From epigenetics to bacterial symbionts – towards sustainable targets of aphid pest management
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Aphids are notorious insect pests that harm ornamentals and crops by transmitting viruses and feeding on phloem sap, thus causing substantial economic damage. The extensive use of chemical insecticides is still the dominant aphid control strategy. The consequences of this are obvious: rapidly evolving resistance, environmental pollution, and risks ... to non-target organisms. For the last two decades, traditional control measures have been under debate due to an increasing ecological awareness of the society. This ongoing scenario illustrates the necessity to develop alternative, novel strategies and methods for sustainable aphid management. This dissertation is devoted to aspects of aphid biology, which should be considered to refine the application of existing and novel insecticides. Underexplored target genes and enzymes that may assist in development of new substances for aphid control are treated and RNA interference (RNAi) as a promising alternative pest control strategy is discussed in detail. The pea aphid (Acyrthosiphon pisum) is a well-known laboratory model organism to study the insect family Aphididae, insect-plant interactions, symbiosis with bacteria, aphid transmitted viruses and phenotypic plasticity. It was also the first hemipteran whose genome was fully sequenced. The intention of this thesis was to explore the role of epigenetic mechanisms in the ontogenesis of this aphid. Epigenetic modifications, e.g. the acetylation of histones, are heritable variations of DNA structure that affect gene expression or cellular functions without changes to the underlying DNA sequence. Such changes are regulated by the opposing activities of enzymes called histone acetyltransferases (KATs) and histone deacetylases (KDACs). These enzymes are essential in the regulation of numerous biological processes. In insects, the disruption of the tightly controlled equilibrium of acetylation and deacetylation of histones results in severely affected life-history traits, such as fecundity or longevity. This thesis provides a comprehensive overview of histone acetylation/deacetylation enzymes present in the genome of A. pisum. Compared to other insects, an enlarged diversity of KATs and KDACs has been identified in the pea aphid. Epigenetic multiple ligand (3,5-Bis-(3,5-dibromo-4-hydroxybenzylidene)-tetrahydro-pyran-4-one) and suberoylanilide hydroxamic acid (N-Hydroxy-N′-phenyloctandiamide) were used for chemical inhibition of these enzymes, which negatively affected survival and reproduction and delayed the development of the aphids. These findings indicate that the epigenetic machinery is a promising target system for the development of novel aphid control substances. However, specific gene silencing of the KATs kat6b, kat7, kat14, and the KDAC rpd3, mediated by RNAi, revealed mild effects on life- history traits -mentioned above (Kirfel et al., 2019). Conversely, the attenuation of the histone acetyltransferase p300/CBP severely reduced lifespan and the number of offspring of the aphids. A much shorter reproductive phase and more premature nymphs, which developed in abnormally structured ovaries, have been observed. These data confirmed the evolutionarily conserved function of p300/CBP known from other insects during ontogenesis and indicated that this protein is an ideal target for RNAi-based aphid control (Kirfel et al., 2020). It is well known, that aphids harbor the obligate bacterial symbiont Buchnera aphidicola, which is localized in a specialized organ (bacteriome), thus enabling the host to survive on a nutritionally poor phloem-sap diet by providing essential amino acids. Notably, aphids can live in symbiosis with a number of other, facultative symbionts (e.g. Serratia symbiotica, Hamiltonella defensa, and Regiella insecticola), facilitating adaptations to biotic and abiotic stress. In this context the question arose whether the symbiont S. symbiotica, which is present in the aphid line used in this study, has an effect on host fitness. In particular, the effect on the susceptibility of the aphids to different insecticidal compounds was investigated. Surprisingly, the facultative symbiont S. symbiotica was found to significantly impair the aphids’ fitness and the ability of A. pisum to tolerate different classes of insecticides, although it does provide benefits in certain circumstances (Skaljac et al., 2018). Antimicrobial peptides (AMPs), key players of the insect’s innate immune system, are short proteins with antimicrobial activity. During their long evolutionary history, aphids have lost many genes encoding AMPs, most likely because AMPs would harm their bacterial symbionts. The venoms of animals preying on insects contain molecules, including AMPs, which are highly efficient in targeting insects. Consequently, venom-derived scorpion AMPs, which are orally delivered to aphids, reduced their survival, reproduction and the density of bacterial symbionts. The AMPs compromised the bacteriome but also the aphid directly, holding the potential to be developed as bioinsecticides to replace or complement conventional insecticides for aphid control. (Luna-Ramirez et al., 2017).