Tri-Trophic Effects of Seasonally Variable Induced Plant Defenses Vary across the Development of a Shelter Building Moth Larva and Its Parasitoid

Plant chemical defenses can negatively affect insect herbivore fitness, but they can also decrease herbivore palatability to predators or decrease parasitoid fitness, potentially changing selective pressures on both plant investment in production of chemical defenses and host feeding behavior. Larvae of the fern moth Herpetogramma theseusalis live in and feed upon leaf shelters of their own construction, and their most abundant parasitoid Alabagrus texanus oviposits in early instar larvae, where parasitoid larvae lay dormant for most of host development before rapidly developing and emerging just prior to host pupation. As such, both might be expected to live in a relatively constant chemical environment. Instead, we find that a correlated set of phenolic compounds shows strong seasonal variation both within shelters and in undamaged fern tissue, and the relative level of these compounds in these two different fern tissue types switches across the summer. Using experimental feeding treatments, in which we exposed fern moth larvae to different chemical trajectories across their development, we show that exposure to this set of phenolic compounds reduces the survival of larvae in early development. However, exposure to this set of compounds just before the beginning of explosive parasitoid growth increased parasitoid survival. Exposure during the period of rapid parasitoid growth and feeding decreased parasitoid survival. These results highlight the spatial and temporal complexity of leaf shelter chemistry, and demonstrate the developmental contingency of associated effects on both host and parasitoid, implying the existence of complex selective pressures on plant investment in chemical defenses, host feeding behavior, and parasitoid life history.     

Herbivore-specific elicitation of photosynthesis by mirid bug salivary secretions in the wild tobacco Nicotiana attenuata

Herbivory is thought to be detrimental to plant fitness and commonly results in a metabolic shift in the plant: photosynthetic processes are typically down-regulated, while resource allocation to defenses is increased in herbivore-attacked plants, resulting in fitness costs of induced plant responses. Wild tobacco, Nicotiana attenuata, attacked by Tupiocoris notatus mirid bugs becomes resistant against more damaging herbivores through mirid-induced direct and indirect defenses. However, mirid-induced resistance and tissue loss do not result in a reduction of plant fitness. These findings suggest induced metabolic responses allowing the plant to compensate for the lost tissue and resources allocated to defenses. While feeding by Manduca sexta larvae results in a strong down-regulation of photosynthesis, we demonstrate a specific induction of elevated photosynthetic activity in N. attenuata leaves by elicitors in mirid salivary secretions. The elevated CO(2) assimilation rate is sufficient to compensate for the loss of photosynthetically active tissue and balances the net photosynthesis of infested leaves. We discuss the observed increase in the plant's primary metabolic activity as a mechanism that allows plants to alleviate negative fitness effects of mirid attack and mediates the vaccination effects that result in a net benefit in environments with multiple herbivores.     

GAP-43 regulates NCAM-180-mediated neurite outgrowth

The neural cell adhesion molecule (NCAM), and the growth-associated protein (GAP-43), play pivotal roles in neuronal development and plasticity and possess interdependent functions. However, the mechanisms underlying the functional association of GAP-43 and NCAM have not been elucidated. In this study we show that (over)expression of GAP-43 in PC12E2 cells and hippocampal neurons strongly potentiates neurite extension, both in the absence and in the presence of homophilic NCAM binding. This potentiation is crucially dependent on the membrane association of GAP-43. We demonstrate that phosphorylation of GAP-43 by protein kinase C (PKC) as well as by casein kinase II (CKII) is important for the NCAM-induced neurite outgrowth. Moreover, our results indicate that in the presence of GAP-43, NCAM-induced neurite outgrowth requires functional association of NCAM-180/spectrin/GAP-43, whereas in the absence of GAP-43, the NCAM-140/non-receptor tyrosine kinase (Fyn)-associated signaling pathway is pivotal. Thus, expression of GAP-43 presumably acts as a functional switch for NCAM-180-induced signaling. This suggests that under physiological conditions, spatial and/or temporal changes of the localization of GAP-43 and NCAM on the cell membrane may determine the predominant signaling mechanism triggered by homophilic NCAM binding: NCAM-180/spectrin-mediated modulation of the actin cytoskeleton, NCAM-140-mediated activation of Fyn, or both.     

Co(i)-ordinating defenses: NaCOI1 mediates herbivore- induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses

Arabidopsis and tomato plants mutated in the F-box protein COI1 mediating jasmonate (JA) responses are more susceptible to herbivores in laboratory trials, but the exact mechanisms of COI1-mediated resistance are not known. We silenced COI1 by transformation with an inverted repeat construct (ir-coi1) in Nicotiana attenuata, a plant the direct and indirect defenses of which against various herbivores have been well studied. ir-coi1 plants are male sterile and impaired in JA-elicited direct [nicotine, caffeoylputrescine and trypsin proteinase inhibitor (TPI) activity] and indirect (cis-alpha-bergamotene emission) defense responses; responses not elicited by JA treatment (ethylene production and flower TPI activity) were unaffected. Larvae of Manduca sexta, a common herbivore of N. attenuata, gained three times more mass feeding on ir-coi1 than on wild-type (WT) plants in glasshouse experiments. By regularly moving caterpillars to unattacked leaves of the same plant, we demonstrate that larvae on WT plants can grow and consume leaves as fast as those on ir-coi1 plants, a result that underscores the role of COI1 in mediating locally induced resistance in attacked leaves, and the importance of herbivore movement in avoiding the induced defenses of a plant. When transplanted into native habitats in the Great Basin Desert, ir-coi1 plants suffer greatly from damage by the local herbivore community, which includes herbivores not commonly found on N. attenuata WT plants. Choice assays with field-grown plants confirmed the increased attractiveness of ir-coi1 plants for both common and unusual herbivores. We conclude that NaCOI1 is essential for induced resistance in N. attenuata, and that ir-coi1 plants highlight the benefits of herbivore movement for avoiding induced defenses.     

Symbiont‐mediated chemical defense in the invasive ladybird Harmonia axyridis

The volatile alkylpyrazines methyl‐ and methoxypyrazines (MPs) present in the reflex bleeds of coccinellid beetles such as the harlequin ladybird beetle Harmonia axyridis are important semiochemicals that function in antipredatory defense behavior. Pyrazines have also been coadapted from a primarily defensive role into pheromones that function in intraspecific communication, attraction, and aggregation behavior. However, the biosynthesis of MPs in ladybird beetles is poorly understood. Here, we tested the hypothesis that MPs could be produced by microbial symbionts in H. axyridis, which generates four different MPs. The evaluation of tissue‐specific MP production showed that MP concentrations were highest in the gut tissue and hemolymph of the beetles rather than the fat body tissue as the presumed site of MP biosynthesis. Furthermore, manipulation of gut microbiota by antibiotic‐containing diets resulted in a lower MP content in adult beetles. The analysis of the bacterial community of the digestive tract revealed the presence of bacteria of the genera Serratia and Lactococcus which are reportedly able to produce MPs. In line with the known diet‐dependent production of MP in H. axyridis, we determined that the presence or relative abundance of some of the potential MP producers (Enterococcus and Staphylococcus) is also diet‐dependent. We hypothesize a potential role of the microbiota in MP production in H. axyridis as a possible example for outsourcing the synthesis of ecologically important semiochemicals to its gut bacteria.     

Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores

Acylsugars are secondary metabolites exuded from type IV glandular trichomes that provide broad-spectrum insect suppression for Solanum pennellii Correll, a wild relative of cultivated tomato. Acylsugars produced by different S. pennellii accessions vary by sugar moieties (glucose or sucrose) and fatty acid side chains (lengths and branching patterns). Our objective was to determine which acylsugar compositions more effectively suppressed oviposition of the whitefly Bemisia tabaci (Gennadius) (Middle East—Asia Minor 1 Group), tobacco thrips, Frankliniella fusca (Hinds), and western flower thrips, Frankliniella occidentalis (Pergande). We extracted and characterized acylsugars from four S. pennellii accessions with different compositions, as well as from an acylsugar-producing tomato breeding line. We also fractionated the acylsugars of one S. pennellii accession to examine the effects of its components. Effects of acylsugars on oviposition were evaluated by administering a range of doses to oviposition sites of adult whiteflies and thrips in non-choice and choice bioassays, respectively. The acylsugars from S. pennellii accessions and the tomato breeding line demonstrated differential functionality in their ability to alter the distribution of whitefly oviposition and suppress oviposition on acylsugar treated substrates. Tobacco thrips were sensitive to all compositions while western flower thrips and whiteflies were more sensitive to acylsugars from a subset of S. pennellii accessions. It follows that acylsugars could thus mediate plant-enemy interactions in such a way as to affect evolution of host specialization, resistance specificity, and potentially host differentiation or local adaptation. The acylsugars from S. pennellii LA1376 were separated by polarity into two fractions that differed sharply for their sugar moieties and fatty acid side chains. These fractions had different efficacies, with neither having activity approaching that of the original exudate. When these two fractions were recombined, the effect on both whiteflies and thrips exceeded the sum of the two fractions’ effects, and was similar to that of the original exudate. These results suggest that increasing diversity of components within a mixture may increase suppression through synergistic interactions. This study demonstrates the potential for composition-specific deployment of acylsugars for herbivore oviposition suppression, either through in planta production by tomato lines, or as biocides applied by a foliar spray.