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A New Modeling Approach for Estimating Abiotic and Biotic Stress-Induced De Novo Emissions of Biogenic Volatile Organic Compounds from Plants

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A New Modeling Approach for Estimating Abiotic and Biotic Stress-Induced De Novo Emissions of Biogenic Volatile Organic Compounds from Plants ORIGINAL RESEARCH published: 25 June 2019 doi: 10.3389/ffgc.2019.00026 A New Modeling Approach for Estimating Abiotic and Biotic Stress-Induced de novo Emissions of Biogenic Volatile Organic Compounds From Plants Rüdiger Grote 1*, Monica Sharma 2,3, Andrea Ghirardo 3 and Jörg-Peter Schnitzler 3 1 Institute of Meteorology and Climate Research - Atmospheric Environmental Research, Karlsruhe Institute of Technology, Garmisch-Partenkirchen, Germany, 2 Faculty of Geosciences, Geoengineering and Mining, Technische Universität Bergakademie Freiberg, Freiberg, Germany, 3 Research Unit Environmental Simulation (EUS), Helmholtz Zentrum München, Munich, Germany The emission of biogenic volatile organic compounds (BVOCs) is usually thought to depend on species-specific emission capacities that vary with seasonal and phenological conditions. Actual—so called constitutive—emissions are then calculated from prevailing temperature and radiation. However, various abiotic and biotic stressors such as ozone, Edited by: extreme radiation and temperature conditions, as well as wounding e.g., from insect Silvano Fares, Council for Agricultural and feeding, can lead to de-novo emissions of stress-induced BVOCs (sBVOCs) that may Economics Research, Italy excel constitutive emissions by more than an order of magnitude. These emissions Reviewed by: often have a considerable different compound composition and are short-lived but can Steffen M. Noe, Estonian University of Life prolong under continuous stress for quite some time. Thus, they may easily have a Sciences, Estonia large impact on overall regional BVOC emissions. However, sBVOCs are generally not Guy Schurgers, considered in models since up to date no consistent mechanism has been proposed. University of Copenhagen, Denmark This manuscript suggests a new mechanism based on the finding that sBVOCs *Correspondence: Rüdiger Grote originate from a handful of biosynthetic pathways which synthesize compounds in the [email protected] groups of monoterpenes, sesquiterpenes, and green leave volatiles, as well as methyl salicylate, ethanol/acetaldehyde, methanol/formaldehyde, and acetone. Isoprene is also Specialty section: This article was submitted to considered but since it is often constitutively emitted, the specific role of stress induction Forests and the Atmosphere, is difficult to determine for this compound. A function is proposed that describes the a section of the journal production of all de-novo sBVOCs sufficiently well and scales with stress intensity. It Frontiers in Forests and Global Change is hypothesized that the response delay and the form of the function is specific for Received: 06 March 2019 the production pathway and valid for ozone as well as wounding (herbivory) induced Accepted: 20 May 2019 stress. Model parameters are then derived from pooled literature data based on a meta- Published: 25 June 2019 analysis of suitable induction-response measurements of different plant species. The Citation: Grote R, Sharma M, Ghirardo A and overall emission amount derives from the intensity and frequency of the stress impulse. Schnitzler J-P (2019) A New Modeling We present a number of literature studies that are used to parameterize the new model as Approach for Estimating Abiotic and well as a selection of evaluations for single- and multiple-stress inductions. Furthermore, Biotic Stress-Induced de novo Emissions of Biogenic Volatile Organic coupling and interaction with constitutive emission models as well as limitations and Compounds From Plants. possible further developments are discussed. Front. For. Glob. Change 2:26. doi: 10.3389/ffgc.2019.00026 Keywords: ozone impact, herbivory, wounding, oxidative stress, induced emissions, BVOCs, modeling Frontiers in Forests and Global Change | www.frontiersin.org 1 June 2019 | Volume 2 | Article 26 Grote et al. Modeling Stress-Induced BVOC Emissions INTRODUCTION fact, many of the volatile terpenes that serve as antioxidative defenses, are also non-specific toxins active against a wide Volatile organic compounds (VOCs) are important precursors range of organisms (bacteria, fungi, plants, and animals) (Meena for the formation of tropospheric ozone and secondary aerosols et al., 2017). Nevertheless, the large variety of the emitted (Shallcross and Monks, 2000; Atkinson and Arey, 2003). compounds and the species-specific as well as stress-specific Excessively high ozone concentrations in the lower atmosphere emission intensity results in a multitude of different possible are representing a considerable threat to human health, causing blends (Kravitz et al., 2016). yield losses in agriculture and forestry, and reduce carbon Numerous structurally quite different molecules can be sequestration as well as other ecosystem services (Wilkinson produced but oxygenated VOCs, and more specifically green et al., 2012; Lombardozzi et al., 2015; Silva et al., 2017). Secondary leaf volatiles (GLVs), constitute a general element in most aerosols or fine and ultrafine particles are also causing pulmonary blends of induced emissions, in particular aldehydes, alcohols diseases, directly affect the radiation regime of the atmosphere, and acetates (Blande et al., 2014). The emission is generally and are important cloud condensation nuclei (Riipinen et al., proportional to the extent of wounding (Mithöfer et al., 2005; 2012; Shrivastava et al., 2017). A considerable share of VOCs Niinemets et al., 2013; Portillo-Estrada et al., 2015) and occurs originates from biogenic emissions (BVOCs) (Laothawornkitkul in attached or detached leaves. Other relevant sBVOCs are et al., 2009). Therefore, in order to evaluate the most efficient the C11 homoterpene dimethyl-nonatriene (DMNT) and the air pollution reduction strategies, it is important to know the volatile benzoid methyl salicylate (MeSA). Emissions of DMNT quantity and composition of BVOC emissions from different have often been found in response to herbivore attack (e.g., plant sources and thus their spatial and temporal distribution. Vuorinen et al., 2004b; Ibrahim et al., 2008; Tholl et al., 2011; BVOC emissions have been studied since the late 1980’s and Copolovici et al., 2014) but also as a response to ozone (Behnke relationships between some main compounds and environmental et al., 2009; Carriero et al., 2016). Similarly, MeSA is often conditions have been quantified for many plant species. associated with ozone responses (e.g., Hartikainen et al., 2012; This led to the general distinction between constitutive and Cardoso-Gustavson et al., 2014; Li et al., 2017; Bison et al., 2018) induced emissions, assuming continuously developing boundary but is similarly common in herbivore induced emission blends conditions to drive the first, and oxidative and mechanical (Vuorinen et al., 2007; Kigathi et al., 2009). Since isoprene and stress to trigger the second (Litvak and Monson, 1998; Brilli terpenoids help to mitigate any kind of membrane damage, their et al., 2009; Ali et al., 2011; Joo et al., 2011; Jiang et al., 2016; production may be induced or upregulated in response to abiotic Copolovici et al., 2017). Constitutive emissions are described as well as biotic stress (Litvak et al., 1999; Prieme et al., 2000; based on genetically determined emission potentials and the Brilli et al., 2011; Achotegui-Castells et al., 2013; Faiola et al., ability to form compound-specific VOC storages in different 2015; Semiz et al., 2017; Kanagendran et al., 2018b; Visakorpi types of plant tissues and organs. Various environmental et al., 2018) but may also been downregulated in favor of GLVs conditions are responsible for the expression of this species- (Brilli et al., 2009; Copolovici et al., 2017). The up-regulation specific potential, from which temperature and radiation are the of terpenoids have been found to increase the emissions by most important ones, both for short- and longer-term impacts. a factor of ∼10–20 in response to needle damages of feeding Water availability affects BVOC emission directly and indirectly insects (Ghimire et al., 2017) as well as to bark beetle infestations and may act in different directions dependent on stress severity. (Amin et al., 2012, 2013). CO2 and nutrient availability do also change BVOC emission Similar to constitutive emissions, induced compounds may be intensity but possible connections to production pathways are de-novo produced or released from storages when the diffusive numerous and the exact mechanism is yet not fully elucidated resistance is decreased by wounding of any kind. In some plant (Grote et al., 2013). species, storages in specific tissues occur from which volatiles In contrast, BVOC emissions may also occur as responses can be released that reduce the attractiveness of tissues for to specific stressors. Such stressors can be oxidative stress herbivores and protect wounds from getting infected by microbes originating from excessive light, temperature and air pollutants, and fungi. As far as we know, not all stored compounds but or mechanical stress such as biting, sucking, cutting, or wounding only monoterpenes are released from such storages (Litvak and including abrasion due to wind movement (Haase et al., 2011) Monson, 1998; Clancy et al., 2016), possibly because of their and membrane damages due to freeze/thaw cycles (Fall et al., antibiotic properties (e.g., Michelozzi, 1999). Therefore, most 2001). Although the drivers can be abiotic or biotic, the plant induced BVOCs are directly emitted after production but a internal signal cascades and thus the responses of plants are clear differentiation
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