Inhibition of histone acetylation and deacetylation enzymes affects longevity, development, and fecundity in the pea aphid (Acyrthosiphon pisum)

Abstract

Histone acetylation is an evolutionarily conserved epigenetic mechanism of eukaryotic gene regulation which is tightly controlled by the opposing activities of histone acetyltransferases (HATs) and histone deacetylases (HDACs). In insects, life-history traits such as longevity and fecundity are severely affected by the suppression of HAT/HDAC activity, which can be achieved by RNA-mediated gene silencing or the application of chemical inhibitors. We used both experimental approaches to investigate the effect of HAT/HDAC inhibition in the pea aphid (Acyrthosiphon pisum) a model insect often used to study complex life-history traits. The silencing of HAT genes (kat6b, kat7, and kat14) promoted survival or increased the number of offspring, whereas targeting rpd3 (HDAC) reduced the number of viviparous offspring but increased the number of premature nymphs, suggesting a role in embryogenesis and eclosion. Specific chemical inhibitors of HATs/HDACs showed a remarkably severe impact on life-history traits, reducing survival, delaying development, and limiting the number of offspring. The selective inhibition of HATs and HDACs also had opposing effects on aphid body weight. The suppression of HAT/HDAC activity in aphids by RNA interference or chemical inhibition revealed similarities and differences compared to the reported role of these enzymes in other insects. Our data suggest that gene expression in A. pisum is regulated by multiple HATs/ HDACs, as indicated by the fitness costs triggered by inhibitors that suppress several of these enzymes simultaneously. Targeting multiple HATs or HDACs with combined effects on gene regulation could, therefore, be a promising approach to discover novel targets for the management of aphid pests. K E Y W O R D S acetyltransferase, deacetylase, epigenetics, life-history, RNA interference

Histone acetylation regulates the expression of genes involved in worker reproduction and lifespan in the ant Temnothorax rugatulus

“…In social insects, histone acetylation has previously been linked to various processes including the regulation of foraging behavior and caste determination (Simola et al, 2016(Simola et al, , 2013Spannhoff et al, 2011;Wojciechowski et al, 2018), but evidence for the regulation of life history traits such as fecundity and longevity have been lacking so far. In contrast, in solitary insects such as the pea aphid, the inhibition of histone acetylation and deacetylation affects development, fertility, and longevity (Kirfel, Kessel, Skaljac, Seip, & Vilcinskas, 2020). In fact, fertility appears to be regulated by this epigenetic mark in various taxonomic groups, which includes other insects such as the planthopper Nilaparvata lugens (Zhang et al, 2018), but also mammals including mice (Ma, Pan, Montgomery, Olson, & Schultz, 2012) and men (Wang, Gao, Li, & Liu, 2019).…”

10-hydroxy-2E-decenoic acid (10HDA) does not promote caste differentiation in Melipona scutellaris stingless bees

“…The expression starts to increase in the late-larvae stages and reach a dramatic increase in 1-day-old pupae 59 , as we also observed for queen but not for worker pupae in M. scutellaris . In addition, recently, it was suggested a role for HDAC1 in embryogenesis and in eclosion in pea aphids 62 . All together, these evidences indicate that HDAC1 may be potentially involved in insects development.…”

10-hydroxy-2E-decenoic Acid (10HDA) is not a Caste-differentiation Factor in Melipona Scutellaris Stingless Bees

“…scutellaris. In addition, recently, it was suggested a role for HDAC1 in embryogenesis and in eclosion in pea aphids [61] . All together, these evidences indicate that HDAC1 may be potentially involved in insects development across different species.…”