Linking Histone Methylation States and hsp Transcriptional Regulation in Thermo-Tolerant and Thermo-Susceptible A. mellifera L. Subspecies in Response to Heat Stress

Abstract

Genetic and epigenetic responses to environmental cues of worker honeybees mediate hsp synthesis, a key mechanism to tolerate high ambient temperatures in Apis mellifera. In this study, the chromatin immunoprecipitation assay followed by qPCR were used to determine alterations in histone methylation states (H3K27me2, H3K27me3, H3K4me2, and H3K4me3) associated with hsp/hsc/trx in A. m. jemenetica (thermo-tolerant subspecies) and A. m. carnica (thermo-susceptible subspecies) after heat treatment. The results revealed significant changes in enrichment folds of histone methylation states associated with hsp/hsc/trx. Indeed, the enrichment of H3K27me2 decreased strongly in response to heat stress. Changes in histone methylation states were significantly higher in A. m. carnica samples compared to A. m. jemenitica samples. Our study provides a new perception on linking histone post-translational methylation as an epigenetic mechanism of gene regulation with hsp/hsc/trx in A. mellifera subspecies exposed to heat stress.

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

“…Still, the enrichment fold values at all histone marks (especially at gene silencing mark H3K27) might demonstrate potentially higher transcriptional levels of l2efl (ID: 72474, 724405, 724488) in A. m. jemenitica compared to A. m. carnica even under control conditions and higher response (sensitivity) in A. m. carnica in response to heat stress. Modification of the chromatin methylation states at H3K4 and H3K27 was previously reported to increase the profusion of HSP70 in both honeybee subspecies under desert conditions, demonstrating a higher response variation in A. m. carnica due to treatment (42 • C) [28].…”

“…The decreased profusion of PR-set7 in response to treatment, mainly in A.m. carnica, indicates higher methylation activities at H3. This remolding of H3K4 at HMT (trx), HMT (PR-set7) and l2efl (as well as HSP70 [28]) demonstrated a high harmonized coordination of gene activation in response to heat treatment. The relatively higher profusion of l2efl (ID: 72474, 724405, 724488) and HMT (trx) in A. m. carnica after treatment is expected.…”

“…Yet, hsp transcription might be associated with epigenetic inheritance [25][26][27]. Histone post-translational modifications (PTMs) represent the main epigenetic mechanism of thermal adaptation in A. mellifera [27][28][29]. These modifications include the methylation, acetylation, ubiquitination and phosphorylation of histone proteins leading to the upregulation/silencing of targeted genes [27,29,30].…”

Expression Levels of Heat-Shock Proteins in Apis mellifera jemenetica and Apis mellifera carnica Foragers in the Desert Climate of Saudi Arabia

“…The heat-resistance mechanisms of Apis mellifera can include genetic or epigenetic modifications of the individual honeybee [ 20 , 21 , 33 ]. Heat-shock proteins (HSPs) are expressed in the cells of all organisms [ 34 ] and play a key role in the thermoregulation of insects, including Apis mellifera [ 35 , 36 , 37 ].…”

“…The expression of heat-shock proteins to increased ambient temperatures [ 39 ] is typically rapid, but unstressed cells keep the transcription of the inducible heat-shock proteins (HSPs) inactive. In a recent study, the exposure of A. m. jemnetica nurse bees to sublethal heat induced the transcriptional activation of many heat-shock protein genes by remodeling histone methylation states [ 33 ]. While some heat-shock proteins (HSPs) are induced by environmental stressors, others are continuously expressed during normal cell function [ 35 ].…”