Abstract
Plants induce volatile organic compounds (VOCs) after pathogen infection and exposure to a neighbouring infected plant. In a greenhouse, we measured VOCs from maize cv. ‘Prosna’ 3 or 7 d following foliar, or 42 d following soil, inoculation of Panteoa ananatis, a bacterial pathogen, as well as from uninfected neighbouring maize located 1 or 3 m from each infected plant treatment. We predicted the degree of VOC induction to be greatest 7 d post-foliar > 3 d post-foliar > 42 d post-soil inoculation; also, infected plant VOC induction > 1 m uninfected neighbour > 3 m uninfected neighbour. Maize infected by P. ananatis induced six common green leaf volatiles (GLVs), four common terpenes, and one common skikimic acid pathway derivative. Our results in general confirmed these two predictions, but there was an interaction. While 3 d post-foliar inoculated plants had greater VOC induction than an uninfected neighbour exposed 1 m from a 7 d post-foliar inoculated plant, 42 d post-soil inoculated plants had lower VOC induction than an uninfected neighbour exposed 1 m from a 3 d post-foliar inoculated plant. Thus, infected maize did not always emit higher VOC concentrations than uninfected maize exposed to an infected plant; it depended on the route of infection (foliar vs. soil inoculation) for the infected plant and which infected plant treatment was exposed to an uninfected plant. The VOC blend of maize cv. ‘Prosna’ after P. ananatis infection appears to be quantitatively different when compared to infection by a Fusarium spp. blend. The relevance of these maize VOC blend differences after infection by different pathogens needs to be studied, but our results suggest that maize responds with quantitatively different VOC blends depending on the infecting pathogen.
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Abbreviations
- BAC:
-
benzyl acetate
- CAR:
-
caryopyllene
- GLV:
-
green leaf volatile
- HAC:
-
hexenyl acetate
- HAL:
-
hexenal
- HOL:
-
hexenol
- IND:
-
indole
- LIN:
-
linalool
- MeSA:
-
methyl salicylate
- MYR:
-
myrcene
- OCI:
-
ocimene
- PIN:
-
pinene
- TSB:
-
tryptic soy broth
- VOC:
-
volatile organic compound
References
Bonello P, McNee WR, Storer AJ, Wood DL & Gordon TR, 2001. The role of olfactory stimuli in the location of weakened hosts by twig-infesting Pityophthorus spp. Ecol Entomol 26, 8–15.
Cardoza YJ, Albron HT & Tumlinson JH, 2002. In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28, 161–174.
Carr EA, Bonasera JM, Zaid M, Lorbeer JW & Beer SV, 2008. First report of bulb disease of onion caused by Pantoea ananatis in New York. Plant Dis 94, 916.
Choh Y, Shimoda T, Ozawa R, Dicke M & Takabayashi J, 2004. Exposure of lima bean leaves to volatiles from herbivore-induced conspecific plants results in emission of carnivore attractants: active or passive process? J Chem Ecol 30, 1305–1317.
Claflin LE, 2000. Diseases caused by Prokaryotes. In: White D.G. (ed.). Compendium of Corn Diseases, pp. 3–9. APS Press, St. Paul, MN, USA.
Coplin DL & Kado CI, 2001. Gram-negative bacteria — Pantoea. In: Schaad, N.W., Jones, J. B., & Chun, W. (ed.), Laboratory guide for identification of plant pathogenic bacteria, pp. 73–83. APS Press, St. Paul, MN, USA.
Coutinho TA & Venter SN, 2009. Pantoea ananatis: an unconventional plant pathogen. Mol Plant Pathol 10, 325–335.
D’Alessandro M, Held M, Triponez Y & Turlings TCJ, 2006. The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32, 2733–2748.
De Baere T, Verhelst R, Labit C, Verschraegen G, Wauters G, Claeys G & Vaneechoutte M. 2004. Bacteremic infection with Pantoea ananatis. J Clin Microbiol 42, 4393–4395.
De Lacy Costello BPJ, Evans P, Ewen RJ, Gunson HE, Jones PRH, Ratcliffe NM & Spencer-Phillips PTN, 2001. Gas chromatography-mass spectrometry analyses of volatile organic compounds from potato tubers inoculated with Phytophthora infestans or Fusarium coeruleum. Plant Pathol 50, 489–496.
Dicke M & Baldwin IT, 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15, 167–174.
Engelberth J, Alborn HT, Schmelz EA & Tumlinson JH, 2004. Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101, 1781–1785.
Gitaitis R, Walcott R, Culpepper S, Sanders H, Zolobowska L & Langston D, 2002. Recovery of Pantoea ananatis, causal agent of center rot of onion, from weeds and crops in Georgia, USA. Crop Prot 21, 983–989.
Gouinguené SP & Turlings TCJ, 2002. The Effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129, 1296–1307.
Hare JD, 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Ann Rev Entomol 56, 161–180.
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.
Hoballah ME, Köllner TG, Degenhart J & Turlings TCJ, 2004. Costs of induced volatile production in maize. Oikos 105, 168–180.
Hoballah ME & Turlings TCJ, 2005. The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J Chem Ecol 31, 2003–2018.
Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S & Morisaki H, 2009. Rice seeds as sources of endophytic bacteria. Microbes Environ 24 154–162.
Kido K, Adachi R, Hasegawa M, Yano K, Hikichi Y, Takeuchi S, Atsuchi T & Takikawa Y, 2008. Internal fruit rot of netted melon caused by Pantoea ananatis (= Erwinia ananas) in Japan. J Gen Plant Pathol 74, 302–312.
Kost C & Heil M, 2006. Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94, 619–628.
Kozak M, Bocianowski J, Sakwojć S & Wnuk A, 2010. Call for more graphical elements in statistical teaching and consultancy. Biometrical Letters 47, 157–68.
Krawczyk K, Kamasa J, Zwolinska A & Pospieszny H, 2010. First report of Pantoea ananatis associated with leaf spot disease of maize in Poland. J Plant Pathol 92, 807–811.
Paccola-Meirelles LD, Ferrera AS, Meirelles WF, Marriel IE & Casela CR, 2001. Detection of a bacterium associated with a leaf spot disease of maize in Brazil. J Phytopathol 149, 275–279.
Pérez-y-Terrón R, Villegas MC, Cuellar BA, Muñoz-Rojas J, Castañeda-Lucio M, Hernández-Lucas I & Bustillos-Cristales R, 2009. Detection of Pantoea ananatis, causal agent of leaf spot disease of maize, in Mexico. Australas Plant Dis Notes 4, 96–99.
Piesik D, Lemńczyk G, Skoczek A, Lamparski R, Bocianowski J, Kotwica K & Delaney KJ, 2011. Fusarium infection in maize: Volatile induction of infected and neighboring uninfected plants has the potential to attract a pest cereal leaf beetle, Oulema melanopus. J Plant Physiol 168, 1534–1542.
Piesik D, Łyszczarz A, Tabaka P, Lamparski R, Bocianowski J & Delaney KJ, 2010. Volatile induction of three cereals: influence of mechanical injury and insect herbivory on injured plants and neighbouring uninjured plants. Ann Appl Biol 157, 425–434.
Piesik D, Pánka D, Jeske M, Wenda-Piesik A, Delaney KJ & Weaver DK, 2013. Volatile induction of infected and neighboring uninfected plants potentially influence attraction/repellence of a cereal herbivore. J Appl Entomol 137, 296–309.
Piesik D, Rochat D, van der Pers J & Marion-Poll F, 2009. Pulsed odors from maize or spinach elicit orientation in European corn borer neonate larvae. J Chem Ecol 35, 1032–1042.
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon & Turlings TCJ, 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737.
Rostás M, Ton J, Mauch-Mani B & Turlings TCJ, 2006. Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naïve parasitoids. J Chem Ecol 32, 1897–1909.
SAS Institute 2007. SAS: STAT user’s guide: Statistics. SAS Institute, Cary, NC.
Schaad NW, Jones JB & Chun W, 2001. Laboratory guide for identification of plant pathogenic bacteria. 3rd. Ed. APS Press, St. Paul, MN, USA, 1–373.
Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J & Degenhardt J, 2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103, 1129–1134.
Schwachtje J & Baldwin IT, 2008. Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146, 845–851.
Shapiro SS & Wilk MB, 1965. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611.
Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G & Horiuchi J, 2006. Changing green leaf biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA, 103, 16672–16676.
Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G & Dorn S, 1998. The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11, 122–129.
Vikram A, Hamzehzarghani H & Kushalappa AC, 2005. Volatile metabolites from the headspace of onion bulbs inoculated with postharvest pathogens as a tool for disease discrimination. Can J Plant Pathol 27, 194–203.
Yi HS, Heil M, Adame-Álvarez RM, Ballhorn DJ & Ryu CM, 2009. Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol 151, 2152–2161.
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Delaney, K.J., Breza-Boruta, B., Lemańczyk, G. et al. Maize Voc Induction after Infection by the Bacterial Pathogen, Pantoea ananatis, Alters Neighbouring Plant Voc Emissions. J Plant Dis Prot 122, 125–132 (2015). https://doi.org/10.1007/BF03356541
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DOI: https://doi.org/10.1007/BF03356541