The aphid BCR4 structure and activity uncover a new defensin peptide superfamily

Aphids (Hemiptera: Aphidoidea) are among the most injuring insects for agricultural plants and their management is a great challenge in agronomical research. A new class of proteins, called Bacteriocyte-specific Cysteine-Rich (BCR), provides an alternative to chemical insecticides for pest control. BCRs have been initially identified in the pea aphid Acyrthosiphon pisum. They are small disulfide bond-rich proteins expressed exclusively in aphid bacteriocytes, the insect derived cells that host intracellular symbiotic bacteria. Here, we show that one out of the A. pisum BCRs, BCR4, displays an outstanding insecticidal activity against the pea aphid, impairing insect survival and nymphal growth, providing evidence for its potential use as a new biopesticides. Our comparative genomics and phylogenetic analysis indicate that BCRs seem restricted to the aphid lineage. The 3D structure of the BCR4 reveals that this peptide belongs to a yet unknown structural class of peptides and defines a new superfamily of defensins.

Population Dynamics and Yield Loss Assessment for Pea Aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), on Lentil in Morocco

Pea aphid (Acyrthosiphon pisum Harris) is the major insect pest of lentil in Morocco. We investigated pea aphid mean numbers and yield losses on three lentil varieties at one location during three successive cropping seasons during 2015–2018. The effects of several weather factors on pea aphid population dynamics were investigated. Population density increased in early spring followed by several peaks during March–April and then steeply declined during the late spring. Aphid populations peaked at different times during the three years of the study. In 2016, higher populations occurred during the second and third weeks of April for Abda and Zaria varieties with averages of 27 and 28 aphids/20 twigs, respectively. In 2017, higher populations occurred on the 12th and 13th standard meteorological weeks (SMWs) for Zaria with averages of 24.7 and 27.03 aphids/20 twigs, respectively. In 2018, the population peaked for all varieties at three different times, 11th, 13th, and 17th SMW, with the highest for Zaria being 26.00, 47.41, and 32.33 aphids/20 twigs. Pea aphid population dynamics changed with weather conditions. The number of aphids significantly and positively correlated with maximum temperature, but significantly negatively correlated with relative humidity and wind speed. The minimum temperature and rainfall had non-significant correlations. Pea aphid infestation resulted in losses of total seed weight for all lentil varieties, with the highest avoidable losses for Bakria being 12.51% followed by Zaria with 7.72% and Abda with 4.56%. These losses may justify the development of integrated management options for control of this pest.

The Impact of Ultraviolet-B Radiation on the Sugar Contents and Protective Enzymes in Acyrthosiphon pisum

Natural and anthropogenic changes have been altering many environmental factors. These include the amount of solar radiation reaching the Earth’s surface. However, the effects of solar radiation on insect physiology have received little attention. As a pest for agriculture and horticulture, aphids are one of the most difficult pest groups to control due to their small size, high fecundity, and non-sexual reproduction. Study of the effects of UV-B radiation on aphid physiology may provide alternative control strategies in pest management. In this study, we examined the effects of UV-B radiation on protein and sugar contents, as well as the activities of protective enzymes, of the red and green morphs of the pea aphid over eight generations. The results indicated a significant interaction between UV-B radiation and aphid generations. Exposure of the pea aphids to UV-B radiation caused a significant decrease in the protein content and a significant increase in the glycogen and trehalose contents at each generation as measured in whole aphid bioassays. The enzyme activity of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) of the pea aphids changed significantly at each generation with UV-B treatments. The SOD activity increased over eight generations to the highest level at G7 generation. However, the enzyme activity of CAT first increased and then decreased with UV-B treatments, and POD mostly gradually decreased over the eight generations. Therefore, UV-B radiation is an environmental factor that could result in physiological changes of the pea aphid. Moreover, our study discovered that red and green aphids did not display a significant consistent difference in the response to the UV-B treatments. These results may prove useful in future studies especially for assessing their significance in the adaptation and management against UV-B radiation.

Aphids Facing Their Parasitoids: A First Look at How Chemical Signals May Make Higher Densities of the Pea Aphid Acyrthosiphon pisum Less Attractive to the Parasitoid Aphidius ervi

Herbivore-induced plant volatiles constitute the first indicators of insect host presence, and these can affect the foraging behavior of their natural enemies. The density of insect hosts may affect the nature and concentration of these plant-induced volatiles. We tested the impact of infestation density (low, intermediate, and high) of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae), feeding on the broad bean Vicia faba, on the attractiveness of the parasitoid Aphidius ervi (Hymenoptera: Braconidae), using a Y-tube olfactometer (infested vs. non-infested plants). The emitted volatile compounds from both infested and non-infested plants were collected and identified. In addition, two series of experiments were carried out to test the impact of the presence of a conspecific female parasitoid within the aphid/plant complex on the attractiveness to other females. Parasitoids were significantly more attracted to the plants with low and intermediate aphid infestation levels. The volatile blend composition of the infested plants changed in relation to aphid density and may explain the low attraction of parasitoids toward high aphid density. The presence of conspecific females on the aphid patch had no apparent impact on the behavioral choices of other parasitoid females. Our study adds a new aspect to understanding plant–aphid–parasitoid interactions, including the possibility that aphids may manipulate chemical cues of host plants affecting the orientation of parasitoids.

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

Insects harbor a variety of maternally inherited bacterial symbionts. As such, variation in symbiont presence/absence, in the combinations of harbored symbionts, and in the genotypes of harbored symbiont species provide heritable genetic variation of potential use in the insects’ adaptive repertoires. Understanding the natural importance of symbionts is challenging but studying their dynamics over time can help to elucidate the potential for such symbiont-driven insect adaptation. Toward this end, we studied the seasonal dynamics of six maternally transferred bacterial symbiont species in the multivoltine pea aphid (Acyrthosiphon pisum). Our sampling focused on six alfalfa fields in southeastern Pennsylvania, and spanned 14 timepoints within the 2012 growing season, in addition to two overwintering periods. To test and generate hypotheses on the natural relevance of these non-essential symbionts, we examined whether symbiont dynamics correlated with any of ten measured environmental variables from the 2012 growing season, including some of known importance in the lab. We found that five symbionts changed prevalence across one or both overwintering periods, and that the same five species underwent such frequency shifts across the 2012 growing season. Intriguingly, the frequencies of these dynamic symbionts showed robust correlations with a subset of our measured environmental variables. Several of these trends supported the natural relevance of lab-discovered symbiont roles, including anti-pathogen defense. For a seventh symbiont—Hamiltonella defensa—studied previously across the same study periods, we tested whether a reported correlation between prevalence and temperature stemmed not from thermally varying host-level fitness effects, but from selection on co-infecting symbionts or on aphid-encoded alleles associated with this bacterium. In general, such “hitchhiking” effects were not evident during times with strongly correlated Hamiltonella and temperature shifts. However, we did identify at least one time period in which Hamiltonella spread was likely driven by selection on a co-infecting symbiont—Rickettsiella viridis. Recognizing the broader potential for such hitchhiking, we explored selection on co-infecting symbionts as a possible driver behind the dynamics of the remaining six species. Out of twelve examined instances of symbiont dynamics unfolding across 2-week periods or overwintering spans, we found eight in which the focal symbiont underwent parallel frequency shifts under single infection and one or more co-infection contexts. This supported the idea that phenotypic variation created by the presence/absence of individual symbionts is a direct target for selection, and that symbiont effects can be robust under co-habitation with other symbionts. Contrastingly, in two cases, we found that selection may target phenotypes emerging from symbiont co-infections, with specific species combinations driving overall trends for the focal dynamic symbionts, without correlated change under single infection. Finally, in three cases—including the one described above for Hamiltonella—our data suggested that incidental co-infection with a (dis)favored symbiont could lead to large frequency shifts for “passenger” symbionts, conferring no apparent cost or benefit. Such hitchhiking has rarely been studied in heritable symbiont systems. We propose that it is more common than appreciated, given the widespread nature of maternally inherited bacteria, and the frequency of multi-species symbiotic communities across insects.

Effect of Soy Leaf Flavonoids on Pea Aphid Probing Behavior

Flavonoids detected in soybean Glycine max (L.) Merr. (Fabaceae) cause various alterations in the metabolism, behavior, and development of insect herbivores. The pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) poses potential threat to soybeans, but the effect of individual flavonoids on its feeding-associated behavior is relatively unknown. We monitored probing behavior (stylet penetration activities) of A. pisum on its preferred host plant, Pisum sativum L. untreated (control) and treated with 0.1% ethanolic solutions of flavonoids apigenin, daidzein, genistein, and kaempferol. We applied the electrical penetration graph (electropenetrography, EPG) technique, which visualizes the movements of aphid stylets within plant tissues. None of the applied flavonoids affected the propensity to probe the plants by A. pisum. However, apigenin enhanced the duration of probes in non-phloem tissues, which caused an increase in the frequency and duration of stylet mechanics derailment and xylem sap ingestion but limited the ingestion of phloem sap. Daidzein caused a delay in reaching phloem vessels and limited sap ingestion. Kaempferol caused a reduction in the frequency and duration of the phloem phase. Genistein did not affect aphid probing behavior. Our findings provide information for selective breeding programs of resistant plant cultivars to A. pisum.