Abstract
Here, we reveal that the regulation of Drosophila odorant receptor (OR) expression during the pupal stage is permissive and imprecise. We found that directly after hatching an OR feedback mechanism both directs and refines OR expression. We demonstrate that, as in mice, dLsd1 and Su(var)3-9 balance heterochromatin formation to direct OR expression. We show that the expressed OR induces dLsd1 and Su(var)3-9 expression, linking OR level and possibly function to OR expression. OR expression refinement shows a restricted duration, suggesting that a gene regulatory critical period brings olfactory sensory neuron differentiation to an end. Consistent with a change in differentiation, stress during the critical period represses dLsd1 and Su(var)3-9 expression and makes the early permissive OR expression permanent. This induced permissive gene regulatory state makes OR expression resilient to stress later in life. Hence, during a critical period OR feedback, similar to in mouse OR selection, defines adult OR expression in Drosophila.
Highlights
Olfactory sensory neurons (OSNs) in most vertebrates and insects are specified to express a single odorant receptor (OR) from a large repertoire of OR genes in the genome [1,2,3,4]
Drosophila chemoreceptor expression matures during the first few days of adult life We and others have observed that OR reporter expression varies between OSNs in day-old flies, rising to the uniform high level observed in adult flies after a few days (Fig 1A) [26]
We found that 13 of 22 antennal ionotropic receptor (IR) and 8 of 10 gustatory receptor (GR) expressed in OSNs increased 1-fold or more
Summary
Olfactory sensory neurons (OSNs) in most vertebrates and insects are specified to express a single odorant receptor (OR) from a large repertoire of OR genes in the genome [1,2,3,4]. Two OR gene regulatory models have been described: the vertebrate probabilistic selection model and the invertebrate predetermined instructive model. The vertebrate OR regulatory model depends on chromatin state changes—from a repressed state to an active state and back again to a general repressed state [5,6]. In mice, nonexpressed OR genes are embedded in constitutive heterochromatin marked by histone H3 lysine 9 trimethylation (H3K9me3) [5,7]. According to a mathematical model of OR regulation, a yet-to-be-identified H3K9me demethylase sporadically opens the constitutive.
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