Abstract

BACKGROUND Terpenes, abundant in pine trees, function as chemical defenses against pathogens such as the pinewood nematode, the agent of destructive pine wilt disease (PWD). Paradoxically, certain terpenes like α-pinene and β-pinene are known to enhance pinewood nematode population growth; however, the mechanisms behind this adaptation remain unclear. This study aims to investigate how terpenes influence nematode physiology, resource allocation, and pathogenicity. RESULTS High terpene concentrations (137.6 mg/mL), particularly the 10:8 α-pinene/β-pinene ratio prevalent in pinewood nematode-infected pines, enhance nematode population growth and thus pathogenicity by redirecting lipid reserves toward reproduction, while depleting resources for body size and shortening lifespan. Transcriptomic analyses reveal that terpenes up-regulate genes in lysosomal pathways. Pharmacological inhibition of lysosomes and RNA interference knockdown of the lysosomal regulator HLH-30/TFEB suppress reproduction and extend lifespan, suggesting key roles of lysosomal signaling in the trade-off between reproduction and lifespan. CONCLUSION Pinewood nematode co-opts host defensive compounds as signals, triggering a lysosome-mediated shift in resource allocation that favors rapid population expansion and enhanced pathogenicity at the expense of individual longevity. Targeting lysosomal signaling or terpene biosynthesis could disrupt nematode adaptation, offering innovative strategies for sustainable PWD management. © 2026 Society of Chemical Industry.