Biogenic Volatile Organic Compounds and Climate Change

Biogenic Volatile Organic Compounds and Climate Change highlights the relationship between climate change and biogenic VOC and the impact they have on each other. Topics include the synthesis and emission of VOC in plants, how they respond to environmental stresses, how sustainable agricultural practices plants can be used to directly impact climate change beyond carbon sequestration, a review of biogenic VOCs as air pollutants, and the impact of biogenic VOC on clouds. This groundbreaking work is essential for anyone in climate change, global warming and cooling, atmospheric chemistry, clouds, fate and transport of chemicals in the atmosphere, air pollution, sustainability or agriculture.

• Explains how volatile organic compound (VOC) production and emission in plants can ameliorate the consequences of climate change induced abiotic and biotic stresses
• Comprehensively addresses the complex interactions between global warming, atmospheric composition and plant ecology beyond carbon sequestration
• Reviews the use of biogenic VOC in sustainability

• Language: English
• Publisher: Elsevier Science
• Release date: Jun 11, 2024
• ISBN: 9780128210772

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Preface

Federico Brilli and Stefano Decesari

Nowadays, climate change is deeply affecting our lives and reshaping nature in an unprecedented way. New climate trends inevitably influence the capacity of both terrestrial and aquatic organisms to produce biogenic volatile organic compounds (BVOCs). As a result, altered BVOC emissions will have complex feedback on the chemistry of the atmosphere which still needs to be properly understood. Moreover, the expected higher frequency and intensity of environmental stresses will negatively impact the productivity of plants. This demands an agriculture (r)evolution and alternative usage of aquatic ecosystems to feed a fast-growing population without further increasing the use of synthetic chemicals. Within this challenging context, BVOCs emitted from both plants and microbes represent an ideal and not yet fully exploited resource to enhance sustainable defense strategies and crop yield, and BVOCs produced by phytoplankton further add novel eco-friendly prospects and applications.

The study of BVOCs, by its very nature, has been always interdisciplinary. Over the years, the growing interest in BVOCs has continuously led to discoveries across scientific disciplines spanning from plant biology, microbiology, atmospheric chemistry, and physics as well as sustainable agriculture. However, at this time, the large knowledge available on BVOCs result sparse, as it has been treated in many separate books. The experts who pioneered the field, on the one hand, have amply discussed the physiological and ecological functions of BVOCs in plants by mainly considering forest species, while poor attention has been given to BVOCs emitted from aquatic (i.e., marine) ecosystems; on the other, the deepening of the impacts of BVOCs in climate chemistry has been often left out any biology-related topic. In addition, it has provided insights almost exclusively on the role of BVOCs in plant–insect interaction, with little concern for the BVOCs as infochemicals in multiorganism systems, including beneficial and pathogenic microbes, also belonging to the marine environment.

We decided to draw up this book to give a concise manual covering the basics as well as emerging aspects of BVOCs in biology, agriculture, atmospheric chemistry, and climatology. In particular, we summarized the biosynthesis and function of BVOCs over a wide range of organisms, including plants, microbes, and phytoplankton, and linked those with the impact of climate change–related abiotic factors, besides exploring the multiple functions of BVOCs in an eco-active chemosphere. To continue with providing comprehensive contributions to the study of BVOCs, we analyzed hot topics on the role of BVOCs in influencing, directly or indirectly, the ongoing climatic variations through ozone, secondary organic aerosol, and cloud formation. To the best of our knowledge, this book is among the first to provide a peculiar focus on the BVOC exploitation for improving plant defense against climate change–induced stresses in smart and sustainable agricultural activities, by also defining future perspectives for enhancing the resilience of agricultural and aquatic ecosystems.

This book has been realized by bringing together international scientists actively working in different research fields but having in common both expertise and passion for BVOC research. We have put our effort into designing a small set of chapters which comprehensively review the up-to-date issues regarding BVOC production and ecological function, how climate change will both affect and be affected by BVOCs, besides emphasizing the BVOC importance in future sustainable practices, which are as follows:

• Chapter 1 overviews the main pathways leading to the biosynthesis of different classes of BVOCs in plants, microbes, and phytoplankton

• Chapter 2 explores how the many cooccurring, and even extreme, environmental stressors associated with climate change may impact BVOC emissions

• Chapter 3 focuses on BVOC-mediated inter- and intra-specific signaling action that goes behind plant–insect interaction, by providing examples of multiorganism systems in terrestrial and marine habitats

• Chapter 4 aims at closing the gap between theoretical studies and real application of BVOCs in sustainable agriculture, in addition to highlighting innovative exploitations of BVOCs from aquatic ecosystems

• Chapter 5 examines the role of BVOCs in the formation of air pollutants and climate-forcing agents as ozone and particulate matter while discussing the sinks for such compounds provided by terrestrial vegetation

• Chapter 6 finally investigates BVOC–climate interactions by exploring the processes through which BVOC atmospheric chemistry influences the cloud systems and the global radiative forcing, as well as discussing the relevant feedback between climate change, land use change, BVOC emissions and the underlying biotic and abiotic drivers.

We believe this book might come in handy for a large audience of scholars of all levels working in biology who have an interest in the fate of BVOCs in the atmosphere within a global change scenario. At the same time, this book represents a reference text for atmospheric chemists and climatologists who would like to approach the study of BVOCs in plant stress biology, microbiology, and agroecology. We also feel this book would appeal to whoever seeks to exploit the great potential of BVOCs in future sustainable practices to address the challenge of both improving the productivity of terrestrial plants and exploiting aquatic ecosystems without negatively affecting the environment.

In conclusion, the broad vision of BVOCs offered by this book has the potential to connect researchers across new disciplines, which we hope will further strengthen the multidisciplinary and make the study of BVOCs even more fascinating.

Chapter 1

Synthesis and function of biogenic volatile organic compounds

Federico Brilli¹, Francesca Gallo² and Cecilia Balestreri³,    ¹Institute for Sustainable Plant Protection (IPSP) - National Research Council of Italy (CNR), Sesto Fiorentino (Firenze), Italy,    ²The National Aeronautics and Space Administration (NASA) - Langley Research Center, Hampton, VA, United States,    ³Department of Veterinary Population Medicine, University of Minnesota, St. Paul, MN, United States

Abstract

It will overview the main biochemical pathways leading to the production of the most relevant classes of biogenic volatile organic compounds (BVOCs) in plants, microbes, and marine phytoplankton. Terpenes are the most abundant class of BVOCs emitted in plants and can be constitutively synthesized both by the plastidial methylerythritol phosphate pathway and the cytosolic mevalonate pathway, following immediate emission or storage in specialized structures. A relevant amount of photosynthetically assimilated carbon is also employed in the shikimate pathway for the synthesis of phenylpropanoids and benzenoids. In all plant species, induction of the octadecanoid pathway following mechanical damage leads to the emission of a green leaves volatiles mixture. Moreover, methanol production is ubiquitously catalyzed in growing leaves by pectin methyl esterase, while oxygenated-BVOC (i.e., acetaldehyde, acetic acid, acetone, and ethanol) are synthesized in leaves through other enzymatic pathways. Microbes (bacteria and fungi) produce BVOCs through pathways featuring their primary and secondary metabolism, some of which are the same as in plants, but many biosynthetic steps remain mostly unknown.

In the marine environment, BVOCs are produced by microscopic organisms, called phytoplankton, through metabolic pathways similar to the ones used by terrestrial plants. The main BVOC produced by phytoplankton are dimethylsulfoniopropionate, isoprene, and halogenated carbon compounds, and they are characterized by seasonal and spatial variability.

Keywords

Methylerythritol phosphate pathway; MEP; mevalonate pathway; MVA; shikimate pathway; octadecanoid pathway; pectin methyl esterase (PME); microbial catabolic pathways; marine BVOC, halogenated carbon compounds

1.1 Plants

Plants are extraordinary factories able to emit a multitude (~1700) of biogenic volatile organic compounds (BVOCs) belonging to different chemical families (Dudareva et al., 2006). Despite the great diversity of plant BVOC, only a few pathways are responsible for their biosynthesis (Pichersky et al., 2006). All BVOC have in common a high vapor pressure, low boiling point, and low molecular weight (<300 Da), which make them either evaporate or diffuse above- and belowground at ambient conditions of temperature and pressure. Emission of BVOCs is spatially regulated, as BVOCs synthesis occurs in different plants’ organs, namely flowers (Knudsen et al., 2006; Farré-Armengol et al., 2020), leaves (Bracho-Nunez et al., 2011, 2013) and roots (Steeghs et al., 2004; Peñuelas et al., 2014; Delory et al., 2016). Biosynthesis and emission of BVOCs are also temporally separated due to the time that elapses between gene expression, enzyme production, and effective enzymatic activation by substrate availability (Dudareva et al., 2013). Constitutive emission of BVOCs, which occurs throughout the whole plant life cycle or during certain ontogenetic stages, characterized only some species (Kesselmeier and Staudt, 1999) and can be affected by the presence of other neighboring plants (Kigathi et al., 2019). However, BVOC mission can be induced in all plants following abiotic (see Chapter 2) and biotic (see Chapter 3) stresses. Hence, BVOCs play key physiological and ecological roles in defending plants against stresses (Kessler and Baldwin, 2001; Loreto and Schnitzler, 2010), and by modulating tri-trophic interactions involving plants, herbivores, and parasites (Dicke et al., 2009). In particular, BVOC orchestrate intra- and inter-plant communication (Frost et al., 2007; Heil and Karban, 2010) very specifically, both aboveground (De Moraes et al., 1998) and belowground (Rasmann and Turlings, 2008) (see Chapter 3). Because of the paramount role of BVOCs, which represent ~1% of all secondary metabolites, plants invest a substantial amount of carbon and energy for their synthesis from different cellular parts (Dudareva et al., 2004). The following sections discuss the few main pathways leading to the biosynthesis of terpenes (Section 1.1), phenylpropanoids and benzenoid (Section 1.2), as well as C6-aldehydes alcohols and esters (Section 1.3). In addition, the reactions catalyzed by cellular enzymes which produce oxygenated-BVOCs such as methanol (Section 1.4), acetaldehyde, ethanol, and acetone are described (Section 1.5).

1.1.1 Mevalonate and methylerythritol phosphate pathways

Terpenes (or isoprenoids) are the most diverse (Christianson, 2008) and abundant class of BVOCs (Table 1.1), whose release by the vegetation accounts for ~690 Tg/y, representing almost 50% of the overall emission of BVOCs (Guenther et al., 2012). Terpenes have lipophilic properties and are produced via two independent routes, namely the mevalonate (MVA) pathway (Rohmer, 1999) and the 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway (Lichtenthaler, 1999) (Fig. 1.1). The five-carbon isopentenyl diphosphate (IPP) and its allylic isomer dimethylallyl diphosphate (DMAPP) are the precursors of all terpenes (Table 1.2). The MEP pathway is exclusively located within the chloroplasts and generates both IPP and DMAPP starting from pyruvate and glyceraldehyde-3-phosphate (GA3P) through a sequence of seven enzymatic reactions (Vranová et al., 2013). The MVA pathway takes place mainly in the cytosol, but it has been found in other subcellular compartments (Simkin et al., 2011), and forms IPP from the condensation of two molecules of acetyl-CoA in an (acetoacetyl-CoA) intermediate, which is subsequently converted, first to 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA), and then to mevalonic acid. Despite the MVA and MEP pathways being spatially separated within the plant cells, cross-talks between these two biochemical routes have been observed in seedlings (Laule et al., 2003) and flowers (Dudareva et al., 2005), allowing IPP to be exchanged mainly from plastids to the cytosol (Laule et al., 2003; Bick and Lange, 2003; Hemmerlin et al., 2012). In plants, the condensation of DMADP and IPP originates from all-trasn and all-cis substrates (Table 1.2) that can be used by more than hundreds of terpenes synthases/cyclases (TPSs) enzymes, belonging to different sub-families (Degenhardt et al., 2009), to catalyze the formation of hemi- (C5H8), as well as acyclic or (mono-bi-tri-) cyclic mono- (C10H16), sesqui- (C15H24) and di- (i.e., C20H32) terpenes (Chen et al., 2011) (Table 1.1). TPSs can make multiple and diverse terpene carbon skeletons starting from the same prenyl diphosphates units, and thus are bonded to a wide range of substrates (Tholl, 2006), but always require a divalent metal ion (i.e., Mg²+ or Mn²+) to perform their activity (Bohlmann et al., 1998). In addition, oxidation, hydroxylation, dehydrogenation, and acylation reactions can modify the primary products of TPSs, thus increasing the diversification of the terpene structures (Zhou and Pichersky, 2020). For example, enzymatic oxidation of the sesquiterpene (E)-nerolidol and the diterpene (E,E)-geranyllinalool by specific P450 monooxygenases generates the C11 and C16 homoterpenes, (E)-3,8-dimethyl-1,4,7-nonatriene (DMNT) and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT), respectively (Richter et al., 2016). Despite the synthesis of terpenes occus both in above- and belowground plant parts, the terpene mixtures in leaves are completely different from that found in roots, due to tissue-specific expression profiles of TPS genes (Tholl and Lee, 2011).

Table 1.1

List of the main terpenes which have been investigated in the literature.

Figure 1.1 A simplified overview of the plastidial MEP and cytosolic MVA pathways leading to the synthesis of terpenes. In the chloroplast, the prime end-product of photosynthesis GA3P combined with pyruvate originating from PEP and, after a series of reactions involving enzymes such as DXP and DXR, forms the MEP intermediate which is then converted to IPP and then to DMAPP by isopentenyl pyrophosphate isomerase IDI. In the cytosol, acetyl-CoA (derived from pyruvate) originates the HMG-CoA intermediate, which is subsequently converted to MVA by HMGR, and then to IPP and DMAPP. Cross-talk between both pathways occurs through the export of IPP from the plastid to the cytosol. DMAPP, dimethylallyl pyrophosphate; DXP, 1-deoxy-D-xylulose 5-phosphate; DXR, 1-deoxy-D-xylulose 5-phosphate reductoisomerase; FPP, farnesyl pyrophosphate; GA3P, glyceraldehyde-3-phosphate; GGPP, geranylgeranyl diphosphate; GPP, geranyl pyrophosphate; HMG-CoA, 3-hydroxy-3-methylglutaryl-CoA; HMGR, HMG-CoA reductase; IPP, isopentenyl pyrophosphate; MEP, 2-C-methyl-D-erythritol; MEP, methylerythritol phosphate; MVA, mevalonic acid; PEP, phosphoenolpyruvate carboxylase; PQ-9, plastoquinone-9. Source: Designed by Rachele Ossola.

Table 1.2

List of the substrates employed by isoprene (IspS) and terpene (TPSs) synthases for the synthesis of terpenes.

1.1.1.1 Isoprene

In the chloroplasts, isoprene synthases (IspS) use DMAPP (Silver and Fall, 1995) to form isoprene (2-methyl-1,3-butadiene) (Sharkey et al., 2008). Isoprene synthases are unique among the other TPS as they display a higher temperature optimum (~44°C) (Rasulov et al., 2010) and a ten to hundred-fold higher substrate affinity (Schnitzler et al., 2005; Wolfertz et al., 2004) than both monoterpenes (Fischbach et al., 2000) and sesquiterpenes synthases (Tholl et al., 2001). Isoprene emission immediately follows its synthesis, and it occurs constitutively at high rates across different species of mosses (Hanson et al., 1999), ferns [e.g., Azolla spp.; (Brilli et al., 2022a)], herbaceous [i.e., Pureria lobata (Sharkey et al., 2005); Arundo spp. (Brilli et al., 2022b)] and trees [i.e., Populus spp. (Wiberley et al., 2008); Quercus spp. (Loreto et al., 2009)]. Isoprene emission is always light-dependent, being activated by photosynthetic energy (adenosine triphosphate, ATP; nicotinamide adenine dinucleotide phosphate, NADPH) (Loreto and Sharkey, 1993) as well as by electron flow (Niinemets et al., 1999), and requiring a pool of DMAPP synthesized primarily (~80–90%) from photosynthetically assimilated carbon channeled into the MEP pathway (Delwiche and Sharkey, 1993). Under non-stressful conditions, isoprene biosynthesis accounts for ~2% of the net assimilated carbon, and its emission rate can be controlled by the carbon flux through the MEP pathway that determines the pool size of DMADP (Rasulov et al., 2009), as well as by IspS amount and/or activity (Lantz et al., 2019). However, isoprene emission can be supported either by an extra-chloroplastic pool of DMAPP (Loreto et al., 2004) or alternative carbon sources present within the chloroplasts (i.e., starch) and/or transported from the xylem (i.e., carbohydrates) (Schnitzler et al., 2004; Karl et al., 2002), especially under stress (Brilli et al., 2007; de Souza et al., 2018). Although isoprene is a very reactive molecule, recent experiments carried out on red oak trees have demonstrated that its oxidation with reactive oxygen species (ROS), leading to the emission of methyl vinyl ketone (MVK) and methacrolein (MACR), does not occur within the leaf mesophyll (Cappellin et al., 2019), and therefore the biosynthetic origin of these carbonyl compounds remains enigmatic. It has been suggested that, after being emitted in the atmosphere, isoprene is oxidized to MVK and MACR and then absorbed by the leaves, where it is converted into methyl ethyl ketone (MEK) and further released into the atmosphere (Canaval et al., 2020).

Despite more than 50 years of research, the complex role of isoprene is still under debate (Sharkey and Monson, 2017). However, multiple physiological functions of isoprene have been already recognized in improving thermotolerance (Sharkey and Singsaas, 1995) of the thylakoid membranes (Velikova et al., 2011), particularly by maintaining both the functionality of the photosystem II (PSII) and the thylakoid membrane stiffness (Pollastri et al., 2019), besides affecting the network of genes involved in stress tolerance by acting as a signal molecule (Zuo, 2019). Isoprene has also been demonstrated to have an ecological role in interfering with herbivory feeding (Laothawornkitkul et al., 2008), as well as in the attraction of the natural enemy of herbivorous insects (Loivamäki et al., 2008). On the other hand, the low affinity of IspS enzymes for DMAPP inspired a theory according to which, by producing isoprene, IspS would prevent the excessive supply and accumulation of DMAPP that would otherwise unnecessarily waste phosphate, also justifying why IspS function only with high concentrations of DMAPP (Rosenstiel et al., 2004). Moreover, a recent study confirmed that root tissues are capable of emitting isoprene, further highlighting a ROS-mediating and signaling function of isoprene in belowground plant parts, which contributes to regulating plant developmental processes and response to environmental changes (Miloradovic van Doorn et al., 2020).

1.1.1.2 Mono-, sesqui-, and diterpenes

Always within the chloroplasts, the enzyme geranyl pyrophosphate (GPP) synthase catalyzes the combination of one molecule of IPP with one of DMAPP to form C10 GPP (Table 1.2), which is used by monoterpenes synthases as the universal precursor of all the monoterpenes (Gershenzon and Croteau, 1990). Monoterpenes synthases are mainly bound to the chloroplasts (Dong et al., 2015) and their activities regulate monoterpenes emission (Loreto et al., 2001). Following biosynthesis, pools of monoterpenes can be stored within specialized structures (including glandular trichomes, ducts, or glands) (Guenther et al., 1993). However, in some cases, monoterpenes can also be released immediately after their synthesis from freshly assimilated carbon—such for α-pinene, cis-β-ocimene in Quercus ilex (Loreto et al., 1996), and α-pinene, β-pinene, camphene, and limonene in other trees species (Ghirardo et al., 2010). Always in the chloroplasts, geranylgeranyl pyrophosphate synthase catalyzes the condensation of one molecule of DMAPP with three molecules of IPP forming geranylgeranyl diphosphate (GGPP) (Table 1.2), the C20 diphosphate precursor of all diterpenes. Despite the high molecular weight, the diterpenes karuene is emitted from plants (Otsuka et al., 2004), mainly from storage pools rather than synthesized de novo from photosynthetically fixed carbon (Yáñez-Serrano et al., 2018). One study reported constitutive biosynthesis of diterpenes (i.e., rhizathalenes) in roots of Arabidopsis plants, which is likely released out the peripherical root cells to exert both indirect priming activities in inducing defense responses within- and between plants, and a direct protective role against root-feeding insects (Vaughan et al., 2013).

In cytosol, the enzyme farnesyl pyrophosphate synthase catalyzes the combination of two molecules of IPP with DMAPP, thus leading to the formation of C15 farnesyl pyrophosphate (FPP) (Table 1.2), which is the precursor of all sesquiterpenes, the most common of which are β-caryophyllene, α- and β-farnesene, and α-humulene. However, the synthesis of sesquiterpenes has also been reported from precursors of the MEP pathway (Sallaud et al., 2009). The structural diversity of sesquiterpenes is higher than that of the monoterpenes because the greater length of the farnesyl chain allows for a larger number of cyclization processes in their backbone (Nagegowda, 2010). Sesquiterpenes, like mono- and di-terpenes, accumulate in internal or external storage structures of leaves (i.e., resin duct or glandular trichomes), especially in conifers and Laminacee species (Delatte et al., 2018), and can be also found within plant roots (Koo and Gang, 2012). Active transporters, similar to those found in flower petals, make these high molecular weight BVOCs move unidirectionally from the site of biosynthesis to the final storage cavity (Adebesin et al., 2017; Liao et al., 2023). This allows for their accumulation at high levels without the induction of toxic effects, through molecular mechanisms involving vesicular/membrane transport and/or soluble carrier proteins that have not yet been fully elucidated (Tissier et al., 2017). The emission of stored terpenes is uncoupled from the availability of photosynthetic intermediates, and it mostly depends on temperature, as increasing temperatures facilitate their evaporation out of storage structures (Niinemets et al., 2002). Nevertheless, several studies report the release of sesquiterpenes to depend on the light conditions, which highlighted how their emission rate could be directly regulated by biosynthesis [reviewed in Duhl et al. (2008)].

Besides being constrained by the availability of carbon and energy provided by primary photosynthetic metabolism, the production and emission of all terpenes are intricately related to the biosynthesis of other nonvolatile metabolites, precursors of major plant hormones, downstream to the MEP pathway such as cytokinins (Dani et al., 2021), gibberellins and other carotenoids-derivate hormones. Cytosolic FPP is also a substrate for the formation of sterols and brassinosteroids, whereas plastidic GGPP is employed for the synthesis of chlorophyll, carotenoid, strigolactone, abscisic acid (ABA) and gibberellins (Rodriguez-Concepcion, 2016). As a consequence, the carbon flow within the MEP pathway might be allocated with priority to the production of essential nonvolatile terpenes-derived metabolites which, in turn, limits the upstream biosynthetic reactions of volatile terpenes (Owen and Peñuelas, 2005), particularly in young developing leaves (Rasulov et al., 2014).

A deeper understanding of terpenes biosynthetic pathway and function has been achieved by the creation of genetically modified plants (Dudareva and Pichersky, 2008). Transgenic tobacco that became capable of emitting isoprene resulted in less damage to ozone exposure and with a higher photosynthetic rate than the respective non-emitting wild-type plants, as production of isoprene avoided excessive accumulation of ROS while increasing the antioxidant levels (Vickers et al., 2009b). Moreover, isoprene emission enhanced the tolerance of trasngenic tobacco plants against drought through a stimulation of both nonvolatile de-epoxidated xanthophylls and ABA, as well as sugars and phenylpropanoids (Tattini et al., 2014). On the other hand, in isoprene emitting poplars, down-regulation of genes expressing IspS which suppressed isoprene production, caused a reduction of phenolic compounds biosynthesis (Behnke et al., 2010) and increased the production of nonvolatile terpenes (i.e., lutein and β-carotene) (Ghirardo et al., 2014), likely as a mechanism to compensate for the for lack of antioxidant protective capacity isoprene. However, suppression of isoprene emission did not hamper photosynthetic function and the woody biomass production of hybrid-poplar trees (Monson et al., 2020). This has been explained as the consequence of both phenological response and compensatory changes in protein expression (i.e., up-regulation of pathways leading to terpenes, carotenoid, and α-tocopherol biosynthesis), this latter consistent with a reconfiguration of chloroplast proteins already reported in laboratory experiments (Velikova et al., 2014). Moreover, the use of genetically engineered isoprene-emitting Arabidopsis together with non-emitting poplar plants, and their respective wild-type genotypes, revealed correlations between isoprene and cytokinins transcriptional regulation and metabolism, which impact plant development, reproduction, and senescence (Dani et al., 2021). In another study, the genetic engineering of maize to synthesize sesquiterpene aboveground (i.e., (E)-ß-farnesene, (E)-α-bergamotene) resulted in improved plant defense against herbivores through the enhanced attraction of beneficial arthropods (Schnee et al., 2006), while belowground emission of (E)-ß-caryophyllene attracted entomopathogenic nematodes that protect plants against roots pests (Degenhardt et al., 2009).

Overall, the synthesis of terpenes has been postulated to help plants cope with oxidative stress by a unified mechanism which implies direct scavenging of ROS, indirect signaling through modulation of ROS levels, as well as stabilization of cellular membranes (Vickers et al., 2009a). In addition, a higher investment of photosynthetic carbon to synthesize either monoterpenes (Brilli et al., 2009; Litvak and Monson, 1998) or sesquiterpenes (Zhuang et al., 2012; Schnee et al., 2006; Ghirardo et al., 2012) following herbivory attack, demonstrated a multiple key role of terpenes in disguising plants from herbivores, as well as in deterring herbivores from plants, in addition to attract the natural enemies of herbivores (Gershenzon and Dudareva, 2007).

1.1.2 Shikimate pathway

In the cytosol of all plant cells, more than 30% of the photosynthetic carbon employed to synthesize phosphoenolpyruvate (PEP) and D-erythrose 4-phosphate (E4P) is channeled into the plastidic shikimate pathway (Maeda and Dudareva, 2012) for the production of both phenylpropanoids and benzenoids. These compounds are the second biggest group of BVOCs after terpenes, and they typically occur in floral scent (Knudsen et al., 2006), which exerts an ecological role in plant-pollinator relationships (Schiestl, 2010). However, synthesis of phenylpropanoids and benzenoids are also commonly found in plant roots and rhizomes, which take part in belowground tri-trophic interaction by repelling herbivores while attracting entomopathogenic nematodes to prevent biomass loss (Rasmann et al., 2011). Transcriptional control of genes encoding the enzymes of the shikimate pathway regulates the carbon flow through this metabolic route and, indirectly, balances the competition with the MEP pathway for common PEP and E4P intermediates (Tohge et al.,