goff amp Klee 2006) Fruit odour can attractseed dispersers and allows them to locate and discriminatebetween ripe and unripe fruits even within the same plantspecies (Luft et al 2003 Hodgkison et al 2007) BVOCstherefore play a role at all stages of plant reproduction anddevelopment

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Roles of BVOCs in plant defence against biotic stresses SomeBVOCs released from flowers leaves and roots may protectplant organs from pathogens by their antimicrobial or antifungalactivity (Croft et al 1993 Shiojiri et al 2006) They can alsodirectly affect the physiology and behaviour of herbivoresthrough their toxic repellent and deterrent properties (DeMoraes et al 2001 Vancanneyt et al 2001 Aharoni et al2003 Laothawornkitkul et al 2008c) Some such as 4812-trimethyl-13(E)7(E )11-tridecatetraene and 48-dimethyl-13(E )7-nonatriene serve as information conveyors that canprovide communication between and within trophic levelsFoliage may emit blends of herbivore-induced BVOCs thatattract insect or acarid predators and parasitoids as firstdemonstrated by Dicke (1986) Since then it has been shownthat BVOCs serve several functions in plant ecology (Table 2)Recently it has been demonstrated that isoprene influencesplantndashherbivore interactions by deterring herbivores fromfeeding (Laothawornkitkul et al 2008c) and by interfering intritrophic interactions (Loivamaki et al 2008)

Tritrophic communication is not restricted only to above-ground plant parts but may also occur below ground Forexample insect attack on maize roots triggers the release of asesquiterpene (E )-β-caryophyllene which attracts nematodesthat prey on insect larvae (Rasmann et al 2005) Howeverlittle is known at present about the role of BVOCs in therhizosphere and in soil ecology This is at least in part a resultof the difficulty of conducting experiments and field observa-tions on soil without disturbing soil structure and root systems(Hayward et al 2001 Owen et al 2007)

Some BVOCs for example MeJA (Farmer amp Ryan 1990)MeSA (Shulaev et al 1997) some green leaf volatiles (Engel-berth et al 2004 Farag et al 2005) and some terpenes(Arimura et al 2002) can serve as airborne signals betweenplants (Engelberth et al 2004 Kessler et al 2006 Ton et al2007) and between organs within the same plant (Karbanet al 2006 Frost et al 2007 Heil amp Silva Bueno 2007)This communication can occur between neighbours of thesame or different species (Dolch amp Tscharntke 2000 Kessleret al 2006) On perception by receiver plants these BVOCsignals can directly activate herbivore defence mechanisms ormay prime a subset of defence-related genes for earlier andorstronger induction on subsequent defence elicitation (Arimuraet al 2000 Engelberth et al 2004 Kessler et al 2006 Frostet al 2007 Ton et al 2007)

Molecular chemical and behavioural assays show thatVOC-induced priming which targets a specific subset ofJA-inducible genes leads to improvements in both direct andindirect defences (Ton et al 2007) However the reliability ofthis mechanism varies For example the BVOCs released byManduca sexta-infested wild tobacco plants (Nicotiana attenuata)fail to prime neighbouring N attenuata for defence (Pascholdet al 2006) but BVOCs emitted by mechanically damagedsagebrush (Artemesia tridentata tridentata) can primeN attenuata against subsequent attack by M sexta (Kessler

et al 2006) By contrast communication among silver sage-brush (Artemesia cana) individuals does not lead to increasedresistance to herbivory in receiver plants (Shiojiri amp Karban2008) What causes this variability requires further explanationthere would seem to be no benefit for damaged plants to warntheir neighbours when they are competing for limited resourcesin a local environment One possible explanation is thatplants might have evolved such communication for their ownuse namely for communication within an individual plant asBVOC concentrations in air decrease rapidly with distancefrom source (Karban et al 2006)

Plant resistance mechanisms can be induced or primed byBVOCs released from mechanically damaged neighbouringplants (Kessler et al 2006 Shiojiri amp Karban 2006) or bysuch damage within the same plant (Karban et al 2006)This raises several questions (i) can plants distinguishmechanical damage caused by biotic factors (eg pathogens orherbivores) vs abiotic factors (eg hail and strong wind) andif so how and (ii) how do plants discriminate a lsquostressrsquo signalfrom background BVOCs in heterogeneous and changingenvironments A mechanistic understanding of the nature ofBVOC receptors and the cells responsible for mediating thesignal transduction pathways requires further investigation asdo the ecological consequences of BVOC-induced resistanceand priming Such knowledge could have potential in thefuture development of sustainable agricultural practices

Roles of BVOCs in plant defence against abiotic stressesIsoprene emission might serve as a metabolic safety valve todissipate excess energy (Sanadze 2004) and metabolites(Rosenstiel et al 2004) However Sharkey et al (2007) arguedthat this does not explain the random distribution of theisoprene emission trait across the plant kingdom or differencesin isoprene emission capacity at the canopy level In additionthere are probably other energy-consuming mechanisms inplants that are more effective than isoprene synthesis

Isoprene and monoterpenes can protect the photosyntheticapparatus of plants from damage caused by transient high-temperature episodes and may prevent a progressive reductionin photosynthetic capacity (Singsaas et al 1997 Loreto et al1998b Behnke et al 2007) (Fig 3) Several mechanisticexplanations of this phenomenon have been proposed (Sharkeyamp Yeh 2001) When thylakoid membranes become leaky athigh temperature isoprene may enhance hydrophobic inter-actions and so strengthen the thylakoid membrane It mightalso help more generally to enhance the integrity of membranesand protein complexes Recent mechanistic evidence supportsthis hypothesis by showing that isoprene can directly protecta model phospholipid membrane from heat spikes (Siwko et al2007)

Despite early work which suggested that isoprenendashO3interactions may damage plant tissue (Hewitt et al 1990) itis now known that isoprenoids function as antioxidants inleaves and confer protection against O3-induced oxidative

Tansley review


Review 35

stress and singlet oxygen accumulation during photosynthesis(Loreto et al 2001b 2004 Affek amp Yakir 2002 Vickerset al 2009) Isoprenoids may perhaps exert their protectiveaction at the membrane level by quenching hydrogen peroxideformed in leaves and by reducing lipid peroxidation of cellularmembranes caused by oxidants (Loreto amp Velikova 2001)and may interfere with the molecular signalling that leads toprogrammed cell death (Velikova et al 2005) This processmight counteract the hypersensitive response (for examplerapid cell death in response to pathogen infection) that requiresinitiation by reactive oxygen species This suggests possibleantagonistic interactions between the hypersensitive responseand the antioxidant capacity of BVOCs Clearly how plantsare able to balance their defence strategies in response to bothabiotic and biotic stresses is complicated and the role playedby BVOCs remains to be determined

2 Roles of BVOCs in the atmosphere

Estimates of the global flux of BVOCs from the biosphere tothe atmosphere are rather uncertain but may be 700ndash1000times 1012 g (C) per year (Table 1) There are large uncertaintiesassociated with these estimates although the remotely sensedconcentrations of BVOC oxidation products in the atmosphereinverted and modelled using an atmospheric chemistrytransport model are now beginning to constrain these estimates(for example the use of formaldehyde observations to constrainisoprene emission estimates Guenther et al 2006) In anyevent the BVOC flux far exceeds the global anthropogenicVOC flux Although very many BVOC species have beenidentified from plants as mentioned above much of theglobal flux and subsequent effect on atmospheric chemistry isprobably caused by a relativity small number of compoundsIsoprene makes the largest contribution followed by themonoterpene family (Levis et al 2003) Some oxygenatedcompounds such as methanol acetone and acetaldehydemay also be important in the atmosphere (Guenther et al1995 Kesselmeier amp Staudt 1999 Fuentes et al 2000)Estimating the emission rates of C15 sesquiterpenes andrelated compounds is difficult as they present particularanalytical challenges because of their reactivity and low vapourpressures they are important precursors to secondary organicaerosols (SOAs) (Hoffmann et al 1997 Bonn amp Moortgat2003)

Oxidation of BVOCs in the atmosphere When reactiveBVOCs are released into the atmosphere they are subject tooxidation reactions potentially leading to the ultimate productsof CO2 and water (Fig 3) Many of their intermediate partiallyoxidized products are water soluble and hence may beremoved from the atmosphere by wet deposition (Fehsenfeldet al 1992) or may have lower vapour pressures than theprimary compounds and hence enter the particle (solid oraerosol) phase and be removed from the atmosphere by wet

and dry deposition thereby removing reactive carbon fromthe atmosphere The relative importance of this process is notcurrently possible to quantify but requires a better understandingof the yield of SOAs from BVOCs

Hydroxyl radicals (OH) dominate the daytime chemistryof the troposphere and the oxidation of VOCs is primarily ini-tiated by reaction with them OH is itself produced in part bythe photolysis of tropospheric O3 and the subsequent reactionof electronically excited atomic oxygen O(1D) with watervapour The initial products of the VOCndashOH reaction can befurther oxidized to form peroxy radicals (RO2) In the presenceof sufficient oxides of nitrogen (NOx = NO plus NO2) forexample in polluted air these RO2 species may oxidize NO toNO2 which can in turn be photodissociated leading to theformation of O3 and the regeneration of OH (Fig 3) In cleanair with low NOx concentrations RO2 may recombine orreact with HO2 to form less reactive peroxides which may beremoved from the atmosphere by deposition processes (Feh-senfeld et al 1992) which lead to the net consumption of O3Recent field observations of OH and BVOC concentrationssupported by laboratory experiments have suggested that ourunderstanding of BVOC oxidation processes may in fact beinadequate and that in low-NOx conditions more regener-ation of OH by these reactions may occur than previouslythought (Lelieveld et al 2008) This has significant implica-tions for the understanding of the oxidant budget of air receivinglarge BVOC inputs for example in the boundary layer abovetropical and boreal forests However this important result hasyet to be verified and further field laboratory and modellingstudies are required to test it

As well as OH O3 can itself act as an oxidant for unsatu-rated BVOCs The addition of O3 to carbonndashcarbon doublebonds leads to the formation of ozonides which are unstableand undergo rapid decomposition This can generate organicfree radicals that can form OH and RO2 so mediating the O3budget of the troposphere as outlined above

At night when OH concentrations are effectively zeroBVOC oxidation may be driven by reaction with the nitrateradical (NO3) (Wayne 2000) (Fig 3) Because of its rapidreaction with NO and its short lifetime (sim5 s) in sunlight as aresult of photolysis NO3 concentrations are low during theday but can increase substantially at night This may lead tothe removal of BVOCs that would otherwise be available fordaytime O3 formation However the reaction rates of NO3with most BVOCs are quite low (one-fifth of that with OHin the case of isoprene) and so reaction with OH is normallythe dominant route of oxidation

Although the details of BVOC oxidation reactions are notyet known with complete certainty it is clear that BVOC oxi-dation may affect the oxidative capacity of the troposphereand hence influence the rate of oxidation formation andconcentration of other trace gases (see below) (Fehsenfeldet al 1992 Wayne 2000 Atkinson amp Arey 2003 Lelieveldet al 2008)

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Review36

Gas phase chemistry of BVOCs As mentioned above theoxidation of BVOCs by OH can in the presence of sufficientNOx lead to the formation of O3 in the troposphere bydisruption of the photochemical steady state of O3 (ie allowthe oxidation of NO to NO2 without removal of an O3molecule) and so cause elevated O3 concentrations (Fig 3)NOx emissions may result from fossil fuel combustion fertilizerapplication and biomass burning as well as natural productionby lightning As tropospheric photochemistry is highly nonlinearwith respect to the emissions of O3 precursors modelling isrequired to determine the effects of BVOC emissions on O3concentrations in the troposphere (Fowler et al 2008)

Since the seminal work of Chameides et al (1988) it hasbeen recognized that BVOC emissions may be importantprecursors of photochemical smog and regional-scale O3production Furthermore because OH is the principal oxidantof methane the third most important greenhouse gas in theatmosphere (after water vapour and CO2) emissions of BVOCsmay increase the atmospheric lifetime of methane and soindirectly influence the Earthrsquos radiation balance (Wuebbleset al 1989) The resulting changes in climate may in turndirectly and indirectly affect BVOC emission rates potentiallyestablishing a positive feedback in the climate system Thedevelopment of next-generation coupled BVOC emissionndashatmospheric chemistryndashclimate models is required before themagnitude of this effect can be constrained

Although carbon monoxide (CO) is emitted directly byliving senescing and dead leaves (Tarr et al 1995) theoxidation of BVOCs also contributes significant amounts ofCO to the atmosphere (Hatakeyama et al 1991 Fehsenfeldet al 1992 Bergamaschi et al 2000 Griffin et al 2007)CO influences the oxidative capacity of the atmosphere in thesame way as isoprene by functioning as a sink for OH (Loganet al 1981) Hence the oxidation of CO can act as a sourceor sink of O3 depending on the availability of NOx Oncegenerated CO can be transported over large distances becauseof its relatively long atmospheric lifetime of several monthsand hence BVOCs can in this way influence atmosphericchemistry on the global scale (Fehsenfeld et al 1992 Lerdauet al 1997 Lerdau amp Slobodkin 2002)

Atmospheric oxidation of BVOCs and their primaryoxidation products (eg methyl vinyl ketone and methacroleinin the case of isoprene) can in the presence of NOx result inthe formation of organic nitrates including peroxyacetylnitrates(PANs) and peroxymethacrylic nitric anhydrides (MPANs)(Fehsenfeld et al 1992) PANs and MPANs have longeratmospheric lifetimes than NOx (days to months) and hencecan be transported over greater distances allowing them to actas carriers of reactive nitrogen (Fig 3) Once thermallydecomposed in warmer air they release NOx (Fehsenfeldet al 1992 Poisson et al 2000) resulting in an increase inNOx concentrations in areas without local NOx sources Thisprocess may markedly alter atmospheric composition andchemistry and lead to O3 formation in remote areas PANs

MPANs and other organic nitrates may be lost by wet depo-sition (Neff et al 2002) removing reactive nitrogen from theatmosphere

Influence of BVOCs on aerosol formation BVOCs not onlyinfluence gas phase atmospheric chemistry but can also leadto the formation of SOAs (Fig 3) The mechanisms by whichBVOC oxidation may lead to SOAs in clean air are still notfully understood (Kulmala 2003) but it is clear that BVOCoxidation products generally have lower vapour pressures thanthe primary compounds and so may more readily condenseon pre-existing molecular clusters (Joutsensaari et al 2005)Laboratory studies and field observations suggest that terpenesand sesquiterpenes emitted by vegetation may be significantsources of SOAs (Leaitch et al 1999 Joutsensaari et al2005) with yields as high as 80 (Hoffmann et al 1997)Oxidation of isoprene also produces SOAs (Claeys et al2004 Meskhidze amp Nenes 2006) However recent fieldobservations over tropical forests have not always foundsignificant SOA production to the degree expected (Rizzoet al 2006) indicating that further work is needed in this area

Aerosols directly affect climate by scattering solar radiationThey also indirectly alter the Earthrsquos radiative balance by actingas cloud condensation nuclei changing cloud albedo and thedegree of cloud cover so potentially leading to net cooling ofthe Earthrsquos surface during the day Although it is known thata substantial fraction of the aerosol particles in remote regionsis organic material and that the oxidation of BVOCs maylead to the formation of SOAs it is not yet clear how importantis SOA formation in altering the climate system Increasedcloud cover may also reduce the occurrence of low night-timesurface temperatures which can damage plants (Hayden1998) The possibility that SOA formation from BVOCemissions cools the Earth and so moderates temperature-dependent BVOC emission from plants ndash and other similarfeedbacks in the Earth system ndash is the focus of much currentresearch Hence there is the potential for feedback betweenBVOC emissions SOA and climate

IV BVOCs in a changing global environment

In the sections above we have described the impact ofBVOCs on the Earthrsquos environment We now turn toaddressing how changes in environmental conditions mayaffect BVOC production As the Earthrsquos biosphere andatmosphere change as a result of both natural processes andhuman activities BVOC emissions from the terrestrialbiosphere to the atmosphere will change with the potential tocause feedbacks so potentially exacerbating the effects of changeon the environment Understanding how BVOC emissionsrespond to future environmental change will help us to predictthe future impacts of BVOCs The ultimate goal of thisresearch is to build comprehensive predictive models of theEarth system

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Review 37

1 Atmospheric CO2 concentration and BVOC emissions

The CO2 concentration in the atmosphere has risen byapproximately 35 from pre-industrial times to the presentand is predicted to double within the 21st century[Intergovernmental Panel on Climate Change (IPCC) 2007]Elevated CO2 concentrations have been shown to increase(Sharkey et al 1991 Staudt et al 2001) decrease (Sharkeyet al 1991 Loreto et al 2001a Rosenstiel et al 2003Possell et al 2004 Vuorinen et al 2004c Wilkinson et al2008) or have no significant effects (Penuelas amp Llusia 1997Constable et al 1999 Buckley 2001 Centritto et al 2004)on BVOC production and emission at the whole plant shootor leaf levels Various factors including plant species ageexperimental duration and CO2 concentration may explainthese contrasting results Limitations in experimental designand implementation may also cause confounding resultsGlasshouses (Penuelas amp Llusia 1997 Staudt et al 2001Possell et al 2004) artificially illuminated controlled environ-ment chambers (Vuorinen et al 2004c Wilkinson et al2008) open-top and closed solar domes (Buckley 2001Loreto et al 2001a) and free-air CO2 enrichment (FACE)facilities (Centritto et al 2004) have all been used to studythe effect of elevated CO2 on BVOC emissions The sizelimitation of most experimental facilities (except FACE) meansthat young small pot-grown plants are usually used Theresulting limited rooting volume may diminish plant responsesto elevated CO2 by both nutrient exhaustion (Korner 2003)and root compaction (Thomas amp Strain 1991) Solar domesand other chambers may influence vegetation growth bycausing differences in aerial microclimate inside the chamber(Murray et al 1996) Despite these problems on balance itseems that increasing CO2 causes a decrease in isopreneemissions on a leaf surface area basis but that this might beoffset by increases in emissions as a result of increasing vegetationproductivity and leaf area growth caused by elevated CO2(Possell et al 2005 Arneth et al 2007)

Although growth under elevated CO2 concentrationsincreases leaf foliar density BVOC emissions from most plantcanopies are limited by light intensity (Sharkey et al 1996Guenther et al 2006) and temperature (Monson et al 1992Sharkey et al 1996) Thus the increase in shading associatedwith increased leaf area index might also directly affect canopy-scale emission rates (Possell et al 2005 Guenther et al2006) This should be taken into account when enclosureexperiments are extrapolated to the canopy scale

2 Global warming and BVOC emissions

Climate models suggest that during the 21st century themean global temperature will increase by 1ndash6degC (with a bestestimate of 2ndash3degC) (IPCC 2007) This increase intemperature will directly affect plant biochemical activity and

the length of the active growing season (Myneni et al 1997)Emissions of BVOCs are strongly temperature dependentbecause higher temperatures increase chemical reaction ratesincrease cellular diffusion rates and increase the vapourpressures of volatile compounds (Tingey et al 1991 Lerdauet al 1994 Fuentes et al 2000 Sharkey amp Yeh 2001)Various attempts have been made to estimate how an increasein temperature will enhance BVOC emission rates Forexample Penuelas amp Llusia (2003) have suggested thatincreasing mean global temperatures by 2ndash3degC could enhanceglobal BVOC emissions by 25ndash45 At the regional scaleusing Great Britain as a case study it was predicted that anincrease in temperature of 1degC would increase isopreneemissions by 14 in the summertime whereas a 3degCincrease would increase emissions by 50 (Stewart et al2003) At very high temperatures (above approximately40degC) isoprene emissions decline dramatically and it ispossible that extreme temperature rises will eventually causea decrease in isoprene emissions first in the tropicsirrespective of other changes to ecosystems

Climate warming can also indirectly influence global- andregional-scale BVOC emissions by altering vegetation speciescomposition and vegetation characteristics (Starfield amp Chapin1996 Wilmking et al 2004) Warming can also alter latitudinaland altitudinal treelines (Starfield amp Chapin 1996 Lerdau ampSlobodkin 2002 Wilmking et al 2004) Simulation modelspredict forest dieback at lower latitudes (Cox et al 2004)especially in Amazonia but show the upward and northwardexpansion of boreal forests under climate warming (Chapinet al 2000 Kittel et al 2000) as confirmed by field obser-vations (Luckman amp Kavanagh 2000 Kullman 2001 Penuelasamp Boada 2003) The expansion of boreal forests may increaseBVOC emissions through the spread of high-BVOC-emittingtaxa ie Populus sp and Picea spp (Lerdau amp Slobodkin2002) but degradation of lower latitude forests such as inthe Amazonian area may diminish the increase in BVOCproduction at the global scale

3 Land use change and BVOC emissions

The Earth is experiencing massive land use and land coverchanges at unprecedented rates not only as a result of climatechange but also because of urbanization agriculture andagroindustrialization These pressures are altering plant speciesdistributions and characteristics and may dramatically influenceBVOC emissions as a result of their biome- and species-specificcharacteristics Inventories and spatial analysis suggest a globalincrease in crop area of 455 in the past 300 yr (1700ndash1990)and a more than six-fold increase in pasture area (Goldewijk2001) Grasses and cereals are not generally major isopreneemitters (Table 1) although they do emit oxygenated BVOCsparticularly during harvesting (Koumlnig et al 1995 Kirstineet al 1998 Davison et al 2008) Hence the conversion offorest to crops is predicted to decrease BVOC emissions over

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Review38

large geographical areas For example in Amazonia the isopreneemission flux may decrease by as much as 90 followingdeforestation (Ganzeveld amp Lelieveld 2004) and in East Asiaannual isoprene and monoterpene emissions may decrease by30 and 40 respectively because of the expansion ofcropland (Steiner et al 2002) However forest restoration bythe planting of higher isoprene-emitting species (Table 1) willhave major effects on BVOC emission rates especially at thelocal and regional scales (Lathiere et al 2006) The large-scaleexpansion in the cultivation of Elaeis (oil palm Table 1) thatis currently occurring in the tropics for the production ofbiofuel and other applications may be having a significantimpact on BVOC emissions in these regions

4 Drought stress and BVOC emissions

Precipitation frequency and intensity are predicted to changein the future in response to increasing surface temperature(IPCC 2007) Drought stress already affects vegetation inmany areas (Le Houeacuterou 1996) Empirical data summarizedin Table 3 indicate that moderate drought can decreaseenhance or have no effect on isoprene and monoterpeneemissions but severe long-lasting water stress leading to grosswilting or complete inhibition of photosynthesis significantlyreduces BVOC emissions However for sesquiterpenes theeffects of drought are more consistent in the four plant speciesstudied causing a significant reduction in emissions (Ormenoet al 2007)

The varying responses of BVOC emissions to moderatedrought may be a result of differences in leaf physiologyBVOC biochemistry and experimental protocol One impor-tant difference in leaf physiology across plant species is thepresence or absence of terpene reservoirs (see above) Plantsthat possess specific monoterpene storage compartments areable to maintain their emissions of monoterpenes even whenthey experience a decrease in photosynthesis rate (Llusia ampPenuelas 1998 Pegoraro et al 2004 Fortunati et al 2008)Drought can also increase the accumulation of plant secondarymetabolites by decreasing carbon allocation to plant growthas a result of a trade-off between growth and defence (Turtolaet al 2003) It may be that extra-chloroplastic carbon sourcestemporarily compensate for a reduction in carbon from thechoroplastic photosynthesis-dependent 2-C-methyl-d-erythritol4-phosphate pathway (Funk et al 2004 Fortunati et al 2008)

As for air pollutant exposure experiments variations inexperimental design across studies may explain the contrastingresults seen for water stress Although field experiments usingnatural plants are preferable to laboratory experiments usingpotted plants the field manipulation of drought is difficult inpart because of the deep rooting of field-grown plants (Pegoraroet al 2006) Table 3 suggests that drought period and soilmoisture content are not necessarily correlated causing dif-ficulties in the comparison of laboratory and field studies(Pegoraro et al 2004 2006)

Neither Quercus coccifera L nor Quercus ilex have monoter-pene storage compartments yet they exhibit a different responseto drought Quercus coccifera maintained its emission whenthe soil moisture content was reduced by 82 but themonoterpene emission of Q ilex was inhibited when the soilmoisture content was reduced by only 54 (Table 3) Thismay result from the better water-use efficiency of Q coccifera(Vilagrosa et al 2003)

These examples highlight the importance of the measure-ment of leaf water potential and soil moisture to allow bettercomparison of results across different experimental protocolsPegoraro et al (2004) have also suggested that pre-dawn leafwater potential could be used to parameterize drought impacton isoprene emissions

5 Elevated atmospheric O3 concentration and BVOC emissions

It is highly likely that the concentrations of ground-level O3will change in the future The emission rates of the precursorsto O3 formation will change over time and changes to theEarthrsquos climate will cause changes in atmospheric circulationboth of which will directly affect O3 concentrations Ground-level O3 is already a serious regional-scale air pollutant in manyareas of the world but the prediction of future trends dependscritically on assumptions made about precursor emissions Itmay be that ground-level O3 pollution will be reduced insome regions where strict emission controls are implementedbut worsened in other less-developed regions (Fowler et al2008)

As both short-term O3 episodes and long-term elevatedconcentrations have adverse effects on plant growth speciescomposition and ecosystem functioning (Ashmore 2005) itis likely that changes in O3 lsquoclimatologyrsquo will change BVOCemissions over time These changes may be the result of thedirect effects of O3 on plants or may be caused by the indirecteffects of species composition Experimental observations haveprobed the former and next-generation Earth systems modelswill before long be able to make predictions about the latter

Experimental evidence on the direct effects of O3 onBVOC emissions is as for other abiotic stresses not clear cutshowing that elevated O3 can increase decrease or have noeffect on BVOC emission rates (Table 4) These differencesdepend on the plant species (Heiden et al 1999 Pentildeuelaset al 1999) the season (Llusiagrave et al 2002) and the BVOCspecies (Llusia et al 2002) Recent work by Ryan et al (2009)has shown that two genotypes of hybrid poplar with differingsensitivities to O3 have different VOC responses whenexposed to O3 The O3-tolerant genotype was able to maintainits isoprene emission rate when exposed to 120 ppb O3 for 6 hdminus1 for 8 d whereas the O3-sensitive genotype could not itsisoprene emission rate fell on exposure to O3 A differenteffect has been seen in tobacco where elevated O3 signifi-cantly increases BVOC emissions from the O3-sensitive clone

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Table 3 Effect of drought on biogenic volatile organic compound (BVOC) emissions (D decrease I increase sig significant soil moisture reduced by of field capacity mono monoterpenes iso isoprene ses sesquiterpenes)

Sources Subdescription ApproachBVOC measurement scale Plant species Replication (n) Effect on BVOC emissions

Bertin amp Staudt (1996) Laboratory observation 18 d of drought period (severe drought)

Branch chamber Quercus ilex L 2 D 100 (mono)

Pot-grown plants Soil moisture reduced by ~54

Young plants (age not specified)

Pegoraro et al (2004) Laboratory observation 10ndash12 d of drought period (severe drought)

Leaf enclosure Quercus virginiana Mill 6 D 64 (iso)


2-yr-old plantsPlaza et al (2005) Field observation Natural drought

(measured diurnal courses of emission rate)

Branch enclosure Quercus ilex spp rotundifolia

1 or 2 Inconsistent monoterpene emission over the 2 yr

Mediterranean oak forest30-yr-old plantsTwo growing seasons (2000ndash01)

Pegoraro et al (2006) Closed biospheres 36 d of drought period (mild drought)

Ecosystem level gas exchange measurement

Mixed isoprene-emitting and nonisoprene-emitting species with deep roots

No sig effect (iso)

(Biosphere 2 tropical rain forest)

Soil moisture reduced by ~50 from field capacity

~15-yr-old plantsLlusia et al (2006) Field observation Sliding plastic curtain (mild

drought)Solvent extraction from leaves

Pinus halepensis L 2ndash4 Contrasting results depending on seasons plant species year and type of BVOC

Mediterranean scrubland (2002ndash04)

Soil moisture reduced by 19 from field capacity

Globularia alypum L

Rosmarinus officinalis LErica multiflora L

Ormeno et al (2007) Laboratory observation 11 d of drought period (severe drought)

Branch enclosure Rosmarinus officinalis L 6 D ~ 20 (total mono + ses)

Pot-grown plants Soil moisture reduced by ~82 from field capacity

No sig effect (total mono)

3-yr-old plants D ~ 70 (total ses)Pinus halepensis L I ~ 290 (total mono + ses)

I ~ 270 (total mono)D ~ 28 (total ses)

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Cistus albidus L I ~ 107 (total mono + ses)I ~ 285 (total mono)D ~ 13 (total ses)

Quercus coccifera L No sig except day 7 I ~ 265 (total mono + ses)No sig effect (total mono)D ~ 1 (total ses)

Llusia et al (2008) Field observation Sliding plastic curtain Branch enclosure Pinus halepensis L 3 I ~ 1665 (selected mono)Mediterranean scrubland Long-term drought

(mild drought)Globularia alypum L I 75 (selected mono)

Two growing seasons (2003ndash05) (protect all rain events)


Erica multiflora L D 19 (iso) I 264 (selected mono)

Fortunati et al (2008) Laboratory observation 35 d of drought period (severe drought)

Leaf enclosure Populus nigra L 9 D ~ 71 (iso)


1-yr-old plants


Table 3 continued

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Table 4 Effect of ozone on biogenic volatile organic compound (BVOC) emissions (D decrease I increase sig significant OTCs open top chambers mono monoterpenes iso isoprene ses sesquiterpenes)

Sources SubdescriptionFumigation method

O3 level (ppbv)

Fumigation period

BVOC measurement scale Plant species

Replication (n) BVOC measure at

Effect on BVOC emissions

Pentildeuelas et al (1999)

Field observation OTCs Ambient + 40 8 h Whole plants Pinus halepensis L

3 Not specified No sig effect (total BVOCs)

Leaf enclosure Solanum lycopersicum L var Tiny Tim

I ~ 74 (total BVOCs)

Heiden et al (1999)

Laboratory observations

Cylindrical glass chamber

120ndash170 5 h Shoot enclosure

Nicotiana tabacum L cv Bel B (O3-tolerant)

2ndash3 24 h after fumigation No sig effect (total BVOCs)




Nicotiana tabacum L cv Bel W3 (O3-sensitive)

2ndash3 24 h after fumigation I ~ 270 (total BVOCs)

Sig presence of C6 VOCs

Field observations OTCs 50 8 h dndash1 for 2 yr Not specified Pinus sylvestris L 4 I 40 (mono)Llusia et al (2002)

Field observation OTCs Ambient + 40 8 h Leaf enclosure Ceratonia siliqua L

3 I ~ 65 (total BVOCs of the four species)

Pot-grown plants Olea europaea L3-yr-old plants Quercus ilex spp

ilex LQuercus ilex spp rotundifolia L

Loreto et al (2004)

Laboratory observation

Growth chamber 100ndash200 4 h dminus1 for 5 d Leaf enclosure Quercus ilex L 4 2 d after fumigation I ~ 182 (mono)

Pot-grown plants Whole-plant fumigation

3-yr-old plantsLoreto et al (2004)


Gas exchange cuvette

250 4 h Excised leaf enclosure

Quercus ilex L 4 4 h after fumigation I ~ 60 (mono)

Pot-grown plants Single-leaf fumigation

3-yr-old plantsVuorinen et al (2004a)


Growth chamber 150ndash400 8 h for 1st day Shoot enclosure

Phaseolus lunatus cv Sieva

6 Soon after fumigation



Unspecified hours for 2nd day

5ndash7 d-old plants

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Velikova et al (2005)




Phragmites australis L

6 Immediately after fumigation

I ~ 55 (iso)


Calfapietra et al (2008)

Field observation FACE 65 Long-term Leaf enclosure Populus tremuloides (271 O3-tolerant)

3 Measurements of both clones performed at O3 concentration at which plants were growing

No significant effect (iso)

10-yr-old plants Populus tremuloides (42 O3-sensitive)

3 D ~ 20 (iso)

Ryan et al (2009)


Growth chamber 120 6 h for 8 d Leaf enclosure Populus deltoides timesP trichocarpa (O3-tolerant)

3ndash4 Soon after fumigation


Pot-grown plants P deltoides timesP trichocarpa (O3-sensitive)

D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

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(Heiden et al 1999) but not from the tolerant clone How-ever in both cases the maintenance of BVOC emissions fromthe tolerant clone may be because these plants have a higherability to detoxify reactive oxygen species that occur after O3uptake through the stomata possibly because they have ahigher carotenoid content which allows O3 quenching insideO3-tolerant leaves (Ryan et al 2009 Calfapietra et al 2008)This could lead to lower cell membrane damage in O3-tolerantplants This hypothesis is supported by the low C6 emissionrates of O3-tolerant plants compared with those from O3-sensitive plants It should also be noted that elevated O3 mayinduce the production of BVOCs that are not present in unex-posed plants (Heiden et al 1999 Vuorinen et al 2004a)

As summarized in Table 4 considerable differences inexperimental design have been used and may be responsiblefor some of the observed differences in response to O3 O3concentrations above 200ndash300 ppb do not have environmentalrelevance and future experiments should use realistic exposures

6 Interactions and feedback

Future increases in global temperature will occur simultaneouslywith other drivers and effects of global change (IPCC 2007)Concern has already been expressed about how the relationshipbetween plants and biotic stresses mediated by BVOCs maybe altered in response to global change ndash future climaticconditions might strengthen or weaken the performance ofherbivores and pathogens depending on their traits (Manningamp Vontiedemann 1995 Ward amp Masters 2007) Similarlyglobal change may affect plant performance and hence mayalter their defences against biotic stresses As BVOCs havebeen shown to exhibit direct and indirect functions in plantdefences (see above) alteration of BVOC emissions as a resultof environmental changes may affect these defence mechanisms

Although evidence of the influence of environmentalchange on the direct role of BVOCs in plantndashherbivore inter-actions is lacking much work has been carried out to investi-gate changes in indirect plant defences O3 may interfere withparasitoid olfactory responses and damage their searchingefficiency (Gate et al 1995) Importantly however the rapidreaction of O3 with some BVOCs in the gas phase may degradethe BVOC signal from herbivore-infested plants As notedabove exposure to O3 may suppress or enhance BVOCemission rates Hence elevated O3 may disrupt the plantndashherbivorendashpredatorparasitoid system However some recentexperiments have indicated that O3 does not affect theorientation of a predatory mite (Phytoseiulus persimilis)or parasitoid (Cotesia plutellae) (Pinto et al 2007 2008) Itmay be that natural enemies learn to exploit degraded BVOCproducts rather than the primary (emitted) BVOCs or thatlong-distance signals between plants and predators or parasi-toids could be provided by the more stable herbivore-inducedvolatile compounds such as MeSA methanol and benzylcyanide (Pinto et al 2007)

By contrast elevated CO2 concentrations may disturb BVOCsignals to the third trophic level by weakening the plantresponse induced by insect herbivores However this mayvary with specific combinations of plants and herbivoreenemies (Vuorinen et al 2004b) Field studies have shownthat interactions in a treendashherbivorendashparasitoid system may bemodified by O3 and elevated CO2 concentrations and thatthe degree of modification is dependent on plant genotype(Holton et al 2003)

Other abiotic factors including water stress light intensitytemperature and nutrient availability are also important indetermining the intensity and variability of induced plantvolatiles Water-stressed corn plants (Zea mays) producedlarger amounts of induced plant volatiles than did nonstressedplants although the former did not show any symptoms ofdesiccation (Gouinguene amp Turlings 2002) When grownunder high light undamaged Lima beans released larger relativeamounts of volatile synomones and were more attractive topredatory mites than those grown under low light (Takabayashiet al 1994) Changes in climatic factors can therefore altersignificantly the relative ratios of the emitted BVOCs andhence influence the quality of the induced odour blendsThese studies have been undertaken on annual plants andthere is still a need to investigate such effects on perennial orwoody plants which are abundant in forest ecosystems

Although trends in BVOC emission rates as the Earthrsquosclimate changes are still uncertain reactive BVOCs especiallyisoprene are of obvious concern as they may give rise to species-specific feedbacks between plants and the atmosphere(Shallcross amp Monks 2000 Fuentes et al 2001 Lerdau2007 Arneth et al 2008b) Simplistically it may be expectedthat climate warming will increase BVOC emissions becauseof their strong temperature dependence and so increaseatmospheric concentrations causing a decrease in the concen-tration of OH and so leading to a reduction in the capacityof the atmosphere to remove tropospheric methane and COresulting in even further global warming Enhancement ofisoprene emissions in response to rising temperature may alsohave the dual effect of promoting tropospheric O3 productionin NOx-polluted air whilst contributing to reduced O3 damageto leaves in isoprene-emitting species (Loreto et al 2001bVelikova et al 2005)

However such simplistic models require considerableelaboration as many BVOCs serve to protect plants againstbiotic and abiotic stresses (see above) It is also possible thatisoprene may serve multiple purposes in plants (Laotha-wornkitkul et al 2008b) and therefore changes to BVOCemission rates caused by stresses may render the plants moresusceptible to other stresses Ultimately these effects might beindirectly amplified by other consequences of global changesuch as regional shifts in precipitation amount and pattern thegeographical redistribution of biomassplant species lengtheningof the growing season and increases in invasive herbivorepathogen species

Tansley review


Review44

Present models are unable to adequately predict these pos-sible interactions and feedbacks partly because the combinedeffects of global warming with other global environmentaldrivers on BVOC emissions may not always give straightfor-ward outcomes Drought episodes for example may removethe positive effect of warming on isoprene emission (Fortunatiet al 2008) whereas enhanced UVB radiation together withwarming may increase emissions (Tiiva et al 2007) Changesin cloudiness driven by BVOC emissions and subsequent SOAformation will change the intensity of photosyntheticallyactive radiation so changing the emission rates of some light-dependent BVOCs Although many experiments have exploredthe effects of global change parameters (eg temperature CO2and O3 concentrations water stress etc) on BVOC emissionsand possible disruption to their functions in and betweenplants multivariate laboratory and field studies are needed toprovide further understanding of possible interactions andfeedbacks between environmental change and BVOCemissions

V Synthesis

It is clear that BVOCs emitted by the terrestrial biospherehave effects on the biological chemical and physical componentsof the Earth system providing connections between thebiosphere and atmosphere and between plants insects andanimal communities However the unprecedented pressurethat humans are now exerting on the Earth system and theimpact that this is having on the global environment maychange the existing relationships mediated by BVOCs andlead to unforeseen consequences Although our understandingof the sources controls and effects of BVOCs has increasedsignificantly over the past few decades and now allows us tomake informed (but still uncertain) predictions of their currentemissions and of their responses to future global environmentalchanges it is clear that there is still much more to be exploredabout the roles of BVOCs in the Earth system In the nearfuture it seems likely that societal pressures around foodsecurity and more sustainable agricultural practises will promotefurther research into the role of BVOCs in tritrophicinteractions and their use and development throughconventional breeding or genetic engineering for cropprotection (Poppy amp Sutherland 2004 Kappers et al 2005)Similarly increasing societal concern over air quality willinevitably drive further research into BVOC emissions andatmospheric chemistry Concern over the Earthrsquos climate systemwill also drive the development of coupled and interactivemodels of the Earth system which will better allow the role ofBVOCs to be explored

The exchange of resources and knowledge betweenatmospheric chemists and plant biologists especially chemicalecologists has greatly enhanced our understanding of theroles and impacts of BVOCs The recent development of fast-response highly sensitive (at the pptv level) analytical tools

commonly used in atmospheric chemistry research such asthe proton transfer reaction mass spectrometer (Hewitt et al2003 Canagaratna et al 2007) now allows rapid (Hz) BVOCconcentration and flux measurements to be made The appli-cation of such tools in plant ecology can for example allowthe response time of stress application to be explored

Although it is possible to factor several parameters intoexperiments or models to simulate the effects of global changeon BVOCs the incorporation of all the dimensions of globalchange into an experiment to mimic real conditions is notcurrently feasible At present it is therefore necessary to con-tinue to probe this topic by for example combining experi-mental results gradient studies simulation modelling andremote sensing Using these integrated approaches it shouldbe possible to make substantial progress in the mechanisticunderstanding of the effects of the important interactionsmediated by BVOCs and their potential to generate positiveand negative feedbacks in response to future global changeand climate warming However the interactive incorporationof all of these variables into a comprehensive model of theEarth system is still many years away

Acknowledgements

The authors thank Alistair Hetherington for inviting us towrite this review the Engineering and Physical SciencesResearch Council (EPSRC)Royal Society Dorothy HodgkinPostgraduate Awards to JL the European Science FoundationlsquoVOCBASrsquo programme and the EC FP6 lsquoISONETrsquo MarieCurie Research Training Network for financial support andMalcolm Possell and Michael Wilkinson for stimulatingdiscussions

References

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Tansley review


Review 45

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Bruce TJA Matthes MC Chamberlain K Woodcock CM Mohib A Webster B Smart LE Birkett MA Pickett JA Napier JA 2008 cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids Proceedings of the National Academy of Sciences 105 4553ndash4558

Bruce TJA Pickett JA Smart LE 2003b Cis-Jasmone switches on plant defence against insects Pesticide Outlook 14 96ndash98

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Tansley review


Review46

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Tansley review


Review 47

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Holton MK Lindroth R Nordheim E 2003 Foliar quality influences treendashherbivorendashparasitoid interactions effects of elevated CO2 O3 and plant genotype Oecologia 137 233ndash244

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Laothawornkitkul J Paul ND Vickers CE Possell M Taylor JE Mullineaux PM Hewitt CN 2008c Isoprene emissions influence herbivore feeding decisions Plant Cell and Environment 31 1410ndash1415

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Review48

Lerdau M Dilts SB Westberg H Lamb BK Allwine EJ 1994 Monoterpene emission from Ponderosa pine Journal of Geophysical Research-Atmospheres 99 16609ndash16615

Lerdau M Guenther A Monson R 1997 Plant production and emission of volatile organic compounds Bioscience 47 373ndash383

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Llusia J Penuelas J 1998 Changes in terpene content and emission in potted Mediterranean woody plants under severe drought Canadian Journal of Botany-Revue Canadienne de Botanique 76 1366ndash1373

Llusia J Penuelas J Alessio GA Estiarte M 2006 Seasonal contrasting changes of foliar concentrations of terpenes and other volatile organic compounds in four dominant species of a Mediterranean shrubland submitted to a field experimental drought and warming Physiologia Plantarum 127 632ndash649

Llusia J Penuelas J Alessio GA Estiarte M 2008 Contrasting species-specific compound-specific seasonal and interannual responses of foliar isoprenoid emissions to experimental drought in a Mediterranean shrubland International Journal of Plant Sciences 169 637ndash645

Llusia J Penuelas J Gimeno BS 2002 Seasonal and species-specific response of VOC emissions by Mediterranean woody plant to elevated ozone concentrations Atmospheric Environment 36 3931ndash3938

Logan JA Prather MJ Wofsy SC McElroy MB 1981 Tropospheric chemistry ndash a global perspective Journal of Geophysical Research-Oceans and Atmospheres 86 7210ndash7254

Loivamaki M Louis S Cinege G Zimmer I Fischbach RJ Schnitzler JP 2007 Circadian rhythms of isoprene biosynthesis in grey poplar leaves Plant Physiology 143 540ndash551

Loivamaki M Mumm R Dicke M Schnitzler Jr-P 2008 Isoprene interferes with the attraction of bodyguards by herbaceous plants Proceedings of the National Academy of Sciences 105 17 430ndash17 435

Loreto F Ciccioli P Brancaleoni E Cecinato A Frattoni M 1998a Measurement of isoprenoid content in leaves of Mediterranean Quercus spp by a novel and sensitive method and estimation of the isoprenoid partition between liquid and gas phase inside the leaves Plant Science 136 25ndash30

Loreto F Fischbach RJ Schnitzler JP Ciccioli P Brancaleoni E Calfapietra C Seufert G 2001a Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex L grown at elevated CO2 concentrations Global Change Biology 7 709ndash717

Loreto F Forster A Durr M Csiky O Seufert G 1998b On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L fumigated with selected monoterpenes Plant Cell amp Environment 21 101ndash107

Loreto F Mannozzi M Maris C Nascetti P Ferranti F Pasqualini S 2001b Ozone quenching properties of isoprene and its antioxidant role in leaves Plant Physiology 126 993ndash1000

Loreto F Pinelli P Manes F Kollist H 2004 Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves Tree Physiology 24 361ndash367

Loreto F Velikova V 2001 Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage quenches ozone products and reduces lipid peroxidation of cellular membranes Plant Physiology 127 1781ndash1787

Lou Y Baldwin IT 2003 Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants Proceedings of the National Academy of Sciences of the United States of America 100 14 581ndash14 586

Loughrin J Manukian A Heath R Tumlinson J 1995 Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae Journal of Chemical Ecology 21 1217ndash1227

Luckman B Kavanagh T 2000 Impact of climate fluctuations on mountain environments in the Canadian Rockies Ambio 29 371ndash380

Luft S Curio E Tacud B 2003 The use of olfaction in the foraging behaviour of the golden-mantled flying fox Pteropus pumilus and the greater musky fruit bat Ptenochirus jagori (Megachiroptera Pteropodidae) Naturwissenschaften 90 84ndash87

Manning WJ Vontiedemann A 1995 Climate-change ndash potential effects of increased atmospheric carbon-dioxide (CO2) ozone (O3) and ultraviolet-B (UV-B) radiation on plant-diseases Environmental Pollution 88 219ndash245

Manriacutequez D El-Sharkawy I Flores F El-Yahyaoui F Regad F Bouzayen M Latcheacute A Pech J-C 2006 Two highly divergent alcohol dehydrogenases of melon exhibit fruit ripening-specific expression and distinct biochemical characteristics Plant Molecular Biology 61 675ndash685

Matsui K 2006 Green leaf volatiles hydroperoxide lyase pathway of oxylipin metabolism Current Opinion in Plant Biology 9 274ndash280

Meskhidze N Nenes A 2006 Phytoplankton and cloudiness in the Southern Ocean Science 314 1419ndash1423

Mithofer A Wanner G Boland W 2005 Effects of feeding Spodoptera littoralis on Lima bean leaves II Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission Plant Physiology 137 1160ndash1168

Monson RK Jaeger CH Adams WW Driggers EM Silver GM Fall R 1992 Relationships among isoprene emission rate photosynthesis and isoprene synthase activity as influenced by temperature Plant Physiology 98 1175ndash1180

Murray MB Leith ID Jarvis PG 1996 The effect of long term CO2 enrichment on the growth biomass partitioning and mineral nutrition of Sitka spruce (Picea sitchensis (Bong) Carr) Trees-Structure and Function 10 393ndash402

Myneni RB Keeling CD Tucker CJ Asrar G Nemani RR 1997 Increased plant growth in the northern high latitudes from 1981 to 1991 Nature 386 698ndash702

Neff JC Holland EA Dentener FJ McDowell WH Russell KM 2002 The origin composition and rates of organic nitrogen deposition a missing piece of the nitrogen cycle Biogeochemistry 57ndash58 99ndash136

Negre F Kish CM Boatright J Underwood B Shibuya K Wagner C Clark DG Dudareva N 2003 Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers Plant Cell 15 2992ndash3006

Niinemets U Loreto F Reichstein M 2004 Physiological and physicochemical controls on foliar volatile organic compound emissions Trends in Plant Science 9 180ndash186

OrsquoDonnell PJ Calvert C Atzorn R Wasternack C Leyser HMO Bowles DJ 1996 Ethylene as a signal mediating the wound response of tomato plants Science 274 1914ndash1917

Ormeno E Mevy JP Vila B Bousquet-Melou A Greff S Bonin G Fernandez C 2007 Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species Relationship between terpene emissions and plant water potential Chemosphere 67 276ndash284

Owen SM Boissard C Hewitt CN 2001 Volatile organic compounds (VOCs) emitted from 40 Mediterranean plant species VOC speciation and extrapolation to habitat scale Atmospheric Environment 35 5393ndash5409

Owen SM Clarke S Hewitt CN Semple KT 2007 Biogenic volatile organic compounds as potential carbon sources for soil microflora in soil from the rhizosphere of Populus tremula FEMS Microbiology Letters 268 34ndash39

Ozawa R Arimura G Takabayashi J Shimoda T Nishioka T 2000 Involvement of jasmonate- and salicylate-related signaling pathways for

Tansley review


Review 49

the production of specific herbivore-induced volatiles in plants Plant and Cell Physiology 41 391ndash398

Pareacute PW Tumlinson JH 1997 Induced synthesis of plant volatiles Nature 385 30ndash31

Park SW Kaimoyo E Kumar D Mosher S Klessig DF 2007 Methyl salicylate is a critical mobile signal for plant systemic acquired resistance Science 318 113ndash116

Paschold A Halitschke R Baldwin IT 2006 Using lsquomutersquo plants to translate volatile signals The Plant Journal 45 275ndash291

Pegoraro E Rey ANA Abrell L Haren J Lin G 2006 Drought effect on isoprene production and consumption in Biosphere 2 tropical rainforest Global Change Biology 12 456ndash469

Pegoraro E Rey A Greenberg J Harley P Grace J Malhi Y Guenther A 2004 Effect of drought on isoprene emission rates from leaves of Quercus virginiana Mill Atmospheric Environment 38 6149ndash6156

Penuelas J Boada M 2003 A global change-induced biome shift in the Montseny mountains (NE Spain) Global Change Biology 9 131ndash140

Penuelas J Llusia J 1997 Effects of carbon dioxide water supply and seasonality on terpene content and emission by Rosmarinus officinalis Journal of Chemical Ecology 23 979ndash993

Penuelas J Llusia J 2003 BVOCs plant defense against climate warming Trends in Plant Science 8 105ndash109

Pentildeuelas J Llusiagrave J Gimeno BS 1999 Effects of ozone concentrations on biogenic volatile organic compounds emission in the Mediterranean region Environmental Pollution 105 17ndash23

Pinto D Blande J Nykaumlnen R Dong W-X Nerg A-M Holopainen J 2007 Ozone degrades common herbivore-induced plant volatiles does this affect herbivore prey location by predators and parasitoids Journal of Chemical Ecology 33 683ndash694

Pinto DM Himanen SJ Nissinen A Nerg AM Holopainen JK 2008 Host location behavior of Cotesia plutellae Kurdjumov (Hymenoptera Braconidae) in ambient and moderately elevated ozone in field conditions Environmental Pollution 156 227ndash231

Plaza J Nunez L Pujadas M Perrez-Pastor R Bermejo V Garcia-Alonso S Elvira S 2005 Field monoterpene emission of Mediterranean oak (Quercus ilex) in the central Iberian Peninsula measured by enclosure and micrometeorological techniques Observation of drought stress effect Journal of Geophysical Research 110 D01105

van Poecke RMP Dicke M 2002 Induced parasitoid attraction by Arabidopsis thaliana involvement of the octadecanoid and the salicylic acid pathway Journal of Experimental Botany 53 1793ndash1799

Poisson N Kanakidou M Crutzen PJ 2000 Impact of non-methane hydrocarbons on tropospheric chemistry and the oxidizing power of the global troposphere 3-dimensional modelling results Journal of Atmospheric Chemistry 36 157ndash230

Poppy GM Sutherland JP 2004 Can biological control benefit from genetically-modified crops Tritrophic interactions on insect-resistant transgenic plants Physiological Entomology 29 257ndash268

Possell M Heath J Nicholas Hewitt C Ayres E Kerstiens G 2004 Interactive effects of elevated CO2 and soil fertility on isoprene emissions from Quercus robur Global Change Biology 10 1835ndash1843

Possell M Hewitt CN Beerling DJ 2005 The effects of glacial atmospheric CO2 concentrations and climate on isoprene emissions by vascular plants Global Change Biology 11 60ndash69

Pott MB Hippauf F Saschenbrecker S Chen F Ross J Kiefer I Slusarenko A Noel JP Pichersky E Effmert U et al 2004 Biochemical and structural characterization of benzenoid carboxyl methyltransferases involved in floral scent production in Stephanotis floribunda and Nicotiana suaveolens Plant Physiology 135 1946ndash1955

Qualley AV Dudareva N 2008 Aromatic volatiles and their involvement in plant defense In Schaller A ed Induced plant resistance to herbivory Netherlands Springer 409ndash432

Ralph S Oddy C Cooper D Yueh H Jancsik S Kolosova N Philippe RN Aeschliman D White R Huber D et al 2006 Genomics of hybrid

poplar (Populus trichocarpa times deltoides) interacting with forest tent caterpillars (Malacosoma disstria) normalized and full-length cDNA libraries expressed sequence tags and a cDNA microarray for the study of insect-induced defences in poplar Molecular Ecology 15 1275ndash1297

Raskin I 1992 Role of salicylic acid in plants Annual Review of Plant Physiology and Plant Molecular Biology 43 439ndash463

Rasmann S Kollner TG Degenhardt J Hiltpold I Toepfer S Kuhlmann U Gershenzon J Turlings TCJ 2005 Recruitment of entomopathogenic nematodes by insect-damaged maize roots Nature 434 732ndash737

Rizzo LV Artaxo P Guenther A Karl T Greenberg J 2006 Measurement of aerosol and VOC turbulent fluxes over a pristine forest in Amazonia Eos trans American Geophysical Union Fall Meeting 87 Abstract A23A-0931

Roumlse UR Tumlinson J 2004 Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds Planta 218 824ndash832

Rosenstiel TN Ebbets AL Khatri WC Fall R Monson RK 2004 Induction of poplar leaf nitrate reductase a test of extrachloroplastic control of isoprene emission rate Plant Biology 6 12ndash21

Rosenstiel TN Potosnak MJ Griffin KL Fall R Monson RK 2003 Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem Nature 421 256ndash259

Ryan A Cojocariu C Possell M Davies WJ Hewitt CN 2009 Defining hybrid poplar (Populus deltoides times Populus trichocarpa) tolerance to ozone identifying key parameters Plant Cell and Environment 32 31ndash45

Sanadze GA 1956 Emission of gaseous organic substance from plants Repertuar Akademiia Nauk Gruzinskoi SSR 17 429ndash433

Sanadze GA 2004 Biogenic isoprene ndash (a review) Russian Journal of Plant Physiology 51 729ndash741

Schiestl FP Ayasse M 2002 Do changes in floral odor cause speciation in sexually deceptive orchids Plant Systematics and Evolution 234 111ndash119

Schmelz E Alborn H Banchio E Tumlinson J 2003a Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory Planta 216 665ndash673

Schmelz EA Alborn HT Tumlinson JH 2003b Synergistic interactions between volicitin jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays Physiologia Plantarum 117 403ndash412

Seo HS Song JT Cheong J-J Lee Y-H Lee Y-W Hwang I Lee JS Choi YD 2001 Jasmonic acid carboxyl methyltransferase a key enzyme for jasmonate-regulated plant responses Proceedings of the National Academy of Sciences of the United States of America 98 4788ndash4793

Shallcross DE Monks PS 2000 New directions a role for isoprene in biospherendashclimatendashchemistry feedbacks Atmospheric Environment 34 1659ndash1660

Sharkey TD Loreto F Delwiche CF 1991 High-carbon dioxide and sun shade effects on isoprene emission from oak and aspen tree leaves Plant Cell and Environment 14 333ndash338

Sharkey TD Singsaas EL 1995 Why plants emit isoprene Nature 374 769

Sharkey TD Singsaas EL Vanderveer PJ Geron C 1996 Field measurements of isoprene emission from trees in response to temperature and light Tree Physiology 16 649ndash654

Sharkey TD Wiberley AE Donohue AR 2007 Isoprene emission from plants why and how Annals of Botany 100 1ndash14

Sharkey TD Yeh SS 2001 Isoprene emission from plants Annual Review of Plant Physiology and Plant Molecular Biology 52 407ndash436

Shiojiri K Karban R 2006 Plant age communication and resistance to herbivores young sagebrush plants are better emitters and receivers Oecologia 149 214ndash220

Shiojiri K Karban R 2008 Vascular systemic induced resistance for Artemisia cana and volatile communication for Artemisia douglasiana American Midland Naturalist 159 468ndash477

Shiojiri K Kishimoto K Ozawa R Kugimiya S Urashimo S Arimura G Horiuchi J Nishioka T Matsui K Takabayashi J 2006 Changing green

Tansley review


Review50

leaf volatile biosynthesis in plants an approach for improving plant resistance against both herbivores and pathogens Proceedings of the National Academy of Sciences 103 16 672ndash16 676

Shulaev V Silverman P Raskin I 1997 Airborne signalling by methyl salicylate in plant pathogen resistance Nature 385 718ndash721

Singsaas EL Lerdau M Winter K Sharkey TD 1997 Isoprene increases thermotolerance of isoprene-emitting species Plant Physiology 115 1413ndash1420

Sivasankar S Sheldrick B Rothstein SJ 2000 Expression of allene oxide synthase determines defense gene activation in tomato Plant Physiology 122 1335ndash1342

Siwko ME Marrink SJ de Vries AH Kozubek A Schoot Uiterkamp AJM Mark AE 2007 Does isoprene protect plant membranes from thermal shock A molecular dynamics study Biochimica et Biophysica Acta (BBA) ndash Biomembranes 1768 198ndash206

Soares FD Pereira T Maio Marques MO Monteiro AR 2007 Volatile and non-volatile chemical composition of the white guava fruit (Psidium guajava) at different stages of maturity Food Chemistry 100 15ndash21

Starfield AM Chapin FS 1996 Model of transient changes in arctic and boreal vegetation in response to climate and land use change Ecological Applications 6 842ndash864

Staswick PE 2008 JAZing up jasmonate signaling Trends in Plant Science 13 66ndash71

Staswick PE Tiryaki I 2004 The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis Plant Cell 16 2117ndash2127

Staudt M Bertin N 1998 Light and temperature dependence of the emission of cyclic and acyclic monoterpenes from holm oak (Quercus ilex L) leaves Plant Cell and Environment 21 385ndash395

Staudt M Joffre R Rambal S Kesselmeier J 2001 Effect of elevated CO2 on monoterpene emission of young Quercus ilex trees and its relation to structural and ecophysiological parameters Tree Physiology 21 437ndash445

Steiner A Luo C Huang Y Chameides WL 2002 Past and present-day biogenic volatile organic compound emissions in East Asia Atmospheric Environment 36 4895ndash4905

Stewart HE Hewitt CN Bunce RGH Steinbrecher R Smiatek G Schoenemeyer T 2003 A highly spatially and temporally resolved inventory for biogenic isoprene and monoterpene emissions model description and application to Great Britain Journal of Geophysical Research-Atmospheres 108 108(D20) 4644 doi1001292002JD002694

Takabayashi J Dicke M Posthumus MA 1994 Volatile herbivore-induced terpenoids in plantndashmite interactions variation caused by biotic and abiotic factors Journal of Chemical Ecology 20 1329ndash1354

Tarr MA Miller WL Zepp RG 1995 Direct carbon-monoxide photoproduction from plant matter Journal of Geophysical Research-Atmospheres 100 11 403ndash11 413

Terry GM Stokes NJ Hewitt CN Mansfield TA 1995 Exposure to isoprene promotes flowering in plants Journal of Experimental Botany 46 1629ndash1631

Thaler JS 1999 Jasmonate-inducible plant defences cause increased parasitism of herbivores Nature 399 686ndash688

Thaler JS Farag MA Pare PW Dicke M 2002a Jasmonate-deficient plants have reduced direct and indirect defences against herbivores Ecology Letters 5 764ndash774

Thaler JS Fidantsef AL Bostock RM 2002b Antagonism between jasmonate- and salicylate-mediated induced plant resistance effects of concentration and timing of elicitation on defense-related proteins herbivore and pathogen performance in tomato Journal of Chemical Ecology 28 1131ndash1159

Thaler JS Karban R Ullman DE Boege K Bostock RM 2002c Cross-talk between jasmonate and salicylate plant defense pathways effects on several plant parasites Oecologia 131 227ndash235

Thomas RB Strain BR 1991 Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide Plant Physiol 96 627ndash634

Tiiva P Rinnan R Faubert P Rasanen J Holopainen T Kyro E Holopainen JK 2007 Isoprene emission from a subarctic peatland under enhanced UV-B radiation New Phytologist 176 346ndash355

Tingey DT Manning M Grothaus LC Burns WF 1980 Influence of light and temperature on monoterpene emission rates from Slash Pine Plant Physiology 65 797ndash801

Tingey DT Turner DP Weber JA 1991 Factors controlling the emission of monoterpene and other volatile compounds San Diego CA USA Academic Press

Ton J DrsquoAlessandro M Jourdie V Jakab G Karlen D Held M Mauch-Mani B Turlings TCJ 2007 Priming by airborne signals boosts direct and indirect resistance in maize The Plant Journal 49 16ndash26

Turtola S Manninen AM Rikala R Kainulainen P 2003 Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings Journal of Chemical Ecology 29 1981ndash1995

Underwood BA Tieman DM Shibuya K Dexter RJ Loucas HM Simkin AJ Sims CA Schmelz EA Klee HJ Clark DG 2005 Ethylene-regulated floral volatile synthesis in petunia corollas Plant Physiology 138 255ndash266

Vancanneyt G Sanz C Farmaki T Paneque M Ortego F Castanera P Sanchez-Serrano JJ 2001 Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance Proceedings of the National Academy of Sciences of the United States of America 98 8139ndash8144

Vasyukova NI Ozeretskovskaya OL 2007 Induced plant resistance and salicylic acid a review Applied Biochemistry and Microbiology 43 367ndash373

Velikova V Pinelli P Pasqualini S Reale L Ferranti F Loreto F 2005 Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone New Phytologist 166 419ndash426

Vickers CE Possell MP Cojocariu C Velikova V Laothawornkitkul J Ryan A Mullineaux PM Hewitt CN 2009 Isoprene synthesis protects transgenic plants from oxidative stress Plant Cell and Environment 32 520ndash531

Vilagrosa A Bellot J Vallejo VR Gil-Pelegrin E 2003 Cavitation stomatal conductance and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought Journal of Experimental Botany 54 2015ndash2024

Vuorinen T Nerg AM Holopainen JK 2004a Ozone exposure triggers the emission of herbivore-induced plant volatiles but does not disturb tritrophic signalling Environmental Pollution 131 305ndash311

Vuorinen T Nerg AM Ibrahim MA Reddy GVP Holopainen JK 2004b Emission of Plutella xylostella-induced compounds from cabbages grown at elevated CO2 and orientation behavior of the natural enemies Plant Physiology 135 1984ndash1992

Vuorinen T Reddy GVP Nerg AM Holopainen JK 2004c Monoterpene and herbivore-induced emissions from cabbage plants grown at elevated atmospheric CO2 concentration Atmospheric Environment 38 675ndash682

Ward NL Masters GJ 2007 Linking climate change and species invasion an illustration using insect herbivores Global Change Biology 13 1605ndash1615

Wayne RP 2000 Chemistry of atmospheres 3rd edn New York USA Oxford University Press

Went FW 1960 Blue hazes in the atmosphere Nature 187 641ndash643Wilkinson MJ Monson RK Trahan N Lee S Brown E Jackson RB

Polley HW Fay PA Fall R 2008 Leaf isoprene emission rate as a function of atmospheric CO2 concentration Global Change Biology 15 1189ndash1200

Wilkinson MJ Owen SM Possell M Hartwell J Gould P Hall A Vickers C Hewitt CN 2006 Circadian control of isoprene emissions from oil palm (Elaeis guineensis) Plant Journal 47 960ndash968

Wilmking M Juday GP Barber VA Zald HSJ 2004 Recent climate warming forces contrasting growth responses of white spruce at treeline in

Tansley review


Review 51

Alaska through temperature thresholds Global Change Biology 10 1724ndash1736

Wright GA Lutmerding A Dudareva N Smith BH 2005 Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera) Journal of Comparative Physiology A ndash Neuroethology Sensory Neural and Behavioral Physiology 191 105ndash114

Wu SQ Schalk M Clark A Miles RB Coates R Chappell J 2006 Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants Nature Biotechnology 24 1441ndash1447

Wuebbles DJ Grant KE Connell PS Penner JE 1989 The role of atmospheric chemistry in climate change Japca ndash the Journal of the Air amp Waste Management Association 39 22ndash28

Xiang L Milc J Pecchioni N Chen L 2007 Genetic aspects of floral fragrance in plants Biochemistry (Moscow) 72 351ndash358

Yahyaoui FEL Wongs-Aree C Latche A Hackett R Grierson D Pech JC 2002 Molecular and biochemical characteristics of a gene encoding an alcohol acyl-transferase involved in the generation of aroma volatile esters during melon ripening European Journal of Biochemistry 269 2359ndash2366

Yakir E Hilman D Harir Y Green RM 2007 Regulation of output from the plant circadian clock FEBS Journal 274 335ndash345

Ziosi V Bonghi C Bregoli AM Trainotti L Biondi S Sutthiwal S Kondo S Costa G Torrigiani P 2008 Jasmonate-induced transcriptional changes suggest a negative interference with the ripening syndrome in peach fruit Journal of Experimental Botany 59 563ndash573

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bull Regular papers Letters Research reviews Rapid reports and both ModellingTheory and Methods papers are encouragedWe are committed to rapid processing from online submission through to publication lsquoas-readyrsquo via Early View ndash our averagesubmission to decision time is just 29 days Online-only colour is free and essential print colour costs will be met if necessaryWe also provide 25 offprints as well as a PDF for each article

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Tansley review


Review28

Qualley amp Dudareva 2008) A number of low-molecular-weight (C lt 5) BVOCs are also emitted by plants for examplemethanol ethylene formaldehyde ethanol acetone andacetaldehyde (Kreuzwieser et al 1999 Fall 2003 Arguesoet al 2007) These pathways have been relatively well studiedand the routes of formation are now well understood (Fig 1)However the biochemical regulation and function of most ofthese compounds are not clearly known

BVOCs are released from above- and below-ground plantorgans In general flowers and fruits release the widest varietyof BVOCs with emission rates peaking on maturation(Dixon amp Hewett 2000 Knudsen et al 2006 Knudsen ampGershenzon 2006 Soares et al 2007) but leaves have thegreatest mass emission rates The vegetative parts of woodyplants are more likely to release diverse mixtures of terpenoidsincluding isoprene monoterpenes sesquiterpenes and somediterpenes (Owen et al 2001 Keeling amp Bohlmann 2006)whereas grass species emit relatively large amounts of oxygen-ated BVOCs and some monoterpenes (Kirstine et al 1998Fukui amp Doskey 2000) When plants are damaged theemissions of these compounds may be increased and otherso-called green leaf volatiles (C6 aldehydes and ketones) mayalso be produced (Fall et al 1999 Laothawornkitkul et al2008a) Biotic and abiotic stresses may also induce the pro-duction of some BVOCs such as terpenes methyl jasmonate(MeJA) and methyl salicylate (MeSA) from leaves themagnitude and quality of which depend on the type ofdamage (Takabayashi et al 1994 Seo et al 2001 Mithoferet al 2005 Laothawornkitkul et al 2008a) The majorclasses of BVOCs the major groups of BVOC-emittingplants and estimates of current and future fluxes into theatmosphere are shown in Table 1

The single most important BVOC in the Earth system isprobably isoprene (C5H8 2-methyl-13-butadiene) Its pro-duction and emission by plants were first described bySanadze (1956) and its effect on the physics and chemistry ofthe atmosphere was first described by Went (1960) (Table 2)Notwithstanding the dominance of isoprene the biosphereproduces and emits hundreds if not thousands of reactiveBVOCs into the atmosphere Of these probably a few tens toa hundred specific species have significant and discernibleeffects in the atmosphere Since the 1960s over 1000 peer-reviewed papers have been published on the biosynthesis roleand function of BVOCs in the biosphere and atmosphere Itis now clear that these compounds have important effectswithin plants between plants between plants and otherorganisms and in the atmosphere at the local regional andglobal scales

How and why plants synthesize BVOCs and what are theireffects or functions are of interest to at least three distinctscientific communities Atmospheric chemists are interestedin BVOC emissions in terms of their effects on atmosphericcomposition and on the atmospherersquos chemistryndashclimate systemPlant biologists are interested in the functions of BVOCs in Ta

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Globularia alypum L








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1-yr-old plants


Table 3 continued

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O3 level (ppbv)

Fumigation period









Heiden et al (1999)

















Loreto et al (2004)



















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I ~ 55 (iso)







3 D ~ 20 (iso)

Ryan et al (2009)






D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

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V Synthesis





Acknowledgements


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 ESP 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 SUO ltFEFF004e00e4006900640065006e002000610073006500740075007300740065006e0020006100760075006c006c006100200076006f0069006400610061006e0020006c0075006f006400610020005000440046002d0061007300690061006b00690072006a006f006a0061002c0020006a006f006900640065006e002000740075006c006f0073007400750073006c00610061007400750020006f006e0020006b006f0072006b006500610020006a00610020006b007500760061006e0020007400610072006b006b007500750073002000730075007500720069002e0020005000440046002d0061007300690061006b00690072006a0061007400200076006f0069006400610061006e0020006100760061007400610020004100630072006f006200610074002d0020006a00610020004100630072006f006200610074002000520065006100640065007200200035002e00300020002d006f0068006a0065006c006d0061006c006c0061002000740061006900200075007500640065006d006d0061006c006c0061002000760065007200730069006f006c006c0061002egt ITA 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 NOR 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 SVE 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 gtgtgtgt setdistillerparamsltlt HWResolution [2400 2400] PageSize [612000 792000]gtgt setpagedevice

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Fumigation period




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Fumigation period




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O3 level (ppbv)

Fumigation period




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Fumigation period




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O3 level (ppbv)

Fumigation period




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Phytologist (2009)

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I ~ 55 (iso)







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O3 level (ppbv)

Fumigation period




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Phytologist (2009)

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I ~ 55 (iso)







3 D ~ 20 (iso)

Ryan et al (2009)






D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

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Phytologist (2009)

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I ~ 55 (iso)







3 D ~ 20 (iso)

Ryan et al (2009)






D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

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newphytologistorg


New

Phytologist (2009)

Review

40











1-yr-old plants


Table 3 continued

Tansley review

copy T

he Authors (2009)

New


pilation copy N


ww

wnew

phytologistorg

Review

41



O3 level (ppbv)

Fumigation period









Heiden et al (1999)

















Loreto et al (2004)



















Tansley review

New


The A

uthors (2009)w

ww

newphytologistorg


New

Phytologist (2009)

Review

42







I ~ 55 (iso)







3 D ~ 20 (iso)

Ryan et al (2009)






D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

Tansley review


Review 43










Tansley review


Review44


V Synthesis





Acknowledgements


References








Tansley review


Review 45








































Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review

copy T

he Authors (2009)

New


pilation copy N


ww

wnew

phytologistorg

Review

41



O3 level (ppbv)

Fumigation period









Heiden et al (1999)

















Loreto et al (2004)



















Tansley review

New


The A

uthors (2009)w

ww

newphytologistorg


New

Phytologist (2009)

Review

42







I ~ 55 (iso)







3 D ~ 20 (iso)

Ryan et al (2009)






D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

Tansley review


Review 43










Tansley review


Review44


V Synthesis





Acknowledgements


References








Tansley review


Review 45








































Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review

New


The A

uthors (2009)w

ww

newphytologistorg


New

Phytologist (2009)

Review

42







I ~ 55 (iso)







3 D ~ 20 (iso)

Ryan et al (2009)






D ~ 18 (iso)


O3 level (ppbv)

Fumigation period




Table 4 continued

Tansley review


Review 43










Tansley review


Review44


V Synthesis





Acknowledgements


References








Tansley review


Review 45








































Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review 43










Tansley review


Review44


V Synthesis





Acknowledgements


References








Tansley review


Review 45








































Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review44


V Synthesis





Acknowledgements


References








Tansley review


Review 45








































Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review 45








































Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review46







































Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review 47










































Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review48






































Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review 49













































Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review50










































Tansley review


Review 51















Tansley review


Review 51















Biogenic volatile organic compounds in the Earth system

Documents

Transcript of Biogenic volatile organic compounds in the Earth system