Natural variation in the transcriptional response of Drosophila melanogaster to oxidative stress

Abstract

Broadly distributed species must cope with diverse and changing environmental conditions, including various forms of stress. Cosmopolitan populations of Drosophila melanogaster are more tolerant to oxidative stress than those from the species’ ancestral range in sub-Saharan Africa, and the degree of tolerance is associated with an insertion/deletion polymorphism in the 3’ untranslated region of the Metallothionein A (MtnA) gene that varies clinally in frequency. We examined oxidative stress tolerance and the transcriptional response to oxidative stress in cosmopolitan and sub-Saharan African populations of D. melanogaster, including paired samples with allelic differences at the MtnA locus. We found that the effect of the MtnA polymorphism on oxidative stress tolerance was dependent on the genomic background, with the deletion allele increasing tolerance only in a northern, temperate population. Genes that were differentially expressed under oxidative stress included MtnA and other metallothioneins, as well as those involved in glutathione metabolism and other genes known to be part of the oxidative stress response or the general stress response. A gene co-expression analysis revealed further genes and pathways that respond to oxidative stress including those involved in additional metabolic processes, autophagy, and apoptosis. There was significant overlap among the genes induced by oxidative and cold stress, which suggests a shared response pathway to these two stresses. Interestingly, the MtnA deletion was associated with consistent changes in the expression of many genes across all genomic backgrounds, regardless of the expression level of the MtnA gene itself. We hypothesize that this is an indirect effect driven by the loss of microRNA binding sites within the MtnA 3’ untranslated region.

Zinc in Cognitive Impairment and Aging

“…Under the condition of oxidative stress [ 228 ], the expressions of MtnA and other metallothioneins, genes involved in glutathione metabolism, and other genes known to belong to oxidative stress responses or general stress response, increase. MtnA also responds to genes and pathways of additional metabolic processes, autophagy, and apoptosis [ 229 ]. Overexpression of MT in cells can protect lysosomes from estrogen-induced damage and maintain viability while inhibiting autophagy [ 230 ].…”

Genome-wide temperature-sensitivity of PcG regulation and reduction thereof in temperateDrosophila melanogaster

“…Prx2540 -2 encodes for a peroxidase with functions in oxidative stress response, and as well as the product of Amyrel , it was shown to have neuroprotective effects and to be involved in healthy aging (Detienne et al 2018; Rai et al 2021). This might be related to that, compared to tropical flies, temperate flies are thought to be better at dealing with oxidative stress (González et al 2009; Guio et al 2014; Ramnarine et al 2022).…”

Angelica keiskei Impacts the Lifespan and Healthspan of Drosophila melanogaster in a Sex and Strain-Dependent Manner

“…The JIV flies are an outbred population derived from flies originally collected in 1978, derived from an Amherst, Massachusetts population established by P.T. Ives in 1975 (#149) [ 48 , 49 ]. This population has been cultured for more than 700 generations with controlled densities of 50–80 eggs per vial.…”