Heritable Epigenomic Modifications Influence Stress Resilience and Rapid Adaptations in the Brown Planthopper (Nilaparvata lugens)

Abstract

DNA methylation in insects is integral to cellular differentiation, development, gene regulation, genome integrity, and phenotypic plasticity. However, its evolutionary potential and involvement in facilitating rapid adaptations in insects are enigmatic. Moreover, our understanding of these mechanisms is limited to a few insect species, of which none are pests of crops. Hence, we studied methylation patterns in the brown planthopper (BPH), a major rice pest, under pesticide and nutritional stress, across its life stages. Moreover, as the inheritance of epigenetic changes is fundamentally essential for acclimation, adaptability, and evolution, we determined the heritability and persistence of stress-induced methylation marks in BPH across generations. Our results revealed that DNA methylation pattern(s) in BPH varies/vary with environmental cues and is/are insect life-stage specific. Further, our findings provide novel insights into the heritability of stress-induced methylation marks in BPH. However, it was observed that, though heritable, these marks eventually fade in the absence of the stressors, thereby suggesting the existence of fitness cost(s) associated with the maintenance of the stressed epigenotype. Furthermore, we demonstrate how 5-azacytidine-mediated disruption of BPH methylome influences expression levels of stress-responsive genes and, thereby, highlight demethylation/methylation as a phenomenon underlying stress resilience of BPH.

Chromosome‐level genome assembly of the aster leafhopper (Macrosteles quadrilineatus) reveals the role of environment and microbial symbiosis in shaping pest insect genome evolution

“…Genetic elements can contribute to gene duplications and the general expansion of other gene families (Finnegan, 1989). Thus, they can enable duplication of advantageous genes, including those that respond to environmental changes such as host plant chemical defences and climate variation, particularly insecticide resistance (Aminetzach et al., 2005; González et al., 2008, 2010; Gupta & Nair, 2022; Rech et al., 2019; Rostant et al., 2012; Schrader et al., 2014; Stapley et al., 2015).…”

Epigenetic regulations as drivers of insecticide resistance and resilience to climate change in arthropod pests

“…Furthermore, the removal of DNA methylation from the esterase gene of Myzus persicae reduced the transcription of this insecticide-detoxifying enzyme (FIELD, 2000). Recently, Gupta and Nair (2022) observed genetic plasticity in brown planthoppers and clarified the role of epigenomic modifications in converting environmental stimuli into heritable changes that may reduce stress and favor insects. They also showed how 5-azacytidinemediated disruption DNA methylation influences the expression levels of some stress-responsive genes and highlighted demethylation/methylation as a phenomenon underlying rapid adaptive phenotypes (Gupta and Nair, 2022).…”

Recent Advances in Plant–Insect Interactions

“…BPH stress resilience is the subject of a paper by Ayushi Gupta and Suresh Nair [4], who studied BPH DNA methylation patterns under pesticide and nutritional stress across BPH life stages. Their results show that DNA methylation in BPH is insect life stage specific and varies with environmental cues.…”