Ian Kaplan

Biosynthesis, function and metabolic engineering of plant volatile organic compounds

Plants synthesize an amazing diversity of volatile organic compounds (VOCs) that facilitate interactions with their environment, from attracting pollinators and seed dispersers to protecting themselves from pathogens, parasites and herbivores. Recent progress in -omics technologies resulted in the isolation of genes encoding enzymes responsible for the biosynthesis of many volatiles and contributed to our understanding of regulatory mechanisms involved in VOC formation. In this review, we largely focus on the biosynthesis and regulation of plant volatiles, the involvement of floral volatiles in plant reproduction as well as their contribution to plant biodiversity and applications in agriculture via crop-pollinator interactions. In addition, metabolic engineering approaches for both the improvement of plant defense and pollinator attraction are discussed in light of methodological constraints and ecological complications that limit the transition of crops with modified volatile profiles from research laboratories to real-world implementation.

CONSTITUTIVE AND INDUCED DEFENSES TO HERBIVORY IN ABOVE- AND BELOWGROUND PLANT TISSUES

A recent surge in attention devoted to the ecology of soil biota has prompted interest in quantifying similarities and differences between interactions occurring in above- and belowground communities. Furthermore, linkages that interconnect the dynamics of these two spatially distinct ecosystems are increasingly documented. We use a similar approach in the context of understanding plant defenses to herbivory, including how they are allocated between leaves and roots (constitutive defenses), and potential cross-system linkages (induced defenses). To explore these issues we utilized three different empirical approaches. First, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) and measured changes in the secondary chemistry of above- and belowground tissues. Second, we reviewed published studies that compared levels of secondary chemistry between leaves and roots to determine how plants distribute putative defense chemicals across the above- and belowground systems. Last, we used meta-analysis to quantify the impact of induced responses across plant tissue types. In the tobacco system, leaf-chewing insects strongly induced higher levels of secondary metabolites in leaves but had no impact on root chemistry. Nematode root herbivores, however, elicited changes in both leaves and roots. Virtually all secondary chemicals measured were elevated in nematode-induced galls, whereas the impact of root herbivory on foliar chemistry was highly variable and depended on where chemicals were produced within the plant. Importantly, nematodes interfered with aboveground metabolites that have biosynthetic sites located in roots (e.g., nicotine) but had the opposite effect (i.e., nematodes elevated foliar expression) on chemicals produced in shoots (e.g., phenolics and terpenoids). Results from our literature review suggest that, overall, constitutive defense levels are extremely similar when comparing leaves with roots, although certain chemical classes (e.g., alkaloids, glucosinolates) are differentially allocated between above- and belowground parts. Based on a meta-analysis of induced defense studies we conclude that: (1) foliar induction generates strong responses in leaves, but much weaker responses in roots, and (2) root induction elicits responses of equal magnitude in both leaves and roots. We discuss the importance of this asymmetry and the paradox of cross-system induction in relation to optimal defense theory and interactions between above- and belowground herbivory.

Physiological integration of roots and shoots in plant defense strategies links above‐ and belowground herbivory

Roots play a critical, but largely unappreciated, role in aboveground anti-herbivore plant defense (e.g. resistance and tolerance) and root-leaf connections may therefore result in unexpected coupling between above- and belowground consumers. Using the tobacco (Nicotiana tabacum) system we highlight two examples of this phenomenon. First, the secondary metabolite nicotine is produced in roots, yet translocated aboveground for use as a foliar resistance trait. We demonstrate that nematode root herbivory interferes with foliar nicotine dynamics, resulting in positive effects on aboveground phytophagous insects. Notably, nematode-induced facilitation only occurred on nicotine-producing plants, and not on nicotine-deficient mutants. In the second case, we use stable isotope and invertase enzyme analyses to demonstrate that foliar herbivory elicits a putative tolerance response whereby aboveground nutritional reserves are allocated to roots, resulting in facilitation of phytoparasitic nematodes. Thus, plants integrate roots in resistance and tolerance mechanisms for leaf defense, and such root-leaf connections inherently link the dynamics of above- and belowground consumers.

APHIDS ALTER THE COMMUNITY-WIDE IMPACT OF FIRE ANTS

Positive species interactions have the potential to strongly influence the structure and dynamics of ecological communities, yet surprisingly few studies have documented their general importance. We tested the hypothesis that the mutualistic association between fire ants and aphids enhances the impact of fire ants on the herbivorous and predaceous arthropod community of cotton. We found that the presence of aphids attracted foraging fire ants onto cotton plants. This shift from ground to foliar foraging resulted in more frequent interactions between fire ants and arthropods associated with cotton. The survival of herbivores (caterpillars) and predators (ladybird beetles and lacewings) was lower in the presence of fire ants and aphids compared with fire ants alone in greenhouse experiments. Similarly, fire ants and aphids deterred plant bugs from spending time on cotton foliage. Using large-scale field manipulations of fire ants along with naturally occurring aphid populations, we found that the ant–aphid ...

Disruption of Cotton Aphid (Homoptera: Aphididae)-Natural Enemy Dynamics by Red Imported Fire Ants (Hymenoptera: Formicidae)

Abstract Red imported fire ants, Solenopsis invicta (Buren) (Hymenoptera: Formicidae), are an invasive species found in high densities throughout southeastern agricultural systems. We tested the hypothesis that fire ants tend cotton aphids, Aphis gossypii Glover (Homoptera: Aphididae), and thus release them from predation by lady beetle larvae, Coccinella septempunctata L. and Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae), and green lacewing larvae, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae). Fire ants preferentially foraged on aphid-infested cotton, Gossypium hirsutum L., plants (x̄ = 103 ± 47 ants per plant) compared with plants without aphids (x̄ = 5 ± 3 ants per plant). In caged greenhouse experiments, fire ants reduced survival of lady beetle larvae by 92.9% and green lacewing larvae by 83.3%. Furthermore, strong mortality imposed on aphid predators by fire ants affected aphid survival. With the addition of fire ants to aphid-predator treatments, aphid survival approximately doubled. In a field experiment, predator larvae were more abundant in cotton plots with experimentally suppressed densities of fire ants (0.62 ± 0.11 lady beetle larvae per sample; 0.06 ± 0.02 lacewing larvae per sample) than in plots with high fire ant densities (0.23 ± 0.06 lady beetle larvae per sample; 0.01 ± 0.01 lacewing larvae per sample). Conversely, cotton aphids were more abundant in high fire ant density field plots (x̄ = 6.83 ± 0.03 aphids per leaf) than in low fire ant density plots (x̄ = 4.04 ± 0.03 aphids per leaf). These data suggest that red imported fire ants enhance cotton aphid survival and density in the field through predator interference.

Ecological Communities: Plant-mediated interactions in herbivorous insects: mechanisms, symmetry, and challenging the paradigms of competition past

Introduction Interspecific interactions between insect herbivores can be either negative (competitive) or positive (facilitative) (Damman 1993, Denno et al. 1995). In the context of traditional community ecology, however, negative interactions have received the most attention (e.g., Lawton and Strong 1981, Schoener 1982, Strong et al. 1984, Denno et al. 1995) until quite recently (e.g., Lill and Marquis 2003, Nakamura et al. 2003). Nonetheless, the importance of interspecific competition as a factor structuring communities of insect herbivores has experienced a controversial history to say the least (Strong et al. 1984, Damman 1993, Denno et al. 1995). During the 1960s and 1970s, competition was revered as a central organizing force structuring communities of phytophagous insects (Denno et al. 1995). During these decades, field investigations into interspecific competition were heavily dominated by observational studies of resource partitioning as evidence for reduced competition and thus coexistence (e.g., McClure and Price 1976, Rathcke 1976, Waloff 1979). Notably, experimental field studies documenting the occurrence of interspecific competition between insect herbivores were scarce (but see McClure and Price 1975). In the 1980s, the role of competition in structuring phytophagous insect communities was challenged severely, and within a few years it fell from a position of prominence to the status of a weak and infrequent process (Lawton and Strong 1981, Lawton 1982, Lawton and Hassell 1984, Strong et al. 1984).

Long distance root–shoot signalling in plant–insect community interactions

Plants mediate interactions between insects, including leaf- and root-feeders; yet the underlying mechanisms and connection with ecological theory remain unresolved. In this review, based on novel insights into long-distance (i.e., leaf-leaf, root-shoot) defence signalling, we explore the role of phytohormones in driving broad-scale patterns of aboveground-belowground interactions that can be extrapolated to general plant-insect relationships. We propose that the outcome of intra-feeding guild interactions is generally negative due to induction of similar phytohormonal pathways, whereas between-guild interactions are often positive due to negative signal crosstalk. However, not all outcomes could be explained by feeding guild; we argue that future studies should target ecologically representative plant-insect systems, distinguish subguilds, and include plant growth hormones to improve our understanding of plant-mediated interactions.

Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging

Most organisms face the problem of foraging and maintaining growth while avoiding predators. Typical animal responses to predator exposure include reduced feeding, elevated metabolism, and altered development rate, all of which can be beneficial in the presence of predators but detrimental in their absence. How then do animals balance growth and predator avoidance? In a series of field and greenhouse experiments, we document that the tobacco hornworm caterpillar, Manduca sexta, reduced feeding by 30–40% owing to the risk of predation by stink bugs, but developed more rapidly and gained the same mass as unthreatened caterpillars. Assimilation efficiency, extraction of nitrogen from food, and percent body lipid content all increased during the initial phase (1-3 d) of predation risk, indicating that enhanced nutritional physiology allows caterpillars to compensate when threatened. However, we report physiological costs of predation risk, including altered body composition (decreased glycogen) and reductions in assimilation efficiency later in development. Our findings indicate that hornworm caterpillars use temporally dynamic compensatory mechanisms that ameliorate the trade-off between predator avoidance and growth in the short term, deferring costs to a period when they are less vulnerable to predation.

Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis

Recent evidence suggests that competitive interactions among herbivores are mostly indirect and mediated by plant responses to herbivory. Most studies, however, emphasize chewing insects and secondary chemistry, thus ignoring the diverse group of vascular-parasites that may be more likely to compete through induced changes in phytonutrients. Using an aboveground phloem-feeding aphid (Myzus persicae) and a belowground gall-forming nematode (Meloidogyne incognita) on tobacco plants, we assessed the importance of competition via induced host–plant sinks. In a series of experimental trials, nematode root herbivory caused 55 and 72% declines in the growth and fecundity of aphids, respectively. Aphids, on the other hand, did not impact nematode performance. Therefore, we predicted that nematodes out-compete M. persicae by attenuating the magnitude of aphid-induced sinks. Through a combination of invertase enzyme measurements and stable isotope (13C and 15N) enrichment, we found evidence that both herbivores act as mobilizing sinks. Aphids attracted photoassimilates to feeding aggregations on leaves and nematode galls accumulated resources in the roots. Levels of invertase enzymes, for example, were more than fourfold higher in nematode galls than in surrounding root tissue. Yet we found no evidence supporting a sink competition model for aphid–nematode interactions. The strength of aphid-induced leaf sinks was entirely unaffected by nematode presence, and vice versa. Thus, induced host–plant sinks appear to be a common strategy employed by vascular parasites to manipulate the physiology of their host, but multi-sink competition may be limited to herbivores that co-occur on the same tissue type and/or plants under growth-limited abiotic conditions.

Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetle

Many herbivores elicit biochemical, physiological, or morphological changes in their host plants that render them more resistant to co-occurring herbivores. Yet, despite the large number of studies that investigate how induced resistance affects herbivore preference and performance, very few have simultaneously explored the cascading effects of induction on higher trophic levels and consequences for prey suppression. In our study system, early-season herbivory by leafhoppers elevated plant resistance to subsequent attack by chrysomelid beetles sharing the same host plant. Notably, beetles feeding on leafhopper-damaged plants incurred developmental penalties (e.g., prolonged time in early larval instars) that rendered them more susceptible to predation by natural enemies. As a result, the combined bottom-up effect of leafhopper-induced resistance and the top-down effect of enhanced predation resulted in the synergistic suppression of beetle populations. These results emphasize that higher trophic level dynamics should be considered in conjunction with induced resistance to better understand how plants mediate interspecific interactions in phytophagous insect communities.