Alterations in Histone Methylation States Increased Profusion of Lethal(2)-Essential-for-Life-Like (l(2)elf), Trithorax and Polycomb Genes in Apis mellifera under Heat Stress

Simple Summary The honeybee subspecies Apis mellifera jemenitica is highly adapted to extreme summer temperatures. This adaptation can be explained by many anatomical, behavioral and molecular components. Basically, many genes are upregulated/silenced in response to stressors. Histone post-translational modifications (PTMs) represent an important gene regulation mechanism in insects. Here, we investigated how the methylation/demethylation of histone (H3) lysine (K4 and K27) impacts the profusion of lethal(2)-essential-for-life-like (l(2)efl), histone methyltransferases (HMTs) and Polycomb genes in A. m. jemenitica and A. m. carnica under thermal stress. The results revealed significant alterations in histone methylation states leading to a higher profusion of l(2)efl and harmonized changes in HMTs and Polycomb genes in response to heat stress with a substantial variation between both honeybee subspecies. Apparently, histone PTMs can diminish the impact of thermal stress and increase the fitness of both honeybee subspecies. In conclusion, the methylation/demethylation of H3K4 and H3K27 is a key epigenetic mechanism in regulating l(2)efl, histone methyltransferases (HMTs) (trx) and Polycomb genes in A. mellifera exposed to heat stress. Abstract Histone post-translational modifications (PTMs) represent a key mechanism in the thermal adaptation of the honeybee Apis mellifera. In this study, a chromatin immunoprecipitation assay and qPCR were employed to explore the changes in the methylation states of H3K4m2, H3K4m3, H3K27m2 and H3K27m3 associated with l2efl (ID: 72474, 724405, 724488), histone methyltransferases (HMTs) ((trx) and PR-set7) and Polycomb (Pc) and (Su(z)12) genes in A. m. jemenitica (tolerant subspecies) and A. m. carnica (susceptible subspecies) in response to heat treatment (42 °C for 1 h). The results revealed significant enrichment fold changes in the methylation/demethylation of most H3K4 and H3K27 marks at all targeted genes. These changes increased the profusion of l2efl (ID: 72474, 724405, 724488), histone methyltransferases (HMTs) (trx) and Polycomb (Pc) and Su(z)12 and decreased the profusion of HMT (PR-set7) in both honeybee subspecies. The changes in the methylation enrichment folds of histone methyltransferases (HMTs) ((trx), PR-set) and Polycomb (Pc), Su(z)12 genes demonstrate the well-harmonized coordination of epigenetic gene regulation in response to heat treatment. Compared to the control, the changes in the methylation enrichment folds of H3K4m3 at Polycomb Su(z)12 were about 30× and 100× higher in treated A. m. jemenitica and A.m. carnica, respectively. Similarly, changes in the methylation/demethylation enrichment folds of HMT (trx) and Polycomb (Pc) and Su(z)12 were 2–3× higher in A. m. carnica than in A. m. jemenitica after treatment (42 °C). It is evident that post-translational chromatin modification in both honeybee subspecies can diminish heat stress impact by (I) increasing the transcriptional provision of l2efl associated with survival and (II) increasing the silencing of genes associated with general cellular activities.