Editorial pubs.acs.org/JAFC
Eavesdropping on Plant−Insect−Microbe Chemical Communications in Agricultural Ecology: A Virtual Issue on Semiochemicals
F
or 65 years, the Journal of Agricultural and Food Chemistry (JAFC) has been publishing high-quality, cutting-edge research on the production and protection of agriculture. In the charter issue of JAFC in 1953, the editors posed the question “will we be able to provide an adequate diet for the world’s population, now about 2.5 billion and growing...[?]”1 The introductory statement promoted the idea of teamwork between scientific disciplines by encouraging chemists and entomologists to work collaboratively. Sixty five volumes and five billion more people later, the idea of teamwork to protect agriculture remains important. Modern day challenges for agriculture are numerous and include biotic stressors (e.g., insects, parasitic nematodes, microbes, weeds, and increased resistance to pesticides) and abiotic stressors (e.g., drought, flood, extreme temperatures, increased carbon dioxide levels, and extreme weather).2 Challenges such as these require the continued combined efforts of experts in a wide range of scientific disciplines, including not only chemistry and entomology, but also biochemistry, chemical ecology, molecular biology, plant physiology, and soil science. Insect pests inflict serious economic, yield, and food safety problems on agriculture worldwide. One approach to protecting agriculture is to understand and apply knowledge of the chemical communication between insects and plants. Both plants and insects respond to chemical signals (semiochemicals), which has important implications for pest control.3,4 Studies of plant−insect interactions and, more recently, interactions among plants, insects, and microbes5 demonstrate that semiochemicals often facilitate insect movement, aggregation, and host location by herbivores, predators, and parasitoids,6,7 all of which can be used to protect agriculture. In this Virtual Issue on semiochemicals, we highlight important recent research into the complex network of volatile chemical communications among plants, insects, and microbes. Below, we present a brief overview of semiochemicals, why they are important for agriculture, and possible directions for semiochemical research as well as their use in protecting agriculture.
Figure 1. Different types of semiochemicals.
purposes, but the chemical basis of this communication is still being revealed. In the 2015 JAFC Research Article of the Year Award Lectureship winner [with American Chemical Society (ACS) Division of Agrochemicals], the authors reported on a plant−insect interaction study. To investigate host choice, the authors observed moth preference among four potential host species, analyzed volatile profiles of potential hosts, performed lab- and field-based bioassays, and, finally, formulated blends of host plant-based volatiles. This study highlights the importance of performing ecologically realistic trials and the challenge of complexity of chemical blends often necessary for relevance in field conditions. We also highlight a study performed in a unique and understudied system, where the authors used metabolic profiling to characterize potato root exudates among four potato cultivars that varied in susceptibility to a root pathogen. Metabolite profiling revealed a diverse group of compounds that were screened for bioactivity in pathogen spore germination. Although performed under controlled laboratory conditions, being able to influence pathogen spores is a potentially important ecological finding. The next four articles highlight plant−insect interactions, with varied approaches or plant−insect systems. These include nematodes, honey bees, multi-insect-stressed plant responses, and mosquito deterrents. The remaining articles focus on plant−microbe interactions and the volatiles involved in these interactions. Papers here also include biomarker fungal volatiles for detection of fungi in food tissue as well as possible semiochemicals for insects.
■
SEMIOCHEMICALS Semiochemicals8 are message-bearing chemicals that influence the behavior of organisms, and they are categorized as either pheromones or allelochemicals. Pheromones transmit signals within the same species, whereas allelochemicals are used for communication between different species (Figure 1). In nature as well as in agriculture, semiochemicals have many uses (Figure 2). This Virtual Issue covers three broad categories of semiochemicals: (1) plant-produced semiochemicals for plant−insect or plant−microbe interactions, (2) insect-produced semiochemicals for insect−insect and insect−plant interactions, and (3) microbe-produced semiochemicals for microbe−insect or microbe−plant interactions. Plant-Produced Semiochemicals. For decades, plants have been suspected of producing volatiles for communication © 2017 American Chemical Society
Published: June 28, 2017 5101
DOI: 10.1021/acs.jafc.7b02741 J. Agric. Food Chem. 2017, 65, 5101−5103
Journal of Agricultural and Food Chemistry
Editorial
Figure 2. Examples of uses for semiochemicals.
Insect-Produced Semiochemicals. Articles in this category deal primarily with insect pheromones, which remain a critical option for manipulating the behavior of agriculturally related insect pests. For example, one paper highlights a potential application of insect−mite interactions: the control of the honey bee ectoparasite Varroa destructor with bee-produced semiochemicals that could inhibit the mite’s detection of the bee. Another study uses a traditional approach to the isolation, identification, and field testing of the aggregation pheromone components of the four-spotted coconut weevil, an insect pest of numerous palm species. Communications between different species of insects in similar ecosystems hold an important research niche that warrants full exploitation as a means to control or influence agricultural insect pests and beneficial insects. Microbe-Produced Semiochemicals. Microbial volatiles are increasingly recognized as cues for insects and insect pests,5 for their contribution to volatile off-flavors in a variety of agricultural products and in mediating interactions among microorganisms, including pest microbes. In this section, highlighted papers describe microbial contributions to fruits or nut volatile blends, reflecting the state of the field as largely descriptive to date, and also discuss the implications and potential uses of microbial semiochemicals for application in agriculture. A Review suggests that beneficial microorganisms may produce semiochemicals that inhibit the activity of pathogenic organisms. Meanwhile, a Perspective discusses the emerging idea that microbe-produced, species-specific semiochemicals may be important cues for insects and plants as well as for their mutualistic interactions with microbes. Although some insect−microbe relationships are known (e.g., bark beetles and fungal symbionts) and microbe-produced semiochemicals have been reported within the literature, this area remains a rich source of semiochemicals, particularly for agriculture plant−insect−microbe systems.
Virtual Issue, other past JAFC articles highlighting this include attractants for insect pests that can be used for monitoring insect populations or in attract and kill baits,10 enhancing the response of the insect to pheromones as a requisite contextual background odor,11 attracting beneficial insects, such as pollinators or parasitoids,12 repellents,13 and biomarkers of biotic or abiotic stressors of plants.14 Volatiles can also play a role in sustainable alternatives to pesticides. Biopesticides, for instance, are often plant-derived and have several benefits over their synthetic counterparts, such as reduced toxicity, specificity toward certain pest species, and lower chances of resistance.15 As a result of the combined efforts of scientists across numerous disciplines and several decades since the discovery of the first pheromone in 1959, a wide range of semiochemical-based products are now commercially available to manage insect pests in agriculture. However, the need for new semiochemicals to control insect pests is still significant, especially for controlling non-native pests. A recent estimate of non-native insect and pathogen damage to U.S. forest and crops puts the cost at nearly $40 billion per year.16
■
FUTURE OF SEMIOCHEMICALS “Agriculture...is our wisest pursuit, because it will in the end contribute most to real wealth, good morals and happiness” Thomas Jefferson The agricultural industry faces innumerable challenges, including invasive pests. It is projected that, as a result of globalization and world trade, invasive insects will be an increasing threat to agriculture globally.16 Thus, it is critical that research is performed to understand and ultimately manipulate the chemical communication between agriculture-related organisms. To help address this, collaborative research between scientists and institutions from different countries can help identify potential attractants for likely non-native agriculture insect pests before they arrive in a local area.17,18 It is anticipated that microbe-produced semiochemicals will play increased roles in the protection and production of agriculture.5 Of particular agricultural interest is pollinator interactions and their health,19 as demonstrated by the study on honey bees and kiwifruit odors. An upcoming important area of study with regard to pollinators is the influence of
■
IMPORTANCE OF SEMIOCHEMICALS “What Is Not Good for the Beehive, Cannot Be Good for the Bees” Marcus Aurelius Semiochemicals are an important component of agricultural ecosystems, mediating numerous interactions among plants, insects, and microbes.3,9 In addition to the articles in this 5102
DOI: 10.1021/acs.jafc.7b02741 J. Agric. Food Chem. 2017, 65, 5101−5103
Journal of Agricultural and Food Chemistry
Editorial
(7) Unsicker, S. B.; Kunert, G.; Gershenzon, J. Protective perfumes: The role of vegetative volatiles in plant defences against herbivores. Curr. Opin. Plant Biol. 2009, 12, 479−485. (8) Regnier, R. E. Semiochemicals − structure and function. Biol. Reprod. 1971, 4, 309−326. (9) Davis, T. S.; Crippen, T. L.; Hofstetter, R. W.; Tomberlin, J. K. Microbial volatile emissions as insect semiochemicals. J. Chem. Ecol. 2013, 39, 840−859. (10) Beck, J. J.; Higbee, B. S.; Light, D. M.; Gee, W. S.; Merrill, G. B.; Hayashi, J. M. Hull split and damaged almond volatiles attract male and female navel orangeworm moths. J. Agric. Food Chem. 2012, 60, 8090−8096. (11) Vacas, S.; Abad-Payá, M.; Primo, J.; Navarro-Llopis, V. Identification of pheromone synergists for Rhynchophorus ferrugineus trapping systems from Phoenix canariensis palm volatiles. J. Agric. Food Chem. 2014, 62, 6053−6064. (12) Suckling, D. M.; Twidle, A. M.; Gibb, A. R.; Manning, L. M.; Mitchell, V. J.; Sullivan, T. E. S.; Wee, S. L.; El-Sayed, A. M. Volatiles from apple trees infested with light brown apple moth larvae attract the parasitoid Dolichogenidia tasmanica. J. Agric. Food Chem. 2012, 60, 9562−9566. (13) Gu, H.-J.; Cheng, S.-S.; Lin, C.-Y.; Huang, C.-G.; Chen, W.-J.; Chang, S.-T. Repellency of essential oils of Cryptomeria japonica (Pinaceae) against adults of the mosquitos Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J. Agric. Food Chem. 2009, 57, 11127− 11133. (14) Beck, J. J.; Baig, N.; Cook, D.; Mahoney, N. E.; Marsico, T. D. Semiochemicals from ex situ abiotically stressed cactus tissue: A contributing role of fungal spores? J. Agric. Food Chem. 2014, 62, 12273−12276. (15) Seiber, J. N.; Coats, J.; Duke, S. O.; Gross, A. D. Biopesticides: State of the art and future opportunities. J. Agric. Food Chem. 2014, 62, 11613−11619. (16) Paini, D. R.; Sheppard, A. W.; Cook, D. C.; De Barro, P. J.; Worner, S. P.; Thomas, M. B. Global threat to agriculture from invasive species. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 7575−7579. (17) Karlsson, M. F.; Birgersson, G.; Cotes Prado, A. M.; Bosa, F.; Bengtsson, M.; Witzgall, P. Plant odor analysis of potato: Response of Guatemalan moth to above- and belowground potato volatiles. J. Agric. Food Chem. 2009, 57, 5903−5909. (18) Kachigamba, D. L.; Ekesi, S.; Ndung’U, M. W.; Gitonga, L. M.; Teal, P. E. A.; Torto, B. Evidence for potential of managing some African fruit fly species (Diptera: Tephritidae) using the mango fruit fly host-marking pheromone. J. Econ. Entomol. 2012, 105, 2068−2075. (19) Berenbaum, M. Does the honey bee “risk cup” runneth over? Estimating aggregate exposures for assessing pesticide risks to honey bees in agroecosystems. J. Agric. Food Chem. 2016, 64, 13−20. (20) Vannette, R. L.; Fukami, T. Nectar microbes can reduce secondary metabolites in nectar and alter effects on nectar consumption by pollinators. Ecology 2016, 97, 1410−1419. (21) Vannette, R. L.; Gauthier, M.-P. L.; Fukami, T. Nectar bacteria, but not yeast, weaken a plant pollinator mutualism. Proc. R. Soc. London, Ser. B 2013, 280, 20122601. (22) Helms, A. M.; De Moraes, C. M.; Mescher, M. C.; Tooker, J. F. The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding. BMC Plant Biol. 2014, 14, 173. (23) Anderson, J. A.; Gipmans, M.; Hurst, S.; Layton, R.; Nehra, N.; Pickett, J.; Shah, D. M.; Souza, T. L. P. O.; Tripathi, L. Emerging agricultural biotechnologies for sustainable agriculture and food security. J. Agric. Food Chem. 2016, 64, 383−393.
nectar-residing microbes on the nectar quality and output of volatiles as well as their influence on pollinators.20,21 One interesting and infrequently published form of chemical communication is that of insect−plant interactions. Researchers have recently demonstrated that goldenrod plants can prime their defenses as a result of sensing an insect-produced semiochemical.22 This strategy of plant priming could be exploited in agriculture to decrease production losses. A challenge for researchers is how to induce the plant to produce this response when needed versus a constitutive response. This Virtual Issue highlights recent work published in JAFC on the broad range of topics covered under the auspices of chemical communication and its applicability to agricultural issues. To overcome the ongoing challenges of agriculture in a sustainable and environmentally friendly manner, continued high-quality research is needed.23 JAFC is committed to publishing the high-impact results of these studies and looks forward to continued dissemination of important molecular aspects of an agricultural chemical ecology communication network.
John J. Beck*,† Baldwyn Torto‡ Rachel L. Vannette§ †
■
Chemistry Research Unit, Center for Medical, Agricultural and Veterinary Entomology, Agricultural Research Service (ARS), United States Department of Agriculture (USDA), 1700 Southwest 23rd Drive, Gainesville, Florida 32608, United States ‡ International Centre of Insect Physiology and Ecology (ICIPE), Post Office Box 30772-00100, Nairobi, Kenya § Department of Entomology and Nematology, University of California, Davis, 1 Shields Avenue, Davis, California 95616, United States
AUTHOR INFORMATION
Corresponding Author
*Telephone: 352-374-5730. Fax: 352-374-5707. E-mail: john.
[email protected]. ORCID
John J. Beck: 0000-0002-0696-5060 Notes
Views expressed in this editorial are those of the authors and not necessarily the views of the ACS.
■
REFERENCES
(1) Murphy, W. J.; Crowe, J. M.; Kenyon, R. L. The editors interview 18 leaders in science, agriculture, and food processing. J. Agric. Food Chem. 1953, 1, 28−41. (2) Feldmann, F.; Alford, D. V.; Furk, C. Crop Resistance to Biotic and Abiotic Factors; Deutsche Phytomedizinische Gesellschaft: Braunschweig, Germany, 2009. (3) Szendrei, Z.; Rodriguez-Saona, C. A meta-analysis of insect pest behavioral manipulation with plant volatiles. Entomol. Exp. Appl. 2010, 134, 201−210. (4) Junker, R. R.; Tholl, D. Volatile organic compound mediated interactions at the plant-microbe interface. J. Chem. Ecol. 2013, 39, 810−825. (5) Beck, J. J.; Vannette, R. V. Harnessing insect-microbe chemical communications to control insect pests of agricultural systems. J. Agric. Food Chem. 2017, 65, 23−28. (6) Loreto, J.; Dicke, M.; Schnitzler, J. P.; Turlings, T. C. J. Plant volatiles and the environment. Plant, Cell Environ. 2014, 37, 1905− 1908. 5103
DOI: 10.1021/acs.jafc.7b02741 J. Agric. Food Chem. 2017, 65, 5101−5103
