Abstract
Plants constitutively release volatile organic compounds (VOCs), but qualitatively and quantitatively alter their emission of VOCs in response to biotic and abiotic stresses. The blend of VOCs emitted reflects the physiological status of the plant. Plants may be exposed to the VOC blend emitted by their near neighbors and gain information that allows them to adjust their own defenses. These plant-plant interactions may potentially be exploited to protect crops from pests, but they can be disturbed by abiotic factors making the process sensitive to environmental perturbation. Despite numerous studies describing plant-plant interactions, relatively few have been conducted with agriculturally significant cultivated plant varieties under field conditions. Here we studied plant-plant interactions in a conspecific association of Brassica oleracea var. capitata (cabbage) and show that undamaged plants exposed to neighbors damaged by the herbivore Pieris brassicae are primed for stronger volatile emissions upon subsequent herbivore attack. We conducted a field study in an ozone free-air concentration enrichment (FACE) facility with ambient and elevated ozone levels and found that elevated tropospheric ozone significantly alters the priming of VOCs in receiver plants. We conclude that plant-plant interactions may prime defensive attributes of receiver plants under field conditions, but are impaired by ozone pollution. Therefore, when planning the manipulation of plant-plant interactions for agricultural purposes, the potential effects of atmospheric pollutants should be considered.
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References
Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J (2000) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277:305–310. doi:10.1006/bbrc.2000.3672
Blande JD, Holopainen JK, Li T (2010) Air pollution impedes plant-to-plant communication by volatiles. Ecol Lett 13:1172–1181. doi:10.1111/j.1461-0248.2010.01510.x
Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904. doi:10.1111/pce.12352
De Moraes C, Mescher M, Tumlinson J (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580. doi:10.1038/35069058
Egigu MC, Ibrahim MA, Yahya A, Holopainen JK (2010) Yeheb (Cordeauxia edulis) extract deters feeding and oviposition of Plutella xylostella and attracts its natural enemy. BioControl 55:613–624. doi:10.1007/s10526-010-9287-9
Egigu MC, Ibrahim MA, Yahya A, Holopainen JK (2011) Cordeauxia edulis and Rhododendron tomentosum extracts disturb orientation and feeding behavior of Hylobius abietis and Phyllodecta laticollis. Entomol Exp Appl 138:162–174. doi:10.1111/j.1570-7458.2010.01082.x
Engelberth J, Alborn H, Schmelz E, Tumlinson J (2004) Airborne signals prime plants against insect herbivore attack. P Natl Acad Sci USA 101:1781–1785. doi:10.1073/pnas.0308037100
Evans N, McAinsh M, Hetherington A, Knight M (2005) ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41:615–626. doi:10.1111/j.1365-313X.2004.02325.x
Farré-Armengol G, Peñuelas J, Li T, Yli-Pirilä P, Filella I, Llusia J, Blande JD (2016) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytol 209:152–160. doi:10.1111/nph.13620
Fuentes JD, Roulston TH, Zenker J (2013) Ozone impedes the ability of a herbivore to find its host. Environ Res Lett 8:014048. doi:10.1088/1748-9326/8/1/014048
Furlong MJ, Wright DJ, Dosdall LM (2013) Diamondback moth ecology and management: problems, progress, and prospects. Annu Rev Entomol 58:517–541. doi:10.1146/annurev-ento-120811-153605
Geneau CE, Wackers FL, Luka H, Daniel C, Balmer O (2012) Selective flowers to enhance biological control of cabbage pests by parasitoids. Basic Appl Ecol 13:85–93. doi:10.1016/j.baae.2011.10.005
Girling RD, Lusebrink I, Farthing E, Newman TA, Poppy GM (2013) Diesel exhaust rapidly degrades floral odours used by honeybees. Sci Rep 3:2779
Hasan F, Ansari MS (2011) Effects of different brassicaceous host plants on the fitness of Pieris brassicae (L.) Crop Prot 30:854–862. doi:10.1016/j.cropro.2011.02.024
Heil M, Adame-Álvarez RM (2010) Short signalling distances make plant communication a soliloquy. Biol Lett 6:843–845. doi:10.1098/rsbl.2010.0440
Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144. doi:10.1016/j.tree.2009.09.010
Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. P Natl Acad Sci USA 104:5467–5472. doi:10.1073/pnas.0610266104
Himanen SJ, Blande JD, Klemola T, Pulkkinen J, Heijari J, Holopainen JK (2010) Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants - a mechanism for associational herbivore resistance? New Phytol 186:722–732. doi:10.1111/j.1469-8137.2010.03220.x
Himanen SJ, Bui TNT, Maja MM, Holopainen JK (2015) Utilizing associational resistance for biocontrol: impacted by temperature, supported by indirect defence. BMC Ecol 15:16. doi:10.1186/s12898-015-0048-6
Holopainen JK, Blande JD (2013) Where do herbivore-induced plant volatiles go? Front Plant Sci 4:185. doi:10.3389/fpls.2013.00185
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184. doi:10.1016/j.tplants.2010.01.006
Kaplan I (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biol Control 60:77–89
Karban R, Shiojiri K, Huntzinger M, McCall A (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930. doi:10.1890/0012-9658(2006)87[922:DRISVA]2.0.CO;2
Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52. doi:10.1111/ele.12205
Karnosky DF, Werner H, Holopainen T, Percy K, Oksanen T, Oksanen E, Heerdt C, Fabian P, Nagy J, Heilman W, Cox R, Nelson N, Matyssek R (2007) Free-air exposure systems to scale up ozone research to mature trees. Plant Biol 9:181–190. doi:10.1055/s-2006-955915
Kessler A, Baldwin I (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. doi:10.1126/science.291.5511.2141
Khaling E, Li T, Holopainen J, Blande J (2016) Elevated ozone modulates herbivore-induced volatile emissions of Brassica nigra and alters a tritrophic interaction. J Chem Ecol 42(5):368–381. doi:10.1007/s10886-016-0697-8
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. doi:10.1016/j.envpol.2015.01.019
Kollist T, Moldau H, Rasulov B, Oja V, Ramma H, Huve K, Jaspers P, Kangasjärvi J, Kollist H (2007) A novel device detects a rapid ozone-induced transient stomatal closure in intact arabidopsis and its absence in abi2 mutant. Physiol Plantarum 129:796–803. doi:10.1111/j.1399-3054.2006.00851.x
Li T, Blande JD (2015) Associational susceptibility in broccoli: mediated by plant volatiles, impeded by ozone. Glob Change Biol 21:1993–2004. doi:10.1111/gcb.12835
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. doi:10.1007/s10886-015-0624-4
McFrederick QS, Fuentes JD, Roulston T, Kathilankal JC, Lerdau M (2009) Effects of air pollution on biogenic volatiles and ecological interactions. Oecologia 160:411–420. doi:10.1007/s00442-009-1318-9
McFrederick QS, Kathilankal JC, Fuentes JD (2008) Air pollution modifies floral scent trails. Atmos Environ 42:2336–2348. doi:10.1016/j.atmosenv.2007.12.033
Morawo T, Fadamiro H (2014) Attraction of two larval parasitoids with varying degree of host specificity to single components and a binary mixture of host-related plant volatiles. Chemoecology 24:127–135. doi:10.1007/s00049-014-0154-5
Paoletti E, De Marco A, Beddows DCS, Harrison RM, Manning WJ (2014) Ozone levels in european and USA cities are increasing more than at rural sites, while peak values are decreasing. Environ Pollut 192:295–299. doi:10.1016/j.envpol.2014.04.040
Peng J, van Loon JJA, Zheng S, Dicke M (2011) Herbivore-induced volatiles of cabbage (Brassica oleracea) prime defence responses in neighbouring intact plants. Plant Biol 13:276–284. doi:10.1111/j.1438-8677.2010.00364.x
Pinto DM, Blande JD, Souza SR, Nerg AM, Holopainen JK (2010) Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmospheres: the ecological effects. J Chem Ecol 36:22–34. doi:10.1007/s10886-009-9732-3
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. Environ Pollut 156:227–231. doi:10.1016/j.envpol.2007.12.009
Pinto DM, Tiiva P, Miettinen P, Joutsensaari J, Kokkola H, Nerg AM, Laaksonen A, Holopainen JK (2007) The effects of increasing atmospheric ozone on blogenic monoterpene profiles and the formation of secondary aerosols. Atmos Environ 41:4877–4887. doi:10.1016/j.atmosenv.2007.02.006
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. doi:10.1111/pce.12301
Quintana-Rodriguez E, Morales-Vargas AT, Molina-Torres J, Adame-Álvarez RM, Acosta-Gallegos JA, Heil M (2015) Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J Ecol 103:250–260. doi:10.1111/1365-2745.12340
Smid H, van Loon J, Posthumus M, Vet L (2002) GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12:169–176. doi:10.1007/PL00012665
Sugimoto K, Matsui K, Iijima Y, Akakabe Y, Muramoto S, Ozawa R, Uefune M, Sasaki R, Alamgir KM, Akitake S, Nobuke T, Galis I, Aoki K, Shibata D, Takabayashi J (2014) Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. P Natl Acad Sci USA 111:7144–7149. doi:10.1073/pnas.1320660111
Tsao R, Zhou T (2000) Antifungal activity of monoterpenoids against postharvest pathogens Botrytis cinerea and Monilinia fructicola. J Essent Oil Res 12:113–121
Turlings TCJ, Loughrin JH, Mccall PJ, Rose USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. P Natl Acad Sci USA 92:4169–4174. doi:10.1073/pnas.92.10.4169
Vuorinen T, Nerg AM, Holopainen JK (2004) Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signalling. Environ Pollut 131:305–311. doi:10.1016/j.envpol.2004.02.027
Wilkinson S, Mills G, Illidge R, Davies WJ (2012) How is ozone pollution reducing our food supply? J Exp Bot 63:527–536. doi:10.1093/jxb/err317
Zebelo SA, Matsui K, Ozawa R, Maffei ME (2012) Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Sci 196:93–100. doi:10.1016/j.plantsci.2012.08.006
Acknowledgments
We thank Timo Oksanen, Marjatta Puurunen and Topi Kuronen for providing technical support. This research was supported by the Academy of Finland decision numbers 256050, 251898 and 283122.
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Giron-Calva, P.S., Li, T. & Blande, J.D. Volatile-Mediated Interactions between Cabbage Plants in the Field and the Impact of Ozone Pollution. J Chem Ecol 43, 339–350 (2017). https://doi.org/10.1007/s10886-017-0836-x
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DOI: https://doi.org/10.1007/s10886-017-0836-x