Genome sequence of the English grain aphid, Sitobion avenae and its endosymbiont Buchnera aphidicola

The English grain aphid, Sitobion avenae, is a major agricultural pest of wheat, barley and oats, and one of the principal vectors of Barley Yellow Dwarf Virus (BYDV) leading to significant reductions in grain yield, annually. Emerging resistance to and increasing regulation of insecticides has resulted in limited options for their control. Using PacBio HiFi data, we have produced a high quality draft assembly of the S. avenae genome; generating a primary assembly with a total assembly size of 475.7 Mb, and an alternate assembly with a total assembly size of 430.8 Mb. Our primary assembly was highly contiguous with only 326 contigs and a contig N50 of 15.95 Mb. Assembly completeness was estimated at 97.7% using BUSCO analysis and 31,007 and 29,037 protein coding genes were predicted from the primary and alternate assemblies, respectively. This assembly, which is to our knowledge the first for an insecticide resistant clonal lineage of English grain aphid, will provide novel insight into the molecular and mechanistic determinants of resistance and will facilitate future research into mechanisms of viral transmission and aphid behavior.

Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (Sitobion avenae)

Benzoxazinoids are important secondary metabolites in gramineae plants and have inhibitory and toxic effects against a wide range of herbivore pests. However, the relationship between benzoxazinoid level and plant resistance to aphids remains controversial. In this study, we investigated the relationship between benzoxazinoids composition and concentration in wheat leaves and the resistance to the grain aphid Sitobion avenae. Overall, six benzoxazinoids were detected and identified by mass spectrometry based metabolites profiling, including three lactams, two hydroxamic acids, and one methyl derivative. The constitutive levels of these benzoxazinoids were significantly different among the wheat varieties/lines. However, none of these benzoxazinoids exhibited considerable correlation with aphid resistance. S. avenae feeding elevated the level of 2-O-β-D-glucopyranosyl-oxy-4,7-dimethoxy-(2H)-1,4-benzoxazin-3(4H)-one (HDMBOA-Glc) and reduced the level of 2-O-β-D-glucopyranosyloxy-4-hydroxy-7-(2H)-methoxy-1,4-benzoxazin-3(4H)-one (DIMBOA-Glc) in some of the wheat varieties/lines. Moreover, aphid-induced level of DIMBOA-Glc was positively related with callose deposition, which was closely associated with aphid resistance. Wheat leaves infiltrated with DIMBOA-Glc caused a noticeable increase of callose deposition and the effect was in a dose dependent manner. This study suggests that the constitutive level of benzoxazinoids has limited impact on S. avenae. Aphid feeding can affect the balance of benzoxazinoids metabolism and the dynamic level of benzoxazinoids can act as a signal of callose deposition for S. avenae resistance. This study will extend our understanding of aphid–wheat interaction and provides new insights in aphid-resistance wheat breeding.

Novel Temporal Expression Patterns of EBF-Binding Proteins in Wing Morphs of The Grain Aphid Sitobion miscanthi

High chemosensitivity of insects to volatile organic compounds (VOC) stimuli is mediated by odorant binding proteins (OBPs). In aphids, three OBPs (OBP3, OBP7 and OBP9) are E-β-farnesene (EBF)-binding proteins. Winged aphids are generally more sensitive than wingless aphids to VOCs, thus, wing presence is a phenotypic correlate of olfaction sensitivity. Here, we investigate the detailed temporal expression of these EBF-binding proteins and two other OBPs (OBP6 and OBP10), in the grain aphid Sitobion miscanthi 0 h, 2 h, 1 day, 3 days, 10 days, and 20 days after adult emergence. Both winged and wingless aphids were examined to further uncover phenotypic specification. Then, the expression patterns before and after EBF induction were analyzed. Throughout adulthood, only OBP7 had significantly higher antennal expression in winged aphids; however, there was no significant difference in the antennal expression of OBP3 between wing morphs at most time points. Except it was lower in newly emerged winged aphids but increased rapidly to the same level in wingless aphids at 1 day. OBP9 did not differ in expression between the morphs and was the only OBP that did not exhibit an expression trough at the beginning of the adult stage (0 h). The expression of OBP9 remained relatively stable and high throughout the adult stage in both phenotypes, showing the highest level among the three EBF-binding proteins. After EBF induction, its expression was further up-regulated in both morphs. Therefore, this protein may be an important molecule for EBF recognition in aphids. OBP7 strongly responded to EBF but only in winged aphids, suggesting that this protein is important in the more sensitive EBF recognition process of winged aphids. In addition, the antennal expression level of OBP3 did not respond to EBF induction. These findings revealed a temporal expression pattern of OBPs in aphids and showed that figuring out the pattern is critical for correctly selecting morphs and sampling times, which will support the discovery of reliable findings and allow solid conclusions to be drawn. Our findings also inspire on the interaction mode of the three EBF-binding proteins in relation to EBF perception in aphids.

Spatial and Temporal Variation in the Aphid–Parasitoid Interaction under Different Climates

Global warming will increase pest insect population sizes and diminish the effectiveness of biological control. This biological control failure scenario appears to be of particular concern for areas with a significant increase in maximum temperatures, such as the increase experienced in the Central Valley of Chile over the last 40 years. We assessed the impact of different climatic zones and maximum temperatures along the coast and the Chilean Central Valley on the grain aphid (Sitobion avenae) density, parasitism rate, and facultative endosymbionts in wheat fields during the growing season in the springs of 2017 and 2018. A significant effect on aphid density due to zones and maximum temperatures was detected; however, this depended on the zone and year analyzed. Changes between zones and seasons were observed for parasitism rates, while maximum temperatures only significantly affected the parasitism rate in 2017. The main parasitoid wasp found was Aphidius ervi in both zones and seasons. Regiella insecticola infected 95% of the samples in both zones, although it does not seem to have a protective role at the field level. Our findings suggest that, at present, global warming does not significantly affect the grain aphid outbreaks and their biological control in Chile. However, this study points out the importance of pre-emptive monitoring to detect aphids and the synchrony loss of their parasitoid wasps.

Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations

Understanding the role of facultative endosymbionts on the host’s ecology has been the main aim of the research in symbiont–host systems. However, current research on host–endosymbiont dynamics has failed to examine the genetic background of the hosts and its effect on host–endosymbiont associations in real populations. We have addressed the seasonal dynamic of facultative endosymbiont infections among different host clones of the grain aphid Sitobion avenae, on two cereal crops (wheat and oat) and whether their presence affects the total hymenopteran parasitism of aphid hosts at the field level. We present evidence of rapid seasonal shifts in the endosymbiont frequency, suggesting a positive selection of endosymbionts at the host-level (aphids) through an agricultural growing season, by two mechanisms; (1) an increase of aphid infections with endosymbionts over time, and (2) the seasonal replacement of host clones within natural populations by increasing the prevalence of aphid clones closely associated to endosymbionts. Our results highlight how genotypic variation of hosts can affect the endosymbiont prevalence in the field, being an important factor for understanding the magnitude and direction of the adaptive and/or maladaptive responses of hosts to the environment.