Maternal mRNAs underlie higher heat tolerance in tropical vs. temperate Drosophila melanogaster embryos
Authors: Emily Mikucki; Thomas O'Leary; Brent Lockwood
Affiliation: University of Vermont, Burlington, VT
Keywords: d. evolution of gene expression; o. canalization/robustness
The earliest stages of embryogenesis are particularly sensitive to environmental change, relative to other life stages. This phenomenon has been attributed to the transcriptional silence of early embryos, yet transcriptional responses to environmental change have not been fully characterized in the developing embryo. Previously, we demonstrated that tropical Drosophila melanogaster embryos have greater tolerance to acute heat stress than temperate North American embryos, suggesting that there is adaptive genetic variation in embryonic heat tolerance. In order to elucidate the molecular physiological basis of genetic differences in embryonic heat tolerance, we sequenced mRNA from early D. melanogaster embryos from tropical isofemale lines that were collected from 5 populations around the globe (Mexico, St. Kitts, Ghana, India, and Guam) and temperate North American lines collected from Vermont, USA. Early embryos (0-1 h old) were exposed to heat stress (32°C, 34°C, or 36°C) or control conditions (25°C) for 45 minutes prior to RNA sequencing. Out of ~29,868 sequenced transcripts, 828 (2.8%) differentiated the transcriptomes of tropical vs. temperate embryos, and all of these transcripts significantly correlated with heat tolerance among the lines. Functional enrichment analysis indicated that tropical embryos had higher abundances of maternally loaded transcripts that encode proteins involved in the oxidative stress response. We also found that tropical and temperate embryos exhibited similar changes in the abundance of 4,534 gene transcripts in response to temperature. 671 of these transcripts were induced by heat shock, indicating that embryos were transcriptionally active in the face of heat stress. Overall, our data indicate that tolerance to environmental perturbation during embryogenesis involves the oxidative stress response, corroborating recent studies on the important role of redox balance in fly development. Further, we demonstrate that transcriptional activity in the early zygote is context dependent.