Different concentrations of 2-Undecanone triggers repellent and nematicidal responses in Caenorhabditis elegans

The compound 2-undecanone is widely distributed in the natural environment and exhibits a dual-action mechanism against nematodes. It demonstrates repellency and contact toxicity against both Caenorhabditis elegans and Meloidogyne incognita. However, research on the dual-function mechanism of 2-undecanone remains relatively limited. In this study, using chemotaxis experiments, we found that 2-undecanone (at concentrations of 1-5 mg/mL) signal is detected through AWB olfactory sensory neurons in nematode, and then transduced through the cGMP pathway to induce repellent behavior. Moreover, we observed that 2-undecanone (at concentrations of 0.06-0.08 mg/mL) induces intracellular calcium accumulation and causes lysosomal membrane rupture. We further identified Hsp70 A and V-ATPase A as the targets of 2-undecanone responsible for its contact killing effect. Furthermore, 2-undecanone was found to alter sphingomyelin metabolism in both wild-type C. elegans and hsp-1 mutants. This alteration led to decreased acid sphingomyelinase activity, reduced ceramide levels, and increased sphingomyelin levels. These results indicated that 2-undecanone has dual functions and two target receptors Hsp70 A and V-ATPase A against nematodes, and one AWB olfactory neuron repelled nematodes. The dual-action mode of 2-undecanone can decrease the nematodes' tolerance to the compound appropriately, extending its efficacy duration. Understanding the dual function mechanism of action of 2-undecanone will aid in devising innovative approaches for managing nematode control.