Identification of an insect-produced olfactory cue that primes plant defenses

It is increasingly clear that plants perceive and respond to olfactory cues. Yet, knowledge about the specificity and sensitivity of such perception remains limited. We previously documented priming of anti-herbivore defenses in tall goldenrod plants (Solidago altissima) by volatile emissions from a specialist herbivore, the goldenrod gall fly (Eurosta solidaginis). Here, we explore the specific chemical cues mediating this interaction. We report that E,S-conophthorin, the most abundant component of the emission of male flies, elicits a priming response equivalent to that observed for the overall blend. Furthermore, while the strength of priming is dose dependent, plants respond even to very low concentrations of E,S-conophthorin relative to typical fly emissions. Evaluation of other blend components yields results consistent with the hypothesis that priming in this interaction is mediated by a single compound. These findings provide insights into the perceptual capabilities underlying plant defense priming in response to olfactory cues.Plants are able to prime anti-herbivore defenses in response to olfactory cues of insect pests. Here, Helms et al. identify the insect pheromone E,S-conophthorin produced by the goldenrod gall fly as the specific chemical component that elicits this priming response in goldenrod plants.

[1]  K. Shinozaki,et al.  Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. , 2013, Journal of experimental botany.

[2]  J. Beck,et al.  Generation of the volatile spiroketals conophthorin and chalcogran by fungal spores on polyunsaturated fatty acids common to almonds and pistachios. , 2012, Journal of agricultural and food chemistry.

[3]  B. Burger Mammalian Semiochemicals , 2004 .

[4]  J. Ton,et al.  Primed plants do not forget , 2013 .

[5]  Y. Kivshar,et al.  Wide-band negative permeability of nonlinear metamaterials , 2012, Scientific Reports.

[6]  한성민,et al.  WDR5 promotes the tumorigenesis of oral squamous cell carcinoma via CARM1/β-catenin axis , 2021, Odontology.

[7]  D. Shibata,et al.  Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense , 2014, Proceedings of the National Academy of Sciences.

[8]  M. Mescher,et al.  Role of plant sensory perception in plant-animal interactions. , 2015, Journal of experimental botany.

[9]  K. Matsui,et al.  Intermittent exposure to traces of green leaf volatiles triggers a plant response , 2012, Scientific Reports.

[10]  D. Maddison,et al.  Coleoptera , 2006, Nature.

[11]  M. Mescher,et al.  The volatile emission of a specialist herbivore alters patterns of plant defence, growth and flower production in a field population of goldenrod , 2017 .

[12]  J. V. van Loon,et al.  Early herbivore alert matters: plant-mediated effects of egg deposition on higher trophic levels benefit plant fitness. , 2015, Ecology letters.

[13]  T. Tscharntke,et al.  Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours , 2000, Oecologia.

[14]  M. Mescher,et al.  Communicative interactions involving plants: information, evolution, and ecology. , 2016, Current opinion in plant biology.

[15]  C. Borgemeister,et al.  Coffee Berry Borer Joins Bark Beetles in Coffee Klatch , 2013, PloS one.

[16]  J. Borden,et al.  DIFFERENTIAL BIOACTIVITY OF CONOPHTHORIN ON FOUR SPECIES OF NORTH AMERICAN BARK BEETLES (COLEOPTERA: SCOLYTIDAE) , 2000, The Canadian Entomologist.

[17]  C. Pieterse,et al.  Recognizing Plant Defense Priming. , 2016, Trends in plant science.

[18]  F. Messina Comparative Biology of the Goldenrod Leaf Beetles, Trirhabda virgata LeConte and T. borealis Blake (Coleoptera: Chrysomelidae) , 1982 .

[19]  M. Whiteside,et al.  Signals and cues in the evolution of plant-microbe communication. , 2016, Current opinion in plant biology.

[20]  C. Pieterse,et al.  Costs and benefits of priming for defense in Arabidopsis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Dawn E. Hall,et al.  Footsteps from Insect Larvae Damage Leaf Surfaces and Initiate Rapid Responses , 2004, European Journal of Plant Pathology.

[22]  Ted C. J. Turlings,et al.  Indole is an essential herbivore-induced volatile priming signal in maize , 2015, Nature Communications.

[23]  Richard Karban,et al.  Explaining evolution of plant communication by airborne signals. , 2010, Trends in ecology & evolution.

[24]  M. Ginzel,et al.  The capacity of conophthorin to enhance the attraction of two Xylosandrus species (Coleoptera: Curculionidae: Scolytinae) to ethanol and the efficacy of verbenone as a deterrent , 2013 .

[25]  W. Kitching,et al.  A diverse suite of spiroacetals, including a novel branched representative, is released by female Bactrocera tryoni (Queensland fruit fly). , 2006, Chemical communications.

[26]  M. Heil,et al.  Volatile Dose and Exposure Time Impact Perception in Neighboring Plants , 2012, Journal of Chemical Ecology.

[27]  J. Carlson,et al.  Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. , 2008, The New phytologist.

[28]  A. Kacelnik,et al.  Pea Plants Show Risk Sensitivity , 2016, Current Biology.

[29]  S. Dötterl,et al.  Deceptive Ceropegia dolichophylla fools its kleptoparasitic fly pollinators with exceptional floral scent , 2015, Front. Ecol. Evol..

[30]  G. Laue,et al.  Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush , 2000, Oecologia.

[31]  W. Kitching,et al.  Spiroacetals in insects , 2001 .

[32]  J. Bronstein,et al.  Ecology and Evolution of a Tritrophic Interaction@@@Evolutionary Ecology across Three Trophic Levels: Goldenrods, Gallmakers, and Natural Enemies , 1998 .

[33]  M. Renton,et al.  Experience teaches plants to learn faster and forget slower in environments where it matters , 2014, Oecologia.

[34]  M. Mescher,et al.  Volatile Chemical Cues Guide Host Location and Host Selection by Parasitic Plants , 2006, Science.

[35]  F. Q. Ribeiro The meta-analysis , 2017, Brazilian journal of otorhinolaryngology.

[36]  U. Conrath,et al.  Priming for enhanced defense. , 2015, Annual review of phytopathology.

[37]  W. Kitching,et al.  Biosynthesis of insect spiroacetals. , 2009, Natural product reports.

[38]  G. Glauser,et al.  The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. , 2017, The New phytologist.

[39]  Christian Gieger,et al.  Correction: Corrigendum: Novel loci affecting iron homeostasis and their effects in individuals at risk for hemochromatosis , 2015, Nature Communications.

[40]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[41]  James D. Blande,et al.  Where do herbivore-induced plant volatiles go? , 2013, Front. Plant Sci..

[42]  W. Abrahamson,et al.  Energetics of the Solidago Canadensis‐stem Gall Insect‐parasitoid Guild Interaction , 1979 .

[43]  W. Francke,et al.  Evidence that Cerambycid Beetles Mimic Vespid Wasps in Odor as well as Appearance , 2016, Journal of Chemical Ecology.

[44]  Junji Takabayashi,et al.  Herbivory-induced volatiles elicit defence genes in lima bean leaves , 2000, Nature.

[45]  R. Karban,et al.  Induced Plant Responses to Herbivory , 1989 .

[46]  P. Fernández,et al.  Male Sexual Behavior and Pheromone Emission Is Enhanced by Exposure to Guava Fruit Volatiles in Anastrepha fraterculus , 2015, PloS one.

[47]  B. Binder,et al.  How plants sense ethylene gas--the ethylene receptors. , 2014, Journal of inorganic biochemistry.

[48]  R. Dolferus,et al.  To grow or not to grow: a stressful decision for plants. , 2014, Plant science : an international journal of experimental plant biology.

[49]  Richard Karban,et al.  Volatile communication between plants that affects herbivory: a meta-analysis. , 2014, Ecology letters.

[50]  D. Hartnett,et al.  The effects of stem gall insects on life history patterns in Solidago canadensis L. (Compositae) , 1979 .

[51]  C. Kost,et al.  Herbivore‐induced plant volatiles induce an indirect defence in neighbouring plants , 2006 .

[52]  Brett A. Melbourne,et al.  Regional Contingencies in the Relationship between Aboveground Biomass and Litter in the World’s Grasslands , 2013, PloS one.

[53]  M. Heil,et al.  Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature , 2007, Proceedings of the National Academy of Sciences.

[54]  R. Karban,et al.  Geographic dialects in volatile communication between sagebrush individuals. , 2016, Ecology.

[55]  W. Kitching,et al.  Oxidative carbon-carbon bond cleavage is a key step in spiroacetal biosynthesis in the fruit fly Bactrocera cacuminata. , 2014, The Journal of organic chemistry.

[56]  M. Hilker,et al.  Plant responses to insect egg deposition. , 2015, Annual review of entomology.

[57]  S. Roy,et al.  Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley , 2014, BMC Plant Biology.

[58]  J. Tumlinson,et al.  Airborne signals prime plants against insect herbivore attack. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Beck Conophthorin from Almond Host Plant and Fungal Spores and Its Ecological Relation to Navel Orangeworm: a Natural Products Chemist's Perspective , 2017 .

[60]  Qing-He Zhang,et al.  Enantiospecific Antennal Response of Bark Beetles to Spiroacetal (E)-Conophthorin , 2002, Journal of Chemical Ecology.

[61]  U. Conrath Molecular aspects of defence priming. , 2011, Trends in plant science.

[62]  W. Kitching,et al.  Chemistry of fruit-flies. Spiroacetal-rich secretions in several Bactrocera species from the South-West Pacific region , 1992 .

[63]  F. Schiestl The evolution of floral scent and insect chemical communication. , 2010, Ecology letters.

[64]  L. Walling,et al.  The Myriad Plant Responses to Herbivores , 2000, Journal of Plant Growth Regulation.

[65]  The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding , 2014, BMC Plant Biology.

[66]  L. D. Uhler Biology and ecology of the goldenrod gall fly , 1951 .

[67]  John L. Orrock,et al.  Exposure of Unwounded Plants to Chemical Cues Associated with Herbivores Leads to Exposure-Dependent Changes in Subsequent Herbivore Attack , 2013, PloS one.

[68]  M. Heil,et al.  Short signalling distances make plant communication a soliloquy , 2010, Biology Letters.

[69]  C. M. De Moraes,et al.  Gall insects can avoid and alter indirect plant defenses. , 2008, The New phytologist.

[70]  J. Tumlinson,et al.  The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. , 2004, The Plant journal : for cell and molecular biology.

[71]  A. Nicotra,et al.  The Impact of Beneficial Plant-Associated Microbes on Plant Phenotypic Plasticity , 2013, Journal of Chemical Ecology.

[72]  Jeroen S. Dickschat,et al.  The scent of bacteria: headspace analysis for the discovery of natural products. , 2012, Journal of natural products.

[73]  Perception, signaling and molecular basis of oviposition-mediated plant responses , 2013, Planta.

[74]  G. Felton,et al.  Plants on early alert: glandular trichomes as sensors for insect herbivores. , 2009, The New phytologist.

[75]  M. Mescher,et al.  Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory , 2012, Proceedings of the National Academy of Sciences.

[76]  R. Karban The ecology and evolution of induced resistance against herbivores , 2011 .