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Elevated Ozone Modulates Herbivore-Induced Volatile Emissions of Brassica nigra and Alters a Tritrophic Interaction

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Abstract

Plants damaged by herbivores emit volatile organic compounds (VOCs) that are used by parasitoids for host location. In nature, however, plants are exposed to multiple abiotic and biotic stresses of varying intensities, which may affect tritrophic interactions. Here, we studied the effects of ozone exposure and feeding by Pieris brassicae larvae on the VOCs emitted by Brassica nigra and the effects on oriented flight of the parasitoid Cotesia glomerata. We also investigated the oriented flight of C. glomerata in a wind-tunnel with elevated ozone levels. Herbivore-feeding induced the emission of several VOCs, while ozone alone had no significant effect. However, exposure to 120 ppb ozone, followed by 24 hr of herbivore-feeding, induced higher emissions of all VOCs as compared to herbivore-feeding alone. In accordance, herbivore-damaged plants elicited more oriented flights than undamaged plants, whereas plants exposed to 120 ppb ozone and 24 hr of herbivore-feeding elicited more oriented flights than plants subjected to herbivore-feeding alone. Ozone enrichment of the wind-tunnel air appeared to negatively affect orientation of parasitoids at 70 ppb, but not at 120 ppb. These results suggest that the combination of ozone and P. brassicae-feeding modulates VOC emissions, which significantly influence foraging efficiency of C. glomerata.

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References

  • Alizadeh H, Behboudi K, Ahmadzadeh M, Javan-Nikkhah M, Zamioudis C, Pieterse CMJ, Bakker PAHM (2013) Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14. Biol Control 65:14–23

    Article  Google Scholar 

  • Atkinson R, Arey J (1998) Atmospheric chemistry of biogenic organic compounds. Acc Chem Res 31:574–583

    Article  CAS  Google Scholar 

  • Atkinson R, Arey J (2003) Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review. Atmos Environ 37:S197–S219

    Article  CAS  Google Scholar 

  • Baldwin IT (2010) Plant volatiles. Curr Biol 20:R392–R397

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp J, Wisthaler A, Hansel A, Kleist E, Miebach M, Niinemets U, Schurr U, Wildt J (2005) Ozone induced emissions of biogenic VOC from tobacco: relationships between ozone uptake and emission of LOX products. Plant Cell Environ 28:1334–1343

    Article  CAS  Google Scholar 

  • Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calfapietra C, Pallozzi E, Lusini I, Velikova V (2013) Modification of BVOC emissions by changes in atmospheric (CO2) and air pollution. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions. Springer, Berlin, pp 253–284

    Chapter  Google Scholar 

  • Calogirou A, Larsen BR, Kotzias D (1999) Gas-phase terpene oxidation products: a review. Atmos Environ 33:1423–1439

    Article  CAS  Google Scholar 

  • Cardoza Y, Teal P, Tumlinson J (2003) Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environ Entomol 32:970–976

    Article  Google Scholar 

  • Cataldo F, Ursini O, Lilla E, Angelini G (2010) Ozonolysis of alpha-Pinene, beta-Pinene, d- and l- turpentine oil studied by chirooptical methods; some implications on the atmospheric chemistry of biogenic volatile organic compounds. Ozone Sci Eng 32:274–285

    Article  CAS  Google Scholar 

  • Copolovici L, Kännaste A, Remmel T, Vislap V, Niinemets Ü (2011) Volatile emissions from Alnus glutinosa induced by herbivory are quantitatively related to the extent of damage. J Chem Ecol 37:18–28

    Article  CAS  PubMed  Google Scholar 

  • de Rijk M, Dicke M, Poelman EH (2013) Foraging behavior by parasitoids in multi-herbivore communities. Anim Behav 85:1517–1528

    Article  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175

    Article  CAS  PubMed  Google Scholar 

  • Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324

    Article  CAS  PubMed  Google Scholar 

  • Farré-Armengol G, Peñuelas J, Li T, Yli-Pirilä P, Filella I, Llusià J, Blande JD (2015) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytol 209:152–160

    Article  PubMed  Google Scholar 

  • Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentes JD, Roulston TH, Zenker J (2013) Ozone impedes the ability of a herbivore to find its host. Environ Res Lett 8:014048

    Article  Google Scholar 

  • Fuhrer J (2009) Ozone risk for crops and pastures in present and future climates. Naturwissenschaften 96:173–194

    Article  CAS  PubMed  Google Scholar 

  • Girling RD, Lusebrink I, Farthing E, Newman TA, Poppy GM (2013) Diesel exhaust rapidly degrades floral odors used by honeybees. Sci Rep 3:2779

    Article  PubMed  PubMed Central  Google Scholar 

  • Girón-Calva PS, Li T, Koski T, Klemola T, Laaksonen T, Huttunen L, Blande JD (2014) A role for volatiles in intra- and inter-plant interactions in birch. J Chem Ecol 40:1203–1211

    Article  PubMed  Google Scholar 

  • Gols R (2014) Direct and indirect chemical defenses against insects in a multi-trophic framework. Plant Cell Environ 37:1741–1752

    Article  PubMed  Google Scholar 

  • Guidi L, Degl’Innocenti E, Martinelli F, Piras M (2009) Ozone effects on carbon metabolism in sensitive and insensitive Phaseolus cultivars. Environ Exp Bot 66:117–125

    Article  CAS  Google Scholar 

  • Heiden A, Hoffmann T, Kahl J, Kley D, Klockow D, Langebartels C, Mehlhorn H, Sandermann H, Schraudner M, Schuh G, Wildt J (1999) Emission of volatile organic compounds from ozone-exposed plants. Ecol Appl 9:1160–1167

    Article  Google Scholar 

  • Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144

    Article  PubMed  Google Scholar 

  • Hewitt CN, Kok GL, Fall R (1990) Hydroperoxides in plants exposed to ozone mediate air-pollution damage to alkene emitters. Nature 344:56–58

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous arthropods? Biol Rev 85:267–280

    Article  PubMed  Google Scholar 

  • Himanen SJ, Nissinen A, Auriola S, Poppy GM, Stewart CN Jr, Holopainen JK, Nerg A (2008) Constitutive and herbivore-inducible glucosinolate concentrations in oilseed rape (Brassica napus) leaves are not affected by Bt Cry1Ac insertion but change under elevated atmospheric CO2 and O3. Planta 227:427–437

    Article  CAS  PubMed  Google Scholar 

  • Himanen SJ, Nerg A, Nissinen A, Pinto DM, Stewart CN Jr, Poppy GM, Holopainen JK (2009) Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multi-trophic communication of transgenic insecticidal oilseed rape (Brassica napus). New Phytol 181:174–186

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JK, Blande JD (2013) Where do herbivore-induced plant volatiles go? Front Plant Sci 4:185

    Article  PubMed  PubMed Central  Google Scholar 

  • Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JK, Semiz G, Blande JD (2009) Life-history strategies affect aphid preference for yellowing leaves. Biol Lett 5:603–605

    Article  PubMed  PubMed Central  Google Scholar 

  • Joutsensaari J, Loivamäki M, Vuorinen T, Miettinen P, Nerg A, Holopainen JK, Laaksonen A (2005) Nanoparticle formation by ozonolysis of inducible plant volatiles. Atmos Chem Phys 5:1489–1495

    Article  CAS  Google Scholar 

  • Kangasjärvi J, Jaspers P, Kollist H (2005) Signaling and cell death in ozone-exposed plants. Plant Cell Environ 28(8):1021–1036

    Article  Google Scholar 

  • Kelly FJ, Mudway I, Krishna MT, Holgate ST (1995) The free radical basis of air pollution: focus on ozone. Respir Med 89:647–656

    Article  CAS  PubMed  Google Scholar 

  • Kessler A, Baldwin IT (2004) Herbivore-induced plant vaccination. Part I. the orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J 38:639–649

    Article  CAS  PubMed  Google Scholar 

  • Khaling E, Papazian S, Poelman EH, Holopainen JK, Albrectsen BR, Blande JD (2015) Ozone affects growth and development of Pieris brassicae on the wild host plant Brassica nigra. Environ Pollut 199:119–129

    Article  CAS  PubMed  Google Scholar 

  • Li T, Holopainen JK, Kokko H, Tervahauta AI, Blande JD (2012) Herbivore-induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants. Funct Ecol 26:1176–1185

  • Li T, Blande JD (2015) Associational susceptibility in broccoli: mediated by plant volatiles, impeded by ozone. Glob Chang Biol 21:1993–2004

    Article  PubMed  Google Scholar 

  • 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 Physiol 24:361–367

    Article  CAS  PubMed  Google Scholar 

  • Lusebrink I, Girling RD, Farthing E, Newman TA, Jackson CW, Poppy GM (2015) The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction. J Chem Ecol 41:904–912

    Article  CAS  PubMed  Google Scholar 

  • Moayeri HRS, Ashouri A, Poll L, Enkegaard A (2007) Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory. J Appl Entomol 131:326–332

    Article  CAS  Google Scholar 

  • Myhre G, Shindell D, Bréon F-M, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J-F, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and natural radiative forcing. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, pp 659–730

    Google Scholar 

  • Niinemets Ü, Kännaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci 4:229–237

    Article  Google Scholar 

  • Peng J, van Loon JJA, Zheng S, Dicke M (2011) Herbivore-induced volatiles of cabbage (Brassica oleracea) prime defence responses in neighboring intact plants. Plant Biol 13:276–284

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas J, Llusià J, Gimeno B (1999) Effects of ozone concentrations on biogenic volatile organic compounds emission in the Mediterranean region. Environ Pollut 105:17–23

    Article  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  • Pinto DM, Blande JD, Nykänen R, Dong W, Nerg A, Holopainen JK (2007a) Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? J Chem Ecol 33:683–694

    Article  CAS  PubMed  Google Scholar 

  • Pinto DM, Nerg A, Holopainen JK (2007b) The role of ozone-reactive compounds, terpenes, and green leaf volatiles (GLVs), in the orientation of Cotesia plutellae. J Chem Ecol 33:2218–2228

    Article  CAS  PubMed  Google Scholar 

  • Pinto DM, Blande JD, Souza SR, Nerg A, Holopainen JK (2010) Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmospheres: the ecological effects. J Chem Ecol 36:22–34

    Article  CAS  PubMed  Google Scholar 

  • Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, Jongema Y, van Loon JJA, Vet LEM, Harvey JA, Dicke M (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLOS Biol 10(11):e1001435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponzio C, Gols R, Pieterse CMJ, Dicke M (2013) Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct Ecol 27:587–598

    Article  Google Scholar 

  • Ponzio C, Gols R, Weldegergis BT, Dicke M (2014) Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant Cell Environ 37:1924–1935

    Article  PubMed  Google Scholar 

  • Räsänen JV, Yli-Pirilä P, Holopainen T, Joutsensaari J, Pasanen P, Kivimäenpää M (2012) Soil drought increases atmospheric fine particle capture efficiency of Norway spruce. Boreal Environ Res 17:21–30

    Google Scholar 

  • Riffell JA, Shlizerman E, Sanders E, Abrell L, Medina B, Hinterwirth AJ, Kutz JN (2014) Flower discrimination by pollinators in a dynamic chemical environment. Science 344:1515–1518

    Article  CAS  PubMed  Google Scholar 

  • Rostás M, Ton J, Mauch-Mani B, Turlings TCJ (2006) Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naive parasitoids. J Chem Ecol 32:1897–1909

    Article  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

  • Shaghaghian S, Niakousari M, Javadian S (2014) Application of ozone post-harvest treatment on kabkab date fruits: effect on mortality rate of Indian meal moth and nutrition components. Ozone Sci Eng 36:269–275

    Article  CAS  Google Scholar 

  • Sitch S, Cox PM, Collins WJ, Huntingford C (2007) Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 448:791–794

    Article  CAS  PubMed  Google Scholar 

  • Sousa AH, Faroni LRA, Silva GN, Guedes RNC (2012) Ozone toxicity and walking response of populations of Sitophilus zeamais (Coleoptera: Curculionidae). J Econ Entomol 105:2187–2195

    Article  CAS  PubMed  Google Scholar 

  • Stam JM, Kroes A, Li Y, Gols R, van Loon JJA, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713

    Article  CAS  PubMed  Google Scholar 

  • Tamò C, Roelfstra L, Guillaume S, Turlings TCJ (2006) Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid: a time-saving foraging strategy. J Anim Ecol 75:1091–1099

    Article  PubMed  Google Scholar 

  • The Royal Society (2008) Ground-level ozone in the 21st century: future trends, impacts and policy implications. Science policy 15/08

  • Velikova V, Fares S, Loreto F (2008) Isoprene and nitric oxide reduce damages in leaves exposed to oxidative stress. Plant Cell Environ 31:1882–1894

    Article  CAS  PubMed  Google Scholar 

  • Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38:650–663

    Article  CAS  PubMed  Google Scholar 

  • Vuorinen T, Nerg A, Holopainen JK (2004) Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signaling. Environ Pollut 131:305–311

    Article  CAS  PubMed  Google Scholar 

  • Weldegergis B, Zhu F, Poelman E, Dicke M (2014) Drought stress affects plant metabolites and herbivore preference but not host location by its parasitoids. Oecologia 177:701–713

    Article  PubMed  Google Scholar 

  • Wimp GM, Wooley S, Bangert RK, Young WP, Martinsen GD, Keim P, Rehill B, Lindroth RL, Whitham TG (2007) Plant genetics predicts intra-annual variation in phytochemistry and arthropod community structure. Mol Ecol 16:5057–5069

    Article  CAS  PubMed  Google Scholar 

  • Yuan JS, Himanen SJ, Holopainen JK, Chen F, Stewart CN Jr (2009) Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank University of Eastern Finland (UEF), Kuopio research garden staff for providing plants and insects and Timo Oksanen (UEF, Kuopio) for programming and maintaining the growth chambers and wind-tunnel. This work was supported by European Science Foundation; EUROCORES programme EuroVOL, which is supported by funds from the Academy of Finland (decision number 141053, 256050, 251898, and 283122).

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  1. Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 1627, FIN-70211, Kuopio, Finland

    Eliezer Khaling, Tao Li, Jarmo K. Holopainen & James D. Blande

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  1. Eliezer Khaling
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Khaling, E., Li, T., Holopainen, J.K. et al. Elevated Ozone Modulates Herbivore-Induced Volatile Emissions of Brassica nigra and Alters a Tritrophic Interaction. J Chem Ecol 42, 368–381 (2016). https://doi.org/10.1007/s10886-016-0697-8

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