Role of plant sensory perception in plant-animal interactions

Plants actively gather information about their environments via a range of sensory modalities and respond in ways that profoundly influence their interactions with other organism

Olfactory Cues from Plants Infected by Powdery Mildew Guide Foraging by a Mycophagous Ladybird Beetle

Powdery mildews (Erysiphales) are economically important plant pathogens that attack many agricultural crops. Conventional management strategies involving fungicide application face challenges, including the evolution of resistance and concerns over impacts on non-target organisms, that call for investigation of more sustainable alternatives. Mycophagous ladybird beetles (Coleoptera: Coccinellidae) feed on powdery mildew and have considerable potential as biological control agents; however, the foraging ecology and behavior of these beetles is not well understood. Here we document the olfactory cues presented by squash plants (Cucurbita moschata) infected by powdery mildew (Podosphaera sp.) and the behavioral responses of twenty-spotted ladybird beetles (Psyllobora vigintimaculata) to these cues. Volatile analyses through gas chromatography revealed a number of volatile compounds characteristic of infected plants, including 3-octanol and its analogues 1-octen-3-ol and 3-octanone. These compounds are typical “moldy” odorants previously reported in volatiles collected from other fungi. In addition, infected plants exhibited elevated emissions of several compounds also observed in collections from healthy leaves, including linalool and benzyl alcohol, which are reported to have anti-fungal properties. In Y-tube choice assays, P. vigintimaculata beetles displayed a significant preference for the odors of infected plants compared to those of healthy plants. Moreover, beetles exhibited strong attraction to one individual compound, 1-octen-3-ol, which was the most abundant of the characteristic fungal compounds identified. These results enhance our understanding of the olfactory cues that guide foraging by mycophagous insects and may facilitate the development of integrated disease-management strategies informed by an understanding of underlying ecological mechanisms

Habitat protection and removal of encroaching shrubs support the recovery of biodiversity and ecosystem functioning

Livestock overgrazing causes environmental degradation, species invasion, biodiversity loss, and productivity decline, with profound consequences for ecological sustainability and human livelihoods. Habitat protection can mitigate such impacts, but we know little about how the long-term recovery of plant communities from livestock overgrazing depends on the presence of encroaching shrubs. Here, we explored how shrub encroachment mediates the effects of habitat protection (i.e., livestock exclusion and creation of UNESCO protected areas) on biodiversity recovery and ecosystem functioning (i.e., biomass productivity). We leveraged a long-term (15–25 years) experiment of livestock exclusion and complemented it with the removal of an encroaching shrub species in pasture areas and protected areas. We reveal that habitat protection has positive effects on patterns of recovery. Yet, the effects of habitat protection are mediated by shrub encroachment. Encroaching shrubs have net positive effects on plant diversity in pasture areas but inhibit biodiversity recovery in protected areas. The combination of habitat protection and the removal of encroaching shrubs best enhances the recovery of plant diversity and biomass productivity. A potential underlying mechanism is the shift in plant interactions from facilitation for recruitment and associated resistance to competition for water. Understanding species interactions is key to guiding conservation and restoration actions which can turn degraded ecosystems back into functional, species-rich communities

Leaf trichomes affect caterpillar feeding in an instar-specific manner

Leaf trichomes play well-established roles in defense against insect herbivores, both as a physical barrier that impedes herbivore movement and by mediating chemical defenses. However, little work has examined how different trichome types influence herbivory by herbivores at different stages of development. We examined whether caterpillar instar and trichome type (glandular or non-glandular) affected the ability of the specialist herbivore caterpillar Manduca sexta to initiate feeding on 11 Solanaceous species exhibiting variation in the density and type of leaf trichomes. Our results suggest that non-glandular trichomes are far more effective than glandular trichomes in deterring the initiation of feeding by first- and second-instar caterpillars. Meanwhile, neither glandular nor non-glandular trichomes significantly affected the ability of third-instar caterpillars to commence feeding. These findings suggest that while non-glandular trichomes deter feeding initiation by early instar caterpillars, the contribution of both trichomes on later instars may depend on effects after feeding initiation

Herbivory and inbreeding affect growth, reproduction, and resistance in the rhizomatous offshoots of Solanum carolinense (Solanaceae)

Resource sharing within clonal plant networks can occur via the translocation of water, nutrients, and photoassimilates through rhizomes and stolons. Similar mechanisms may mediate the sharing of information (e.g., about herbivory or other environmental stressors) among ramets via molecular or biochemical signals. The storage of such information in belowground structures could facilitate the transmission of appropriate phenotypic responses across growing seasons in perennial species. However, few previous studies have explored the potential transfer of ecologically relevant information within such networks. This study addresses the effects of foliar herbivory and belowground overwintering on the growth and flowering, physical defenses, and herbivore resistance in the clonally spreading species Solanum carolinense L. (Solanaceae). We used rhizomes from inbred and outbred plants that were repeatedly exposed to feeding damage by Manduca sexta L. (Sphingidae) caterpillars and rhizomes from undamaged control plants. These rhizomes were either planted immediately or exposed to overwintering conditions and allowed to produce new ramets (rhizomatous offshoots). We then assessed offshoot emergence, flowering, physical defense traits, and herbivore performance. Relative to controls, offshoots of herbivore-damaged plants exhibited greater spine and trichome densities, and reduced performance of M. sexta larvae. However, they also emerged and flowered significantly later, and produced fewer flowers than offshoots of undamaged plants. Inbreeding also negatively affected offshoot emergence, flowering, trichome production, and herbivore resistance. These effects of parental herbivory were more pronounced in outbred offshoots, indicating that inbreeding may compromise the trans-seasonal induction of plant defenses. Finally, exposure to overwintering conditions increased trichome production and reduced caterpillar performance on offshoots. Together, these results show that induced defenses can be transmitted through rhizomes and affect offshoot growth, flowering, defensive traits, and herbivore resistance. They also document fitness-related costs associated with defense induction in offshoots and suggest that the transfer of defenses across seasons can be compromised by inbreeding

Soil-borne fungi alter the apoplastic purinergic signaling in plants by deregulating the homeostasis of extracellular ATP and its metabolite adenosine

Purinergic signaling activated by extracellular nucleotides and their derivative nucleosides trigger sophisticated signaling networks. The outcome of these pathways determine the capacity of the organism to survive under challenging conditions. Both extracellular ATP (eATP) and Adenosine (eAdo) act as primary messengers in mammals, essential for immunosuppressive responses. Despite the clear role of eATP as a plant damage-associated molecular pattern, the function of its nucleoside, eAdo, and of the eAdo/eATP balance in plant stress response remain to be fully elucidated. This is particularly relevant in the context of plant-microbe interaction, where the intruder manipulates the extracellular matrix. Here, we identify Ado as a main molecule secreted by the vascular fungus Fusarium oxysporum. We show that eAdo modulates the plant's susceptibility to fungal colonization by altering the eATP-mediated apoplastic pH homeostasis, an essential physiological player during the infection of this pathogen. Our work indicates that plant pathogens actively imbalance the apoplastic eAdo/eATP levels as a virulence mechanism

Horizontal Gene Acquisitions, Mobile Element Proliferation, and Genome Decay in the Host-Restricted Plant Pathogen \u3ci\u3eErwinia Tracheiphila\u3c/i\u3e

Modern industrial agriculture depends on high-density cultivation of genetically similar crop plants, creating favorable conditions for the emergence of novel pathogens with increased fitness in managed compared with ecologically intact settings. Here, we present the genome sequence of six strains of the cucurbit bacterial wilt pathogen Erwinia tracheiphila (Enterobacteriaceae) isolated from infected squash plants in New York, Pennsylvania, Kentucky, and Michigan. These genomes exhibit a high proportion of recent horizontal gene acquisitions, invasion and remarkable amplification of mobile genetic elements, and pseudogenization of approximately 20% of the coding sequences. These genome attributes indicate that E. tracheiphila recently emerged as a host-restricted pathogen. Furthermore, chromosomal rearrangements associated with phage and transposable element proliferation contribute to substantial differences in gene content and genetic architecture between the six E. tracheiphila strains and other Erwinia species. Together, these data lead us to hypothesize that E. tracheiphila has undergone recent evolution through both genome decay (pseudogenization) and genome expansion (horizontal gene transfer and mobile element amplification). Despite evidence of dramatic genomic changes, the six strains are genetically monomorphic, suggesting a recent population bottleneck and emergence into E. tracheiphila’s current ecological niche

Competition matters: using in vitro community models to study the impact of human skin bacteria on mosquito attraction

The human skin bacteria play an important role in the production of volatiles that attract mosquitoes. Using some of the most abundant human skin bacterial species, we created in vitro community models to assess whether increased microbial biodiversity could reduce human attractiveness to females of the dengue fever mosquito Aedes aegypti and whether co-culturing bacterial commensals affects overall attraction. More complex bacterial models were less attractive to female mosquitoes than the simplest models. For instance, the triple bacterial community model was approximately three times less attractive than Staphylococcus epidermidis alone. Our data show, for instance, that an in vitro community model mimicking the skin composition of a highly attractive individual to the anthropophilic Anopheles gambiae was also more attractive to anthropophilic Ae. aegypti than a community model mimicking the skin composition of a poorly attractive individual to An. gambiae. In line with these results, volatile analyses of the blends emitted by the different in vitro community models showed that the more complex models had lower emission overall. Effects on mosquito responses differed sharply when the different bacteria species were sharing the same resources used for growth, showing that either competition or commensalism may influence their relative growth, and that this consequently can influence mosquito responses. We conclude that studies on mosquito responses to skin volatiles need to take the microbial community into account

Insect Eggs Can Enhance Wound Response in Plants: A Study System of Tomato Solanum lycopersicum L. and Helicoverpa zea Boddie

Insect oviposition on plants frequently precedes herbivory. Accumulating evidence indicates that plants recognize insect oviposition and elicit direct or indirect defenses to reduce the pressure of future herbivory. Most of the oviposition-triggered plant defenses described thus far remove eggs or keep them away from the host plant or their desirable feeding sites. Here, we report induction of antiherbivore defense by insect oviposition which targets newly hatched larvae, not the eggs, in the system of tomato Solanum lycopersicum L., and tomato fruitworm moth Helicoverpa zea Boddie. When tomato plants were oviposited by H. zea moths, pin2, a highly inducible gene encoding protease inhibitor2, which is a representative defense protein against herbivorous arthropods, was expressed at significantly higher level at the oviposition site than surrounding tissues, and expression decreased with distance away from the site of oviposition. Moreover, more eggs resulted in higher pin2 expression in leaves, and both fertilized and unfertilized eggs induced pin2 expression. Notably, when quantified daily following deposition of eggs, pin2 expression at the oviposition site was highest just before the emergence of larvae. Furthermore, H. zea oviposition primed the wound-induced increase of pin2 transcription and a burst of jasmonic acid (JA); tomato plants previously exposed to H. zea oviposition showed significantly stronger induction of pin2 and higher production of JA upon subsequent simulated herbivory than without oviposition. Our results suggest that tomato plants recognize H. zea oviposition as a signal of impending future herbivory and induce defenses to prepare for this herbivory by newly hatched neonate larvae