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Perspective
Harnessing Insect-Microbe Chemical Communications to Control Insect Pests of Agricultural Systems John J Beck, and Rachel L. Vannette J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.6b04298 • Publication Date (Web): 05 Nov 2016 Downloaded from http://pubs.acs.org on November 10, 2016
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Journal of Agricultural and Food Chemistry
Harnessing Insect-Microbe Chemical Communications to Control Insect Pests of Agricultural Systems
John J. Beck*,† and Rachel L. Vannette‡
†
Chemistry Research Unit, Center for Medical, Agricultural and Veterinary Entomology, Agricultural Research Service, U.S. Department of Agriculture, 1700 SW 23rd Drive, Gainesville, Florida, 32608, United States
‡
Department of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, California, 95616, United States
AUTHOR INFORMATION *Corresponding author (Tel: 352-374-5730. Fax: 352-374-5707. E-mail:
[email protected])
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Journal of Agricultural and Food Chemistry
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ABSTRACT:
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Insect pests cause serious economic, yield and food safety problems to managed crops
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worldwide. Compounding these problems, insect pests often vector pathogenic or toxigenic
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microbes to plants. Previous work has considered plant-insect and plant-microbe interactions
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separately. Although insects are well-understood to use plant volatiles to locate hosts,
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microorganisms can produce distinct and abundant volatile compounds which in some cases
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strongly attract insects. In this Perspective, we focus on the microbial contribution to plant
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volatile blends, highlighting the compounds emitted and the potential for variation in microbial
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emission. We suggest that these aspects of microbial volatile emission may make these
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compounds ideal for use in agricultural applications, as they may be more specific or enhance
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methods currently used in insect control or monitoring. Our survey of microbial volatiles in
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insect-plant interactions suggest that not only do these emissions signal host suitability, but may
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indicate a distinctive time frame for optimal conditions for both insect and microbe. Exploitation
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of these host-specific microbe semiochemicals may provide important microbe- and host-based
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attractants, and a basis for future plant-insect-microbe chemical ecology investigations.
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KEYWORDS: insect-microbe mutualism; microbial contamination; semiochemical; volatiles
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INTRODUCTION
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Insect pests are known to impose serious economic, yield, and food safety problems on managed
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crops worldwide. Many strategies have been used to control these pests, including bio-pesticides,
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natural enemies, trap crops, push-pull strategies, genetic modification, pheromone- and host
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plant volatile-based attractants, and pathogenic microbes, among others.1,2 One important
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strategy is the manipulation of insect behavior and movement through the use of volatile
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signals.3-5 The study of plant-insect interactions has revealed that volatile organic compounds
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often mediate insect movement, aggregation, and host location by herbivores, predators and
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parasitoids.6,7 Most studies and applications of volatile signals in agriculture to date focus on
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signals produced by plants and insects, but growing evidence suggests that microbes,8,9 including
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fungi,10,11 bacteria12 and viruses,13 which are often vectored by insects, may also directly emit or
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alter the emission of volatile signals that are used as semiochemicals by insects.
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In this Perspective, we highlight the fact that while research on insect volatile signaling and
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insect-plant-microbe interactions is increasing (Figure 1), the intersection and overlap of these
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fields is an understudied, but important and growing area of research. To illustrate this, we used
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the Web of Science to search for germane keywords using Boolean operators and modifiers, and
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queried over a 15-year time frame. For example, the number of peer-reviewed studies on insects
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and volatiles [I+V], and microbe-insect-plant interactions (microbe OR virus OR bacter* OR
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fung*) AND insect* AND plant* [(M/Vi/B/F)+I+P] (Figure 1) have increased dramatically in
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the past 15 years. In contrast, one can see that only in the last five years has the term volatile*
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been associated with this field of study [(M/Vi/B/F)+I+V+P]. Notably, fewer yet contain the
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terms “microbial volatile” OR “bacteri* volatile” OR “fung* volatile”
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[(MV/Vi/BV/FV)+I+V+P] (Figure 1), suggesting that the study of microbial-produced volatiles
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in these interactions is still in its infancy. Nevertheless, the increase in peer-reviewed scientific
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publications on volatile research has been mirrored by the inclusion of volatiles in professional
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conference sessions on agricultural topics in national and international venues. For example, the
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American Chemical Society AGRO Division has been hosting more symposia that include topics
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concerning volatiles and their applications (i.e., Natural Products as Biorational Pesticides in
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Agriculture, 2016; and, Natural Products for Pest Management, 2012, among others). These
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examples highlight the application of semiochemicals for use as biopesticides, non-pheromonal
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insect pest attractants, enhancements or adjuvants for pheromones, biomarkers for detection of
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plant disease, and repellents. Most of the work in the literature and sessions cited above has
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focused on insect and plant-produced volatile compounds; however, as discussed in this
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Perspective, microbial volatiles are on the rise and should also be included in more symposia. It
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should be noted that in general the frequency of publications of volatiles associated with specific
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microbes followed the trend fungi* > bacter* > virus*. Fungi* volatiles were slightly higher (ca.
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22%) than bacter* volatiles, and with virus* volatiles associated publications a distant third
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(
