Epigenetic regulation clocks the multigenerational olfactory imprinting in C. elegans

Imprinting is an early sensory life experience that induces adult behaviours, such as mother recognition or homing. In a previous study, we demonstrated a striking olfactory imprinting in C. elegans that can be inherited over generations. When exposed to specific odorants during a timely controlled post-hatch period, C. elegans worms display during adulthood an enhanced migration towards these molecules. In order to unveil some of the genetic and epigenetic factors that are responsible for such a behavioural plasticity, we assessed the role of heterochronic genes using a candidate gene approach. We report here that translation of the Hunchback-Like 1 (HBL1) transcription factor in the sensory processing interneuron AIY, is a determining factor for olfactory plasticity timing in C.elegans. HBL1 may associate to the SPR1/CoREST co-repressor, the lysine demethylase SPR5/LSD1 and the histone deacetylase HDA3 to lengthen the plasticity period, whereas the translation initiation factor IFE-4 and the histone deacetylase HDA2 abridge it. We also observed that lengthened plasticity periods allow proportionally faster stable behavioral adaptation of C. elegans populations. We conclude that plasticity timing is a key factor, not only to transiently adapt individuals but also to stably adapt animal populations via multigenerational accumulation of experience.