Abstract
Animals use pheromones as a conspecific chemical language to respond appropriately to environmental changes. The soil nematode Caenorhabditis elegans secretes ascaroside pheromones throughout the lifecycle, which influences entry into dauer phase in early larvae, in addition to sexual attraction and aggregation. In adult hermaphrodites, pheromone sensory signals perceived by worms usually elicit repulsion as an initial behavioral signature. However, the molecular mechanisms underlying neuronal pheromone sensory process from perception to repulsion in adult hermaphrodites remain poorly understood. Here, we show that pheromone signals perceived by GPA-3 is conveyed through glutamatergic neurotransmission in which neuronal DAF-16/FoxO plays an important modulatory role by controlling glutaminase gene expression. We further provide evidence that this modulatory role for DAF-16/FoxO seems to be conserved evolutionarily by electro-physiological study in mouse primary hippocampal neurons that are responsible for glutamatergic neurotransmission. These findings provide the basis for understanding the nematode pheromone signaling, which seems crucial for adaptation of adult hermaphrodites to changes in environmental condition for survival.
Highlights
Pheromones serve as a chemical language through which organisms of the same species communicate in response to environmental changes, including the presence of stress, different sexes and food scarcity
To identify some molecular components involved in perception of pheromones, we screened G-protein subunit genes by assessing the chemotaxis index of C. elegans that had been exposed to three major ascaroside pheromones as a measure of perception of pheromones[8] (Fig. S1a)
We provide a previously unexplored basic framework for neuronal components that are likely involved in neurotransmission of pheromone signals and a potential modulatory role of neuronal DAF-16/FoxO in this process
Summary
Pheromones serve as a chemical language through which organisms of the same species communicate in response to environmental changes, including the presence of stress, different sexes and food scarcity. The nematode ascaroside pheromones have been known to signal worms to enter dauer phase, a non-aging state, under unfavorable growth conditions 1–5. These ascaroside pheromones (pheromones) are involved in diverse biological processes (e.g., sexual attraction, aggregation, and fungal traps) depending on their developmental stage (early larvae vs adults) and sex (hermaphrodites vs male) 6–9. When adult hermaphrodites sense the pheromones, they elicit repulsion response as an initial behavioral output[10]. Despite decades-long research on pheromone function, its perception, the molecular pathway in adult hermaphrodites that starts from an initial pheromone perception to elicit behavioral outputs as a repulsive response is not fully understood. We show that pheromone sensory signals are likely conveyed through glutamatergic neurotransmission in which neuronal DAF-16/FoxO plays an important modulatory role
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