Interactions Among Plants, Insects, and Microbes: Elucidation of Inter

Review Cite This: J. Agric. Food Chem. 2018, 66, 6663−6674

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Interactions Among Plants, Insects, and Microbes: Elucidation of Inter-Organismal Chemical Communications in Agricultural Ecology John J. Beck,*,† Hans T. Alborn,† Anna K. Block,† Shawn A. Christensen,† Charles T. Hunter,† Caitlin C. Rering,† Irmgard Seidl-Adams,§ Charles J. Stuhl,† Baldwyn Torto,‡ and James H. Tumlinson§ †

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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 ‡ International Centre of Insect Physiology and Ecology (icipe), 30772-00100, Nairobi, Kenya § Center for Chemical Ecology, Penn State University, University Park, Pennsylvania 16802, United States ABSTRACT: The last 2 decades have witnessed a sustained increase in the study of plant-emitted volatiles and their role in plant−insect, plant−microbe, and plant−plant interactions. While each of these binary systems involves complex chemical and biochemical processes between two organisms, the progression of increasing complexity of a ternary system (i.e., plant−insect− microbe), and the study of a ternary system requires nontrivial planning. This planning can include an experimental design that factors in potential overarching ecological interactions regarding the binary or ternary system, correctly identifying and understanding unexpected observations that may occur during the experiment and thorough interpretation of the resultant data. This challenge of planning, performing, and interpreting a plant’s defensive response to multiple biotic stressors will be even greater when abiotic stressors (i.e., temperature or water) are factored into the system. To fully understand the system, we need to not only continue to investigate and understand the volatile profiles but also include and understand the biochemistry of the plant’s response to these stressors. In this review, we provide examples and discuss interaction considerations with respect to how readers and future authors of the Journal of Agricultural and Food Chemistry can contribute their expertise toward the extraction and interpretation of chemical information exchanged between agricultural commodities and their associated pests. This holistic, multidisciplinary, and thoughtful approach to interactions of plants, insects, and microbes, and the resultant response of the plants can lead to a better understanding of agricultural ecology, in turn leading to practical and viable solutions to agricultural problems. KEYWORDS: abiotic, biotic, chemical communication, semiochemicals, stressors, volatiles

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INTRODUCTION Agricultural practices have been an integral part of human history for about 10 000 years. The use of chemical compounds for control of insect pests was documented approximately 4 500 years ago with the use of sulfur-containing compounds for the control of insects and mites. About 2 000 years ago the utilization of plants as insecticides was documented with the use of dried flowers of Chrysanthemum cinerariaefolium used to protect stored grains.1,2 Since then, there has been an explosion of synthetic, plant-derived synthetic, and botanical pesticides for the control of insect and microbial pests.2,3 Additionally, modern biotechnology, biorational pesticides (biopesticides), and genetic modification of plants have been employed to help address food security, agricultural sustainability, and protection of crops against biotic and abiotic stressors.4−6 Examples such as these highlight not only the extraordinary historical context of natural products chemistry but also the significant contributions of plantderived compounds toward agriculture security. For many consumers and backyard gardeners, the chemical basis (which we know to be natural products in action) for protection of plants is a liquid or solid (i.e., a spray or granule application), yet an often unnoticed but highly important aspect of plant protection happens in the surrounding air and within the plant itself (Figure 1). The utilization of © 2018 American Chemical Society

Figure 1. Illustration of beneficial and pest insects and nematodes and the role of odors in both above- and belowground systems.

Received: Revised: Accepted: Published: 6663

April 5, 2018 June 10, 2018 June 12, 2018 June 12, 2018 DOI: 10.1021/acs.jafc.8b01763 J. Agric. Food Chem. 2018, 66, 6663−6674

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Journal of Agricultural and Food Chemistry

for genome editing and functional genomics for plants and abiotic stressors.17 Information obtained from current studies to increase the understanding of how volatile and nonvolatile defense chemicals are made, including identification of the genes involved in their biosynthesis, and knowledge of how they function against specific pests can be used to guide manipulation of their production using molecular breeding or engineering to produce crops with enhanced pest/disease resistance. Given the impact of abiotic stress on the interaction of organisms in an agricultural system, work is also underway to investigate its impact on the function and durability of these chemical defenses. A large aspect of this involves elucidating the role of plant hormones in coordinating these responses, as hormones are master regulators of responses to biotic and abiotic stress as well as development. This is important, as chemical defenses not only have to be produced, they have to be produced at the right time to be effective. It is our hope that more articles submitted to the Journal of Agricultural and Food Chemistry will take advantage of teams of interdisciplinary scientists to plan, implement, understand, and apply the learned knowledge from complex binary or ternary interorganismal systems. The more we understand each agricultural system as a whole, the more we can provide sustainable solutions for our stakeholders, or simply stated: understanding agricultural ecology: systems to solutions. Following are examples, thoughts, and discussion from colleagues and collaborators who have explored discrete portions of interorganismal investigations and applied this knowledge in interdisciplinary collaborative projects to better understand the role and influence of their particular portion of the system. We start the discussion with research involving pollinators, which includes the influences of the nectar microbiome on pollinator attraction (nectar−microbe−insect interactions), as well as the chemical-based interactions between a pollinator and its associated insect pests. We then move discussion to the plant’s perspective and its chemical response to biotic and abiotic stressors. This includes the binary systems insect−plant and microbe−plant, and the corresponding defensive response from the plant but then taken one step further to consider the effect of a third abiotic stressor. The plant’s hormonal responses to biotic stresses are then discussed. This section is introduced with a detailed look at one particular class of compounds, green leaf volatiles (GLVs), produced by the plant in response to varying stressors. We then switch gears and discuss the requisite collection and analysis of semiochemicals using the belowground system, plant−nematode interactions, as an example. Finally, we provide some examples of applying this knowledge of interorganismal interactions toward the management of agricultural pests by smallholder farmers in Africa.

semiochemicals (biotically produced chemical compounds used for communication between organisms) that can be either beneficial or harmful to the plant, by insects and microbes, has been recently discussed in a Perspective,7 as well as highlighted in a Virtual Issue8 in the Journal of Agricultural and Food Chemistry. The focus of this paper is to highlight the utility of interdisciplinary projects that holistically take into consideration the complex inter-organismal interactions (i.e., plant, insect, or microbe systems) in question. While there is much work that needs to be done in these systems from a semiochemical approach (study of emitted volatile profiles), the ability to also consider and understand the biochemistry of the plant’s response to multiple stressors, both biotic as well as abiotic, may provide more realistic and sustainable agricultural solutions.

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AGRICULTURAL ECOLOGY SYSTEMS “There are three principal means of acquiring knowledge...observation of nature, reflection, and experimentation” Denis Diderot For chemical ecologists, as with many disciplines, it is the observation of a system (e.g., an herbivore locating its host plant) that provides us with the initiative to investigate what chemicals may be at the heart of the communication of that system. The last 2 decades have witnessed a substantial and sustained increase in the study of plant-emitted volatiles and their role in plant−insect, plant−microbe, and plant−plant interactions,7,8 and there are elegant reports and reviews that discuss some of these individual binary systems in detail.9−14 While each of these systems involves complex chemical and biochemical processes between the two organisms, the progression of increasing complexity toward a ternary system (i.e., plant−insect−microbe) presents higher-order complexity for not only the experimental design but just as important the analysis of the resultant data. The challenge of investigating and interpreting a plant’s defensive response to multiple biotic stressors will be even greater when abiotic stressors (i.e., temperature or water) are factored in. Over the years, the intricacy of agricultural ecology research has increased, which may be in part due to implementation of more sophisticated and sensitive analytical instrumentation as well as methods of headspace volatile collection. For instance, some early reports on plant volatiles in the Journal of Agricultural and Food Chemistry simply listed the identified compounds in tables and compared the volatile profiles (often essential oil extracts) of various cultivars, plant parts, or varying phenological stages. However, in the last 2 decades the inquisitiveness of researchers toward plant responses to increased stressors starts to become more evident. For example, Errard et al.15 performed a nontargeted metabolomics study of the volatile and nonvolatile profiles from tomato plants infested with multiple insect pests (mites and aphids) and at different infestation times. The researchers were able to identify metabolites associated with different signaling pathways and elicited from the different insect pests. Research such as this will lead to a better understanding of the plant’s response to multiple herbivories, which is a daily challenge to many agricultural plants and eventually the ability to assist with the defense of the plants toward biotic and abiotic stressors. More recently, the protection of plants has progressed to involve the use of gene deletion mutants to elucidate the plant’s defensive response to various biotic or abiotic stressors.16 Additionally, CRISPR technology is being applied

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PLANTS AND BEES: INTERACTIONS OF POLLINATORS, FLOWERS, INSECTS, AND MICROBES “A bee is an exquisite chemist” Royal beekeeper to Charles II Floral Microbe Semiochemicals. Flowering plants are faced with an ongoing dilemma, floral visitation is necessary as it enhances reproduction for many plants, including many of the world’s most important crops;18 however, visitors also vector disease, which can negatively impact plant fitness and devastate crop yields. Plants have adapted to these pleiotropic pressures with a variety of strategies for maximizing reward 6664

DOI: 10.1021/acs.jafc.8b01763 J. Agric. Food Chem. 2018, 66, 6663−6674

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destructive pest that consumes honey bee eggs, brood, stored pollen, and honey, thus, making the hive material unsuitable for consumption by the honey bee or humans.32 A microbial pest of the honey bee is the fatal pathogen known as American foulbrood, a disease caused by the spore forming bacterium Paenibacillus larvae.33 Infected brood die at the prepupal or pupal stage,34 and severe infection within a hive weakens the colony, eventually leading to hive death. American foulbrood spores are very resistant to freezing and high temperatures and can remain viable for over 50 years. Because there are no known treatments for American foulbrood, the only current management practice is the destruction of infected colonies and hives by burning. Potential control measures for American foulbrood may eventually include the use of microbe−microbe interactions, such as the introduction of a beneficial microbe that inhibits American foulbrood growth via population control or by emission of volatile or nonvolatile compounds that inhibit growth. The challenge we then face is to efficiently protect, preserve, and even enhance the quality of life of the domesticated pollinator, which plays an essential and critical role in many agricultural systems. To address one aspect of this challenge, the research described for this binary, insect−insect (pollinator−pollinator pest) system entails the collection and interpretation of the chemical mechanisms that govern insect behavior, and the interactions of pest insects within the hive environment. Research within these laboratories has provided important knowledge of the behavior of honey bees infested with the varroa mite35 as well as host location of the varroa mite to its host within the hive. Other recent research has identified both pheromone and host-based semiochemicals of the small hive beetle. This information is being used to develop efficacious and cost-effective attractants and traps for the small hive beetle.36,37 The intention of the two programs described in this Plants and Bees: Interactions of Pollinators, Flowers, Insects, and Microbes section is to merge and modify the individually developed methods and gained knowledge into a project that investigates holistically the plant−insect, plant−microbe, and insect−microbe interactions and how to best develop a solution for both increased pollination as well as protection of the pollinators. The Western honey bee is an excellent model for studying behavioral changes due to infection of pests and microbes as well as pollination behaviors based on semiochemicals received, given that the honey bee can readily be experimentally influenced and handled.38,39 At the core of these discussed systems is the plant and its multitude of internal biochemical processes. The next section explores some defensive systems and how they are either communicated to the surrounding environment or applied to specific biotic or abiotic stressors.

while minimizing risk. Perhaps chief among these strategies is floral scent. Recently, pollination biology studies have incorporated the role of the floral microbiome in plant−insect interactions.19−21 Similar to floral volatiles,22 microbial-produced volatiles may act as important semiochemicals, relaying valuable information about floral resource presence and quality (nectar, pollen, oils). For example, volatiles produced by nectar specialist microorganisms can increase foraging efficiency for pollinators by acting as an honest signal for both the presence and quality of nectar rewards.23 Application of these specialists to agricultural flowers may increase pollinator visitations, thereby increasing yields. Alternatively, microbe semiochemicals may increase the attraction and apparency of flowers to pests and pollinators alike. Floral odors serve not only to attract beneficial species (pollinators, beneficial predators), they also serve in plant defense, by repelling antagonists (nectar robbers, florivores).24 Microbial-produced volatiles have also been hypothesized to filter floral visitation in a similar manner. Microbial presence may alter pollinator affinity for a given flower, either enhancing or decreasing affinity, depending on the species. Microbes introduce new compounds into floral blends25,26 and may metabolize other plant-derived components.27 By altering the floral volatile blend, and with it, the floral apparency or affinity of insect visitors, microorganisms may either suppress or promote successful plant reproduction. The floral microbiome is subject to conventional and biopesticide control measures: fungicides, antibiotics, and biocontrol products are applied to many flowering crops to prevent pathogen infection.28,29 An understanding of the tritrophic interactions between flowering plants, the anthospheric microbiome, and floral visitors (both beneficial and detrimental) may lead to new or improved agricultural technologies. For example, microorganisms capable of emitting certain key volatile components not synthesized by plants may be developed and rapidly deployed to a wide variety of crops, without the need for genetic modification of the plants themselves. Current and ongoing research within our laboratories is demonstrating complex microbe−microbe interactions within the nectar biome26 and that the resultant outcome of this interaction may have significant influence on the semiochemicals produced (i.e., nectar−insect interactions). This highlights the need to thoroughly consider how microbes will affect plant−insect interactions, in particular the pollinator−floral interaction. Thus, the species- and contextdependent nature of many plant−insect and plant−microbe interactions will require further study to ensure successful application of this flexible tool for semiochemical production. Areas closely related to this are the pollinator−insect and the pollinator−microbe interactions. These topics are described next. Pollinator−Insect Interactions. The Western honey bee is a European honey bee subspecies that was introduced into North America in the early 1600s and has been on the decline since 2006 due to Colony Collapse Disorder (CCD).30 There are several factors that threaten honey bee survival and include parasites, pathogens, poor nutrition, and exposure to pesticides. The major arthropod pests of honey bees are the varroa mite, Varroa destructor, and the small hive beetle Aethena tumida. The mite is an external parasite that transmits disease as it feeds on the hemolymph (blood) of adult bees, larvae, and pupae.31 Furthermore, the small hive beetle is a

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PLANT-PRODUCED COMPOUNDS FOR DEFENSE AND SIGNALING “If we understand how plants regulate their own defenses in nature, we will have a very powerful tool that can be used to manipulate the defenses of our crops...” Rick Karban Understanding the Multifaceted Roles of Green Leaf Volatiles (GLVs). Most plant−insect interactions are accompanied by plant volatiles, induced by either herbivory or associated microbe activity or both.40 When volatile such as terpenes are synthesized de novo in response to herbivore damage, as they are in maize, there is a delay of several hours 6665


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Journal of Agricultural and Food Chemistry between damage/induction and release.41,42 Conversely, GLVs are formed rapidly by many plant species after the disruption of their leaf tissues.43 GLVs (Figure 2) are thought to enable

possible that gut bacteria play a direct role in suppressing and/or modifying the GLVs (plant−insect−microbe interaction). However, the physiological and ecological significance of these interactions is not clear. We need to understand the mechanisms by which GLVs are suppressed/modified by herbivores and/or associated microbes and conversely how this affects the insect−plant biome. As Farmer52 stated, “Well adapted attackers must therefore minimize the display of elicitors and also avoid injuring their host since both types of input will surely lead to better detection and stronger defense.” What is not explicitly stated in this quote is that an herbivore may not only minimize its display of elicitors but also may actively suppress the induced defense of its host. Further, the associated microbes may participate in and/or benefit from suppression of plant defenses. We predict that there is strong selection pressure on herbivores and microbes to modify or suppress defensive signals as well as defensive antimicrobial plant compounds. Successful elucidation of the mechanisms and factors involved in this complex multitrophic system will demand a holistic collaborative approach by a multidisciplinary team. Identification and characterization of active components of insect herbivore saliva/regurgitant that suppress or modify GLVs will require bioassay guided purification and identification of small effector molecules and/or enzymes by chromatographic, spectroscopic, and other methods. To fully understand the system, one must determine source (insect digestive compartment or bacteria) of suppressing factors or modifiers. In order to explore the role and importance of plant and insect endogenous microbes and their effect on the “plant−insect” interaction we need to get a better sense of the microbial players involved. Since caterpillars acquire most of their microbes through their food source,53 a metagenomics and metatranscriptomics approach which excludes contaminating chloroplast sequences54 should identify most of the plant’s and insect’s endogenous microbiome and their respective transcriptional activities. A metagenomics and transcriptomics analysis after insect feeding and hence exposure to induced plant volatiles will reveal possible compositional changes in the respective residing microbiomes and their activities and thus allow identification of major players. Identification of microbes that modify either the defensive state of plants or their volatile profile after insect attack is a first step on a trajectory to modifying seeds or seedlings sustainably circumventing the application of pesticides. Elucidation of the mechanism(s) by which the active compounds suppress or modify GLVs can be accomplished using genetically modified plants, deficient in enzymes catalyzing terminal steps in GLV biosynthesis: assaying leaves from genetically modified and wild type plants with purified effectors and synthetic intermediates will identify the biosynthetic step modified by the respective effector. Truly satisfactory and lasting solutions to pest problems will require a shift to understanding and promoting naturally occurring biological agents, like microbes in plants and herbivore insects, insect parasitoids and predators, and other inherent strengths as vital components of total agricultural ecosystems to keep pests within acceptable bounds. An increased knowledge of the basic factors governing these inherent strengths within agricultural ecosystems is crucial to harnessing their potential benefits. It is likely that a more thorough understanding of the behavioral and chemical ecology of pest and beneficial insects and the associated

Figure 2. Volatile compounds, (Z)-3-hexenal, 1; (E)-2-hexenal, 2; (Z)-3-hexenyl acetate, 3; (E)-2-hexenyl acetate, 4; and (E)-βcaryophyllene, 5, involved in plant communications.

self-recognition of damage, inform the host plant of tissue disruption, initiate processes aimed at restoring homeostasis after wounding, and prepare adjacent tissues for the defense against invaders.44 In addition, the physiological significance of the rapid formation of (Z)-3-hexenal (1) has been implicated in defense against biotic stresses.43,45 GLVs likely provide rapid but nonspecific information about the exact location of herbivore damage and have been reported to play a role in host-location by predators and parasitic wasps (i.e., plant− insect−insect interactions).46 Although changes in constitutive GLV ratios can alter the ability of herbivores to locate their host, the degree to which natural enemies use induced GLVs to find plants with prey remains unclear.43 It has also been reported that GLVs negatively affect herbivore performance47 and have antibiotic activity against several microorganisms.48 Since plants and insects harbor endogenous populations of microbes these findings suggest that GLVs have the potential to control plant pathogens directly, and pest insects directly, or indirectly by affecting their microbiome. Savchenko et al.49 reported that emission of GLVs by Arabidopsis is stimulated by wounding incurred mechanically or by aphids but impaired by both generalist and specialist chewing insects. Simultaneously, however, these chewing herbivores stimulated jasmonic acid production, suggesting targeted insect suppression of the 13-hydroperoxide lyase branch of the oxylipin pathway. In an excellent meta-analysis of GLV production by plants, Ameye et al.50 reported that chewing herbivores actually suppress or modify GLV emissions. Allman and Baldwin46 showed that the oral secretion of Manduca sexta contains a heat labile constituent that isomerizes (Z)-3-hexenal, 1, to (E)-2-hexenal, 2, thus altering the proportions of GLV constituents produced by mechanically damaged Nicotiana attenuata. This isomerization appears to be detrimental to the herbivore as the altered GLV blend is more attractive to a predator than the blend released after mechanical damage alone. Also, M. sexta moths can detect 3Z:2E ratios and preferentially oviposited on Datura wrightii plants with higher 3Z:2E ratio of hexenyl acetate, 3 and 4.51 The paradox is that herbivorous caterpillars produce elicitors in their oral secretions/regurgitant that plants respond to by increasing the release of volatiles such as terpenes and indole, while other component(s) of their oral secretion/regurgitant suppress or modify production of (Z)-3-hexenal, 1. The suppression of GLV emissions by caterpillars suggests that GLVs are directly or indirectly detrimental to caterpillar growth and development. GLVs could act indirectly via triggering/inducing plant defenses against the caterpillar or their gut microbiome. From this perspective, it appears 6666


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significantly increasing kauralexin accumulation.64 Elevated CO2 also led to decreased emission of herbivore induced volatiles in maize. 65 Many such changes have been documented66 and they are often species, compound, and even tissue specific responses. Strategies to effectively enhance defense chemistry will therefore also require input from plant physiologists, climate scientists, and chemical ecologists to produce optimal and persistent results. Similar to the maize− insect battle is the biotic maize−microbe interaction and how changes in the surrounding environment can influence this interface as well as each of the players. Maize−Microbe Interactions Under Abiotic Stress. Despite recent advances in molecular breeding, biotechnology, and improved fungicides or pesticides, an average of $5 billion is lost in corn production per year due to diseases caused by microbial pathogens.67 In addition to biotic stress, abiotic stress in the form of heat and drought can contribute to yield losses of up to 39%.68 As the majority of maize production relies on natural precipitation and as disease management strategies struggle to pacify current environmental and human health concerns associated with chemical pesticide use, there is a great interest in the discovery and enhancement of innate immunity to promote resistance against biotic and abiotic stress. Recent discoveries in maize defense chemistry have identified novel resistance mechanisms, elucidating both key components of pathogen-inducible signaling pathways and their respective downstream antimicrobial products. For example, studies exploiting mutations in key maize lipoxygenase (Lox3) and oxo-phytodienoate reductase (Opr7/ Opr8) genes genetically demonstrated the significance of 9oxylipins and jasmonic acid in conferring resistance to pathogen attack.69,70 Connected to these findings was the identification of pathogen-inducible diterpenoid (kauralexins) and sesquiterpenoid (zealexins) defense molecules that are produced in response to jasmonic acid and other hormone signals.71,72 In vitro characterization of kauralexins and zealexins demonstrated strong antimicrobial activity for different phytoalexins against the agro-economically important pathogens Aspergillus f lavus, Fusarium verticillioides, Cochliobolus heterostrophus, Fusarium graminearum, and Colletotrichum graminicola.71−74 Analysis of disease resistance using mutants in the kauralexin biosynthesis gene ent-copalyl diphosphate synthase known as Anther Ear 2 (An2) genetically affirmed the importance of terpenoid phytoalexins in preventing disease progression. Despite the significance of these newly characterized biochemical defenses, recent studies investigating the effects of abiotic stress on maize defense revealed that these inducible responses can be compromised under diverse environmental conditions. Vaughan et al.75 demonstrated that maize exposed to elevated CO2 (eCO2) was more susceptible to F. verticillioides stalk rot, a phenotype that positively correlated with the reduced levels of lipoxygenase transcripts, jasmonic acid, and terpenoid phytoalexins. Accumulation of a newly identified zealexin (ZA4) was also recently shown to be significantly reduced in response to A. f lavus infection and Ostrinia nubilalis herbivory under eCO2 conditions, suggesting that eCO2 has a broad negative effect on maize defense.74 In contrast to the suppression of plant defense by eCO2, drought stress elicited an increased production of jasmonic acid, abscisic acid, zealexins, and kauralexins in maize roots. Moreover, kauralexins appear to play a role in drought

microbiomes will provide the key to successful development of ecologically sound systems for monitoring and control of insect pests in agriculture. Crop Defense: Insects, Chemistry, and Environmental Change. Herbivorous pests are a major problem for agriculture with damage from folivory, sap feeding, and root herbivory estimated to result in a loss of greater than 20% of net primary productivity across biomes.55 The use of chemical insecticides is currently effective for the control of many agricultural pests; however, health and environmental concerns coupled with the high likelihood of insecticide resistance development in many pests means that alternate strategies are urgently needed. The most successful recent technology for insect resistance has been the engineering of Bt toxins in crop plants to provide protection against caterpillars.56 This strategy has led to dramatic reductions in insecticide use; however, Bt resistance is beginning to develop in some species.57 Insect related damage in crops can potentially be reduced by increasing the crops endogenous insect resistance traits through breeding. These insect resistance traits include deterring pest landing, preventing attachment and feeding, reducing plant palatability, and attracting predators or parasites.58 Several of these traits involve plant defense chemicals such as volatiles, waxes, and toxins, which in general have been reduced during crop domestication.59 For instance, the gene Terpene Synthase 23 that catalyzes the production of (E)-β-caryophyllene, 5 (Figure 2), is abundant in maize ancestors and European maize varieties but is not highly expressed in North American maize varieties. (E)-β-caryophyllene, 5, is a component of maize volatile emissions important for recruiting entomopathogenic nematodes (e.g., genera of Heterorhabditis and Steinernema, obligate parasites of insects) and parasitic wasps to infested plants.60 In order to effectively breed for enhanced chemical defenses, clear knowledge of both the bioactivity and biosynthesis of the chemicals of interest is needed. For instance, benzoxazinoids are anti-insect hydroxamic acids found in a variety of grasses and other plant species. They are made from indole using a series of enzymes, denoted as BX1 through BX14 in maize.61 Benzoxazinoids are stored in plant vacuoles as glucosides and when plant cells are damaged by insect feeding, vacuoles are disrupted and glucosidases convert the glucosides to active aglycones that are toxic to the attacking pest. Such detailed information about the production and function of chemical defense compounds is the exception rather than the norm and elucidation and application of this information involves multidisciplinary expertise including chemists, biochemists, geneticists, plant molecular biologists, entomologists, and molecular breeders. A major aspect of uncertainty in using enhanced defense chemistry-based resistance is how persistent it will be in the face of environmental change, particularly considering predicted accelerated insect development and generation number with elevated temperatures.62 Changes in environmental conditions can impact the production and effectiveness of defensive chemicals. For instance, wheat (Triticum aestivum) plants infested with bird cherry-oat aphid (Rhopalosiphum padi) had higher induction of hydroxamic acids when grown at lower temperatures.63 Maize plants grown at elevated CO2 levels had reduced accumulation of the phytoalexins, kauralexins in roots after Diabrotica balteata (rootworm) larval feeding compared to those grown at ambient CO2.64 Drought stress, however, negated the effect of elevated CO2 by 6667


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Journal of Agricultural and Food Chemistry resistance, as an2 mutants displayed an increased susceptibility to drought stress in young maize seedlings.76 Interestingly, drought stress appears to predominate over the effects of eCO2, as eCO2 + drought also promoted heightened terpenoid antimicrobial production, demonstrating the intricate nature of maize−microbe interactions under variable environmental conditions.64 To overcome enormous pest-driven economic losses in corn production and the broad concerns associated with the use of toxic pesticides and fungicides, current maize protection research is focusing on the enhancement of innate immunity. While new discoveries have significantly improved our knowledge of maize defense responses to biotic threats, recent studies have demonstrated the variable impacts of abiotic stressors (e.g., elevated CO2 and drought) on defensive systems, thus demonstrating the complexity of molecular plant−biotic interactions in nature. The future investigation of these combinatorial systems in maize will both elucidate the effects of multiple simultaneous stressors on plants and contribute to a larger multifaceted effort to alleviate current agro-socio-economic challenges in crop production. These efforts will require more advanced climate control facilities that provide accurate natural experimental conditions and more complete genomic resources for better manipulation of innate crop defense systems. The next section further discusses the plant’s response and begins to explore the biochemical regulation of, and potential manipulation to, the plant. Plant Hormones as Control Points for Modulating Stress Responses. As sessile organisms, plants must adapt to the environmental conditions they find themselves in. They have therefore evolved finely tuned, tightly regulated systems for adjusting their physiology and metabolism in response to external stimuli. The modulation of plant defense responses, including production of antimicrobial chemicals or volatiles (as described above), requires precise control of gene expression networks, enzyme activities, and metabolic flux. Plant hormones serve to regulate these processes and are thus control points that might be manipulated for improved or altered plant responses to stresses. While we have extensive knowledge surrounding the roles of specific plant hormones and their involvement in particular responses, we still lack the detailed understanding of how plant hormones interact to govern plant defenses that is needed before we can predict with certainty the outcome of altering hormone pathways. Plant hormones do not act in isolated systems but instead form a mind-numbingly complex network of synergistic and antagonistic signals that modulate responses to external and internal stimuli. Defense-related hormones jasmonic acid, 6, and salicylic acid, 7 (Figure 3), offer the clearest example of an antagonistic relationship, with jasmonic acid, 6, and salicylic acid, 7, governing defense responses to different classes of pests. The jasmonic acid, 6, signaling pathway promotes accumulation of many defense chemicals, including phytoalexins71,72 and defense-related volatiles, and is associated with defense against chewing insects and necrotrophic pathogens. Conversely, salicylic acid is primarily responsive to phloem-feeding insects as well as biotrophic and hemibiotrophic pathogens, where it activates pathogenesis-related proteins and system acquired resistance. Activation of jasmonic acid, 6, represses the salicylic acid, 7, pathway and vice-versa. In contrast, the ethylene and jasmonic acid, 6, pathways are heavily synergistic, and partially codependent, both promoting resistance to necrotrophic

Figure 3. Plant defense-related hormones, jasmonic acid, 6; salicylic acid, 7; and abscisic acid, 8.

pathogens and insects. However, ethylene also works to promote the salicylic acid-dependent repression of jasmonic acid, 6,77 highlighting the complexity of these systems. Abscisic acid, 8 (Figure 3), well-known for its role in abiotic stress responses, appears to be a negative regulator of defense against most biotrophic and necrotrophic pathogens, though its relationship to other defense-related hormones remains unclear and seems to be associated with enhanced resistance or susceptibility, depending on the particular plant−microbe or plant−insect interaction. One way abscisic acid, 8, signaling may lead to enhanced resistance against bacterial and fungal pathogens is in promoting stomatal closure, an effect that requires salicylic acid signaling.78 Abscisic acid, 8, is required for jasmonic acid, 6, biosynthesis and expression of jasmonic acid, 6, responsive genes,79 so its signaling activity is clearly linked with other phytohormone pathways. Additionally, abscisic acid, 8, appears to regulate the production of some chemical defense metabolites, including benzoxazinoids and defensive fatty acids.80 It is also induced by exposure to defense-related volatiles, including indole,81 implicating it in defense priming. The interactions, dependencies, and coregulation of jasmonic acid, 6, ethylene, salicylic acid, and abscisic acid form the central regulatory framework for plant defense responses and are the primary dials, which we may turn to modulate those responses. The remaining plant hormones, including brassinosteroids, gibberellic acid, cytokinin, and auxin are plant growth regulators with only poorly understood roles in plant defense, though the impacts of these hormones are certainly important to consider. The brassinosteroids signaling pathway is associated with pathogen-associated molecular pattern triggered immunity, and brassinosteroids activity has been implicated in promoting resistance to viral, bacterial, and fungal pathogens, though it was found to negatively regulate resistance to necrotrophic pathogens in some grasses.82,83 Roles for gibberellic acid in modulating plant defense responses are evident by its promotion of salicylic acid signaling by degrading DELLA proteins and resistance to biotrophs, though gibberellic acid appears to play a negative role in basal disease resistance.84 For cytokinin, almost nothing is known about its roles in plant defense, though a few clues as to its potential importance have surfaced. For one, tumorforming plant pathogens such as Agrobacterium tumefaciens have been shown to modify cytokinin biosynthesis to promote tumorigenesis.85 Also, cytokinin degradation appears to be accelerated by breakdown products of benzoxazinoid defense chemicals.86 Finally, increased resistance to the phytomyxea, Plasmodiophora brassicae, was observed after overexpressing cytokinin oxidase/dehydrogenase genes in Arabidopsis.87 Lastly, the growth-promoting hormone auxin also appears to 6668


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uprooted and replanted in sand, allowed to recover, and volatiles then collected on an adsorption filter by pulling air through the sand. We used this later technique to successfully detect, isolate, and identify insect damage induced citrus volatiles that attracted entomopathogenic nematodes,94 and the same technique was also successfully used to collect pepper root volatiles attracting plant parasitic nematodes (e.g., Meloidogyne spp.).95 Since uprooting is exceptionally stressful for the plant and might eliminate vital root−microorganism interactions, Deasy et al.96 planted broccoli seedlings in pots equipped with perforated PTFE tubing. Herbivory induced root volatiles produced by fully grown plants could then be statically collected on SPME fibers positioned within the tubing. SPME, as well as solvent extracted filter techniques rely on long sampling times, and therefore will affect any attempts of repeated sampling to monitor ongoing processes and interactions and in addition, the dynamics of the release of volatiles might be missed.94 Danner et al.97 addressed this dilemma by real-time continuous monitoring of insect attacked Brassica root volatiles with soft ionization proton-transfer reaction-mass spectrometry (PTR-MS). However, chromatography free MS techniques can only be used to monitor known compounds having distinctly different m/z ratios, practically eliminating monitoring of changes in blend compositions of common plant volatiles such as mono and sesquiterpenes. In addition, this strictly laboratory based technique is limited to one continuous analysis at a time. An alternative to continuous sampling is to use root probes as shown for field94 and laboratory sampling.98 With such a system, numerous plants can be sampled without the need for expensive equipment or elaborative preparations. When combined with solvent-free thermal desorption sample injection, small air volumes in the range of 10 mL/sampling (less than 5% of the estimated air in a 1 L soil-filled flower pot) can be collected in minutes, or even seconds, and analyzed by GC-MS. Since thermal desorption is known to often degrade sensitive samples,99,100 we developed a new, low cost, thermal desorption system with degradation and chromatographic results qualitatively comparable to on-column injections but with additional sample components normally hidden by the solvent peak.98 Despite the sensitivity and flexibility with solventless techniques such as SPME and Tenax/thermal desorption, one major drawback is that these samples cannot be used for bioassays. Thus, techniques such as Super Q collections followed by solvent extraction and/or destructive plant solvent extractions must be used when any form of bioassays are required. The sand-filled 6-arm olfactometer, developed by Rasmann et al.92 has been a major tool for soil interaction bioassays, making it possible to elucidate nematode, insect, and intact plant (seedlings) interactions. This technique has led to the discoveries of root volatiles role in attraction of entomopathogenic nematodes interactions to root worm infested maize as well as citrus. In addition, the much simpler dual choice sand column olfactometer allowed for efficient testing of extracts and synthetic blends for isolation and identification of actual nematode attractants and repellents. 95 Both types of olfactometers, as well as a simple sand-filled Petri dish arena, were successfully used to further study the behavior of entomopathogenic nematodes, leading to the discovery of these nematodes ability to learn to respond to various chemical

influence defense responses in plants, where it generally functions antagonistically to salicylic acid and synergistically with jasmonic acid. As with abscisic acid, the relationship between auxin signaling and disease resistance seems dependent on the specific plant−pathogen or plant−insect interaction. Other interesting points for consideration when contemplating manipulations of plant hormone pathways are the impacts such manipulations may have on critical plant microbiomes. Microbes residing in the phyllosphere, rhizosphere, or endosphere can serve to protect plants through interfering with pathogenic fungi or bacteria and by production of antibiotics. They also contribute directly to defense-related chemistry, including hormone metabolism, by providing secondary metabolites and even biosynthetic or catabolic enzymes. The potential to modify plant microbiomes to improve resiliency and defense is an area of expanding interest.88 A far greater understanding of the interactions and dependencies between plant hormones and microbiomes is needed before we can feel confident in manipulating either to improve plant performance in the face of biotic or abiotic threats. In this next section, we continue with a different type of plant−insect interaction, the belowground relationship of the plant’s roots and a species of nematode. However, while exploring this interaction, we also discuss a new volatile collection technique used to help discern the chemical communication between the two.

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COLLECTION OF BELOWGROUND VOLATILES AND ROOT−NEMATODE INTERACTIONS As described above, it is well established that various organisms use volatiles for communication, host location, and defense; thus, these types of signals can be utilized for control of pest organisms. For aboveground volatile collections, techniques such as encasement in glass chambers in combination with dynamical collection on porous material such as Super Q and HayeSep Q or static adsorption on a solid phase microextraction fiber (SPME) are well established and routinely used in our laboratory.65,89,90 We now know that volatiles released by roots or root associated microorganisms play a major role in root−insect− nematode interactions. We also know that hormone signaling is used to regulate these signals and that they are similar but not identical to aboveground signals. Finally, we are aware that we can use molecular and genetic techniques also to manipulate belowground defensive signaling. However, research on belowground volatile signaling lags because of the complexity of the systems. For example, we do not fully understand how volatiles disperse into the surrounding air space and how this dispersal is affected by the chemical characteristic of the molecules;91 and thus, how they interact with beneficial or pest organisms. For example, even if volatiles are released slowly or in a short burst, some might adhere to, or degrade on, soil particles and will remain in the proximity of the roots for an extended time. Other compounds might quickly diffuse. This, in combination with the environmentally influenced varying complexity of the soil itself creates challenges for sampling, monitoring, and ultimately understanding root zone (rhizosphere) semiochemicals. To simplify the system, root volatiles are often sampled by uprooting and crushing the roots followed by SPME or Super Q volatile collections,92,93 a technique with limited relevance for what the roots might release into soil. Alternatively, the plant is 6669


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Physiology (icipe) and partners have developed a sustainable and cost-effective cereal-legume intercropping agricultural production system, which significantly reduces pest damage, while increasing cereal yield in smallholder farming systems in East Africa.106,107 This cropping system, commonly referred to as “push−pull” technology exploits behavior-modifying phytochemicals from a repellent (push) intercrop Desmodium uncinatum (Leguminosae) and an attractive (pull) trap plant, Napier grass Pennisetum purpureum (Poaceae) bordering the maize plants to suppress stem borer populations including the recent notorious invasive pest, fall armyworm Spodoptera f rugiperda in Africa,108 while increasing natural enemy populations in maize fields. An adaptation of the “push− pull” technology for smallholder farmers growing cereal crops in drier areas in Africa to control both stem borers and Striga has also been developed and referred to as “climate-adapted push−pull” technology. This climate-adapted push−pull technology utilizes Desmoduim intortum (Leguminosae) as the repellent (push) crop and Brachiaria cultivar “Mulato II” (Poaceae) as the attractant (pull) crop. These recent advances in developing practical solutions to overcome biotic stressors suggest that knowledge of the binary systems plant−insect and plant−plant chemical interactions is necessary to increase food production in smallholder farming systems. However, given the complexity of these intercropping systems, utilizing various plants which interact with each other may create ecosystems that can either boost existing microbe populations and/or introduce new microorganisms to potentially benefit the farming systems. The surrounding landscape effects on these interactions may also contribute to the microbiome of the farming system. The alteration in the ecosystem can occur both aboveground and the rhizosphere to provide complex binary interactions such as microbe−plant, microbe−insect, microbe−microbe, and ternary microbe− insect−plant interactions. Also, the fact that secondary metabolites have been found to drive the interactions leading to reduced pest incidence and increased natural enemy populations in these farming systems suggest that investigating these additional interactions involving microbes may lead to discovery of potential useful phytochemical products that could be exploited for improved agricultural productivity in smallholder farming systems.

cues as well as the discovery of nematode group behavior,101,102 discoveries that will lead to new ways to utilize entomopathogenic nematodes to control root pests. With these belowground collection and sand-filled assay techniques, we are now ready to study biosynthesis and regulation of constitutive as well as herbivore induced root volatiles, how the volatile might be affected by biotic and abiotic factors, and how this might affect the herbivore as well as beneficial organisms like entomopathogenic nematodes. The above sections have discussed and provided examples of discrete interorganismal chemical communications. This last section pulls back a little to discuss these inter-organismal interactions but in a more macroscopic setting, smallholder farmers in Africa and how they use existing natural systems to provide defense for their agricultural commodities.

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PRACTICAL SOLUTIONS FOR REAL WORLD ISSUES OF SMALLHOLDER FARMERS An important goal for many scientists is how to develop simple and ef fective technologies to suppress mainly biotic stressors, while increasing crop yield. The practical application of this question is very important in smallholder cereal farming systems in sub-Saharan Africa. How do scientists elucidate the underlying science behind the binary plant−insect and plant− plant chemical interactions that contribute to the development of these simple and effective technologies? It is important to note that in sub-Saharan Africa, smallholder farming systems contribute about 80% of food production,103 a sector considered the least productive in the world, with a productivity rate of only 36%.104 The low productivity is due to complex abiotic (e.g., soil quality, drought) and biotic (e.g., above- and belowground pests, weeds, and diseases) stressors. Several approaches have been used in attempts to mitigate biotic and abiotic stressors in smallholder farming systems but unfortunately have met with variable results. These include modern agricultural approaches such as biotechnology and genetic modification that lead to the development of pest tolerant cultivars to mitigate against abiotic and biotic stressors as well as use of external agents including fertilizers to improve soil salinity and synthetic pesticide efficacy. Generally, these modern agricultural approaches are not only expensive for the majority of smallholder African farmers, but methods such as use of synthetic pesticides are also ill-suited for environmental, human, and animal health. Despite their often-smaller footprint of overall acreage, practical solutions for the smallholder farmer in Africa still require the application of science and technology.105 One example of a technology that is simple and effective for pest control, and easily adopted by smallholder farmers, is a strategy based on integrated pest management (IPM), which incorporates indigenous knowledge. In Africa, cereals such as maize, sorghum, and millet are the most important agricultural commodities grown by most smallholder farmers. Traditionally, smallholder famers grow these cereals for subsistence, and they are intercropped with various vegetables, such as legumes, which provide nitrogen fixing to the soil but also serve as protein and essential micronutrient sources for farmers’ families. Until recently, management of the key biotic stressors such as stem borers and the parasitic weed Striga in these cereal farming systems have been a major bottleneck for smallholder farmers. With a basic understanding and knowledge of the binary systems plant−insect and plant−plant chemical interaction, the International Centre of Insect

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AGRICULTURAL ECOLOGY: SYSTEMS TO SOLUTIONS When thinking about the intricate interactions in nature we tend to reduce them to binary systems in the laboratories, yet adding more and more players in different temporal sequences has been shown to significantly change the outcome of the interactions.109 Still, in most studies the roles of microbes are either symbionts or pathogens. Rarely do we consider plants and insects as microcosms containing their associated microbiomes. Yet these associated microbes most likely play an important role in the interactions between plants and their pathogens and plants and their herbivores. If we do not investigate these larger systems, we should at least keep that fact in mind when we interpret our data. Our aim has been to highlight the intricacies of agricultural ecology, and the numerous interactions involved among and between plants, insects, and microbes. Sometimes, what appears to be thorough binary or even a ternary project is typically a good project that may not yet fully consider all ecological aspects, microconsequences, or possibilities. Here, 6670


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(10) 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. (11) 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. (12) Junker, R. R.; Tholl, D. Volatile organic compound mediated interactions at the plant-microbe interface. J. Chem. Ecol. 2013, 39, 810−825. (13) Loreto, J.; Dicke, M.; Schnitzler, J. P.; Turlings, T. C. J. Plant volatiles and the environment. Plant, Cell Environ. 2014, 37, 1905− 1908. (14) Voelckel, C.; Jander, G.; Reinecke, A.; Hilker, M. Plant semiochemicals − perception and behavioural responses by insects. In Annual Plant Reviews; Voelckel, C., Jander, G., Eds.; John Wiley & Sons, Ltd: Chichester, U.K., 2014. (15) Errard, A.; Ulrichs, C.; Kuhne, S.; Mewis, I.; Mishig, N.; Maul, R.; Drungowski, M.; Parolin, P.; Schreiner, M.; Baldermann, S. Metabolite profiling reveals a specific response in tomato to predaceous Chrysoperla carnea larvae and herbivore(s)-predator interactions with the generalist pests Ietranchus urticae and Myzus persicae. Front. Plant Sci. 2016, 7, 1256. (16) Gayen, S.; Samanta, M. K.; Hossain, M. A.; Mandal, C. C.; Sen, S. K. A deletion mutant ndv200 of the Bacillus thuringiensis vip3BR insecticidal toxin gene is a prospective candidate for the next generation of genetically modified crop plants resistant to lepidopteran inset damage. Planta 2015, 242, 269−281. (17) Jain, M. Function genomics of abiotic stress tolerance in plants: a CRISPR approach. Front. Plant Sci. 2015, 6, 375. (18) Bailes, E. J.; Ollerton, J.; Pattrick, J. G.; Glover, B. J. How can an understanding of plant-pollinator interactions contribute to global food security? Curr. Opin. Plant Biol. 2015, 26, 72−79. (19) Schaeffer, R. N.; Phillips, C. R.; Duryea, M. C.; Andicoechea, J.; Irwin, R. E. Nectar yeasts in the tall larkspur Delphinium barbeyi (Ranunculaceae) and effects on components of pollinator foraging behavior. PLoS One 2014, 9, e108214. (20) Good, A. P.; Gauthier, M. P. L.; Vannette, R. L.; Fukami, T. Honey bees avoid nectar colonized by three bacterial species, but not by a yeast species, isolated from the bee gut. PLoS One 2014, 9, e86494. (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, e86494. (22) Knauer, A. C.; Schiestl, F. P. Bees use honest floral signals as indicators of reward when visiting flowers. Ecol. Lett. 2015, 18, 135− 143. (23) Raguso, R. A. Why are some floral nectars scented? Ecology 2004, 85, 1486−1494. (24) Junker, R. R.; Blüthgen, N. Floral scents repel facultative flower visitors, but attract obligate ones. Ann. Bot. 2010, 105, 777−782. (25) Golonka, A. M.; Johnson, B. O.; Freeman, J.; Hinson, D. W. Impact of nectarivorous yeasts on Silene caroliniana’s scent. East. Biol. 2014, 3, 1−26. (26) Rering, C. C.; Beck, J. J.; Hall, G. W.; McCartney, M. M.; Vannette, R. L. Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytol. 2018, DOI: 10.1111/nph.14809. (27) 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. (28) Klein, M. N.; da Silva, A. C.; Kupper, K. C. Bacillus subtilis based-formulation for the control of postbloom fruit drop of citrus. World J. Microbiol. Biotechnol. 2016, 32, 1−11. (29) Karise, R.; Dreyersdorff, G.; Jahani, M.; Veromann, E.; RunnoPaurson, E.; Kaart, T.; Smagghe, G.; Mand, M. Reliability of the entomovector technology using Prestop-Mix and Bombus terrestris L. as a fungal disease biocontrol method in open field. Sci. Rep. 2016, 6, 31650.

we touched upon only limited aspects of the monumental complexity of agricultural ecology, with each section seemingly an entity unto itself. We hope to stimulate hallway conversations, exchange of ideas, and formal collaborations not just between scientists within one department but rather scientists with expertise in many different areas. We have been fortunate to work within a group of scientists that includes chemists, chemical ecologists, environmental chemists, entomologists, plant physiologists, molecular biologists, and geneticists. This broad range of expertise has allowed us to consider simple systems (i.e., a kairomone that attracts an herbivore to its host plant) to more complex systems (i.e., a pathogen infecting a host plant that is undergoing abiotic stress). More importantly, our close proximity allows for the informal communication of results that lead to subsequent projects of increasing complexity. Overall, this multidisciplinary and thoughtful approach to interactions of plants, insects, and microbes, and the resultant response of the plants, leads to a better understanding of agricultural ecology, which in turn leads to practical and viable solutions to agricultural problems.

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AUTHOR INFORMATION

Corresponding Author

*Phone: 352-374-5730. Fax: 352-374-5707. E-mail: john. [email protected]. ORCID

John J. Beck: 0000-0002-0696-5060 Baldwyn Torto: 0000-0002-5080-9903 Funding

This work was performed under USDA-ARS Project Numbers 6036-22000-028, 6036-21000-011, and 6036-11210-001-00D. Notes

The authors declare no competing financial interest.

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REFERENCES

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