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      Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator

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          Abstract

          The plant microbiome can influence plant phenotype in diverse ways, yet microbial contribution to plant volatile phenotype remains poorly understood. We examine the presence of fungi and bacteria in the nectar of a coflowering plant community, characterize the volatiles produced by common nectar microbes and examine their influence on pollinator preference. Nectar was sampled for the presence of nectar-inhabiting microbes. We characterized the headspace of four common fungi and bacteria in a nectar analog. We examined electrophysiological and behavioral responses of honey bees to microbial volatiles. Floral headspace samples collected in the field were surveyed for the presence of microbial volatiles. Microbes commonly inhabit floral nectar and the common species differ in volatile profiles. Honey bees detected most microbial volatiles tested and distinguished among solutions based on volatiles only. Floral headspace samples contained microbial-associated volatiles, with 2-ethyl-1-hexanol and 2-nonanone - both detected by bees - more often detected when fungi were abundant. Nectar-inhabiting microorganisms produce volatile compounds, which can differentially affect honey bee preference. The yeast Metschnikowia reukaufii produced distinctive compounds and was the most attractive of all microbes compared. The variable presence of microbes may provide volatile cues that influence plant-pollinator interactions.

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          Defensive function of herbivore-induced plant volatile emissions in nature.

          Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions from Nicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-alpha-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.
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            Wake Up and Smell the Roses: The Ecology and Evolution of Floral Scent

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              Microbial volatile emissions as insect semiochemicals.

              We provide a synthesis of the literature describing biochemical interactions between microorganisms and insects by way of microbial volatile organic compound (MVOC) production. We evaluated the functionality and ecological context of MVOC signals, and explored important metabolic pathways involved in MVOC production. The cosmopolitan distribution of microorganisms creates a context for frequent, and frequently overlooked, insect responses to microbial emissions. There are numerous instances of MVOCs being closely associated with insect feeding behaviors, but some MVOCs are also powerful repellants. Emissions from microorganisms in situ may signal aspects of habitat suitability or potential exposure to entomopathogens. In some ecosystems, bacterial or fungal volatiles can also incite insect aggregations, or MVOCs can resemble sexual pheromones that elicit mating and oviposition behaviors from responding insects. A single microorganism or MVOC can have different effects on insect behaviors, especially across species, ontogenies, and habitats. There appears to be a multipartite basis for insect responses to MVOCs, and complex tritrophic interactions can result from the production of MVOCs. Many biochemical pathways for behaviorally active volatile production by microbial species are conserved across large taxonomic groupings of microorganisms. In addition, there is substantial functional redundancy in MVOCs: fungal tissues commonly produce polyketides and short-chain alcohols, whereas bacterial tissues tend to be more commonly associated with amines and pyrazines. We hypothesize that insect olfactory responses to emissions from microorganisms inhabiting their sensory environment are much more common than currently recognized, and that these signals represent evolutionarily reliable infochemicals. Insect chemoreception of microbial volatiles may contribute to the formation of neutral, beneficial, or even harmful symbioses and provide considerable insight into the evolution of insect behavioral responses to volatile compounds.
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                Author and article information

                Journal
                New Phytologist
                New Phytol
                Wiley
                0028646X
                November 2018
                November 2018
                September 28 2017
                : 220
                : 3
                : 750-759
                Affiliations
                [1 ]Chemistry Research Unit; Center for Medical, Agricultural and Veterinary Entomology; Agricultural Research Service; United States Department of Agriculture; 1700 SW 23 Dr. Gainesville FL 32608 USA
                [2 ]Department of Entomology and Nematology; University of California, Davis; One Shields Ave. Davis CA 95616 USA
                [3 ]Mechanical and Aerospace Engineering; University of California, Davis; One Shields Ave. Davis CA 95616 USA
                Article
                10.1111/nph.14809
                28960308
                27b233ed-23da-4a12-9694-ac76d7fcca64
                © 2017

                http://doi.wiley.com/10.1002/tdm_license_1.1

                http://onlinelibrary.wiley.com/termsAndConditions#am

                http://onlinelibrary.wiley.com/termsAndConditions#vor

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