Harnessing Insect–Microbe Chemical Communications To Control

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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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Journal of Agricultural and Food Chemistry

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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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Journal of Agricultural and Food Chemistry

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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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(