A critical period terminates the differentiation of olfactory sensory neurons

Development generates a vast number of neuron types and classes. When and how neuronal differentiation end is poorly understood. Here, we show that Drosophila olfactory sensory neurons (OSNs) matures during a critical period and reveal that the differentiation termination mechanism is similar to the mammalian odorant receptor (OR) choice mechanism. We first showed that initiation of Drosophila OR expression required heterochromatin opening and a H3K9me3 demethylase, Kdm4b. Further genetic studies demonstrated that Lsd1 and su(var)3-9, similar to mouse, were required to balance heterochromatin in order to stabilize OR expression. Expression analysis showed that Lsd1, su(var)3-9 increased and Kdm4b decreased during the first two days after eclosion. We further showed that environment changes during the period, but not after, caused permanent transformed Lsd1, su(var)3-9 and Kdm4b expression and altered OR gene regulation. These results together suggest the last step in OSN terminal differentiation to be a gene regulatory critical period.