From leaves to aphid honeydew: the zucchini plants enrich bacterium to recruit natural enemy to resist herbivore attacks

Plants have evolved intricate defense strategies to combat herbivorous insect attacks, including the production of toxic secondary metabolites and the attraction of natural enemies. While bacterial-mediated direct toxicity in plant defenses has been demonstrated, the ecological mechanisms by which plants utilize bacteria to indirectly modulate the behavior of natural enemies remain insufficiently explored. In this study, we observed a significant enrichment of Staphylococcus in the tissues of zucchini Cucurbita pepo following infestation by the cotton-melon aphid Aphis gossypii. These bacteria traced from the damaged plant stems and leaves were subsequently found both in aphids and in their secreted honeydew. Among the four dominant bacterial strains isolated from the honeydew, Staphylococcus sp. markedly promoted oviposition preference in mated female ladybird beetles Propylea japonica. Further investigation identified a volatile organic compound, 4-Isopropylbenzyl alcohol, released by Staphylococcus sp. that stimulated strong antennal responses and attracted P. japonica to lay eggs. Collectively, our findings demonstrate that zucchini plants can employ indirect defense against A. gossypii through the enrichment of specific bacteria, revealing a novel ecological role for bacteria in plant defense and expanding our understanding of complex plant-microbe-insect-natural enemy interactions.