Deciphering Plant-Insect-Microorganism Signals for Sustainable Crop Production.

Agricultural crop productivity relies on the application of chemical pesticides to reduce pest and pathogen damage. However, chemical pesticides also pose a range of ecological, environmental and economic penalties. This includes the development of pesticide resistance by insect pests and pathogens, rendering pesticides less effective. Alternative sustainable crop protection tools should therefore be considered. Semiochemicals are signalling molecules produced by organisms, including plants, microbes, and animals, which cause behavioural or developmental changes in receiving organisms. Manipulating semiochemicals could provide a more sustainable approach to the management of insect pests and pathogens across crops. Here, we review the role of semiochemicals in the interaction between plants, insects and microbes, including examples of how they have been applied to agricultural systems. We highlight future research priorities to be considered for semiochemicals to be credible alternatives to the application of chemical pesticides.

Herbivore induced fruit volatiles guide the solitary tephritid endoparasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in selecting an oviposition substrate.

Oviposition in a generalist parasitoid is a complex process that involves interactions among its host, host plant, and spatiotemporal environment. Our study was aimed at exploring the ability of a generalist parasitic wasp, Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), in perceiving odor cues from its host insect [Oriental fruit fly Bactrocera dorsalis (Hendel, Diptera: Tephritidae)] in infested mango fruits. A series of experiments involving behavioral and electrophysiological studies suggest that D. longicaudata is able to distinguish host infested fruit volatiles from uninfested. Additionally, we found that D. longicaudata can distinguish between high and low-level infestations using specific cues emanating from fruits. Coupled gas chromatography-electroantennographic detection (GC-EAD) and gas chromatography-mass spectrometry (GC-MS) analysis of infested mango fruit head space volatiles identified compounds such as ethyl butanoate, ethyl 3-hydroxybutyrate, ß-myrcene, trans-ß-ocimene, allo-ocimene, ethyl octanoate, ethyl-α-toulate, ß-elemene, ß-caryophyllene, humulene, caryophyllene oxide, ethyl dodecanoate, ethyl hexadecanoate, 2-furancarboxylic acid, 3-hydroxy-2-methyl-4-pyrone, and phenethyl alcohol emanated from three different host treatments with different levels of larval infestation which elicited antennal responses in D. longicaudata. We suggest that these cues might play a significant role in attracting D. longicaudata in the field.

Estragole, a potential attractant of the winged melon aphid Aphis gossypii.

BACKGROUND: Aphids are sap-sucking insect pests of economic importance. They exhibit polyphenism, producing two kinds of morphotypes; winged (alate) and wingless (aptera) morphs. While wingless morphs can be controlled by insecticides, winged morphs are a challenge for targeted control measures as they can fly. Although colored sticky traps are used to control and monitor winged aphids, only a small population is trapped, making sticky traps less effective in controlling aphids. Studies have shown that fragrant oils applied to sticky traps increased attraction of sap-sucking insects like whiteflies and thrips. Here, we tested selected essential oils for their attractiveness to winged Aphis gossypii in potato fields. RESULTS: In field assays, selected essential oils with yellow or colorless sticky traps attracted more winged A. gossypii than controls. The combination of yellow traps baited with essential oils attracted ~2-3-fold more winged A. gossypii than did colorless traps baited with essential oils. In a multi-cycle 2 year study, yellow sticky traps baited with basil oil consistently attracted more winged A. gossypii than yellow sticky traps baited with lavender, geranium or tea tree oils. In electrophysiological studies, winged A. gossypii's antennae responded consistently to estragole in basil oil. In olfactometer assays with estragole, winged A. gossypii spent significantly more time in the treatment arm of the olfactometer than in the control arm, validating estragole's attractiveness. Furthermore, yellow sticky traps baited with pure estragole, in potato fields, attracted similar number of winged A. gossypii as yellow sticky traps baited with basil oil. CONCLUSION: Our findings demonstrate the potential of using basil oil as a potential attractant to improve the efficacy of sticky traps in the monitoring and control of winged aphids. © 2023 Society of Chemical Industry.

The greater wax moth, Galleria mellonella (L.) uses two different sensory modalities to evaluate the suitability of potential oviposition sites.

An ovipositing insect evaluates the benefits and risks associated with the selection of an oviposition site for optimizing the fitness and survival of its offspring. The greater wax moth, Galleria mellonella (L.), uses beehives as an oviposition site. During egg-laying, the gravid wax moth confronts two kinds of risks, namely, bees and conspecific larvae. While bees are known to attack the moth's offspring and remove them from the hive, the conspecific larvae compete for resources with the new offspring. To date, little is known about the mechanisms involved in the assessment of oviposition site by the greater wax moth, G. mellonella (L.). Here, we demonstrate that the wax moth uses two different sensory modalities to detect risks to its offspring in the hives of Apis cerena. Bees appear to be detected by the contact-chemoreception system of the gravid wax moth, while detection of conspecifics relies on the olfactory system. Hence, our findings suggest that two different sensory modalities are used to detect two different risks to the offspring and that the selection of oviposition sites by G. mellonella (L.) relies on the integration of inputs from both the olfactory and contact-chemoreception systems.

Antennal Transcriptome of the Fruit-Sucking Moth Eudocima materna: Identification of Olfactory Genes and Preliminary Evidence for RNA-Editing Events in Odorant Receptors.

Unappealing shriveled fruits are a characteristic of one of the most elusive fruit pests. The perpetrator, Eudocima materna, attacks the fruit at a fully formed stage and, therefore, the antennal transcriptome for this insect was deduced to identify the molecular elicitors involved in the attraction to its host plants. A total of 260 olfactory genes, including 16 odorant-binding proteins (OBPs), four pheromone-binding proteins (PBPs), 40 antennal-binding proteins (ABPs), 178 odorant receptors (ORs), 17 chemosensory proteins (CSPs) and five sensory neuron membrane proteins (SNMPs) were identified. Phylogenetic analysis shows the divergence of E. materna proteins from closely related lepidopterans and provides insights on genes that have exclusively evolved in this insect. STRING network analysis revealed interactions of olfactory proteins among themselves and the proteins of other groups. Interestingly, online tools predicted RNA-editing events in the odorant receptor sequences, suggesting the possibility of multiple protein forms. Transcripts matching transposable element sequences were also detected in the dataset. Thus, the work reported here provides a valuable resource to design molecular methods for pest control.

Endosymbiotic Bacteria Aid to Overcome Temperature Induced Stress in the Oriental Fruit Fly, Bactrocera dorsalis.

Endosymbiotic microbiota are known to have an enormous impact on their host, influencing its physiology, behavior, fitness, and various other aspects. The present study hypothesizes that certain bacterial symbionts aid the Oriental fruit fly, Bactrocera dorsalis in its adaptation to survive thermal stress encountered in the environment. Investigative studies on the change in gut and reproductive tract microbiota diversity of male and female B. dorsalis revealed that certain genera of Acinetobacter, Brevibacillus, Bacillus, Enterobacter, Enterococcus, Pseudomonas, and Staphylococcus were involved in the adaptation of B. dorsalis to temperature stresses. The intestinal and reproductive tract bacterial community of B. dorsalis varied depending on the temperature the insects were reared at. We hypothesized that the microbiota present in B. dorsalis' gut helped it endure temperature stresses over prolonged periods. Out of 54 bacterial isolates, 25, 15, and 14 isolates were obtained from flies reared at 27 °C, 18 °C, and 35 °C, respectively. A 16S rDNA analysis revealed that the bacterial isolates (reared at different temperatures) belonged to different genera. The flies were supplemented with antibiotics to suppress the existing gut microbiota and subsequently fed with bacterial isolates from flies reared at 18 °C, 27 °C (control) or 35 °C separately. When these flies were placed in incubators pre-set at the above temperatures, the survival rate exhibited by the flies differed significantly. The flies fed with bacterial isolates from 18 °C could survive only in incubators pre-set at 18 °C, while flies fed with bacterial isolates from 35 °C could survive only at 35 °C and not vice versa. The microbiota supplementation assay established that the presence of specific bacterial isolates aided the flies' survival under varied thermal stresses.

Salicylic Acid Induces Changes in Mango Fruit that Affect Oviposition Behavior and Development of the Oriental Fruit Fly, Bactrocera dorsalis.

The Oriental fruit fly, Bactrocera dorsalis (Hendel) is an important quarantine pest around the globe. Although measures for its control are implemented worldwide through IPM and male annihilation, there is little effect on their population. Hence, there is a need for new strategies to control this minacious pest. A strategy that has received negligible attention is the induction of 'natural plant defenses' by phytohormones. In this study, we investigated the effect of salicylic acid (SA) treatment of mango fruit (cv. Totapuri) on oviposition and larval development of B. dorsalis. In oviposition choice assays, gravid females laid significantly less eggs in SA treated compared to untreated fruit. Headspace volatiles collected from SA treated fruit were less attractive to gravid females compared to volatiles from untreated fruit. GC-MS analysis of the headspace volatiles from SA treated and untreated fruit showed noticeable changes in their chemical compositions. Cis-ocimene and 3-carene (attractants to B. dorsalis) were reduced in the headspace volatiles of treated fruit. Further, reduced pupae formation and adult emergence was observed in treated fruit compared to control. Increased phenol and flavonoid content was recorded in treated fruit. We also observed differential expression of anti-oxidative enzymes namely catalase (CAT), polyphenoloxidase (PPO) and peroxidase (POD). In summary, the results indicate that SA treatment reduced oviposition, larval development and adult emergence of B. dorsalis and suggest a role of SA in enhancing mango tolerance to B. dorsalis.

Oviposition site-selection by Bactrocera dorsalis is mediated through an innate recognition template tuned to γ-octalactone.

Innate recognition templates (IRTs) in insects are developed through many years of evolution. Here we investigated olfactory cues mediating oviposition behavior in the oriental fruit fly, Bactrocera dorsalis, and their role in triggering an IRT for oviposition site recognition. Behavioral assays with electrophysiologically active compounds from a preferred host, mango, revealed that one of the volatiles tested, γ-octalactone, had a powerful effect in eliciting oviposition by gravid B. dorsalis females. Electrophysiological responses were obtained and flies clearly differentiated between treated and untreated substrates over a wide range of concentrations of γ-octalactone. It triggered an innate response in flies, overriding inputs from other modalities required for oviposition site evaluation. A complex blend of mango volatiles not containing γ-octalactone elicited low levels of oviposition, whereas γ-octalactone alone elicited more oviposition response. Naïve flies with different rearing histories showed similar responses to γ-octalactone. Taken together, these results indicate that oviposition site selection in B. dorsalis is mediated through an IRT tuned to γ-octalactone. Our study provides empirical data on a cue underpinning innate behavior and may also find use in control operations against this invasive horticultural pest.