IbPIF1 confers stem nematode resistance by regulating secondary metabolites in sweet potato

The stem nematode (Ditylenchus destructor Thorne) is a pervasive and destructive plant-parasitic nematode worldwide, inflicting severe agricultural and economic losses in a wide range of crops. Despite its global impact, the molecular mechanisms underlying plant resistance to this pathogen remain poorly understood. Our previous studies in sweet potato (Ipomoea batatas L.) identified IbPIF1 as one of the most strongly induced genes following stem nematode infection, positioning it as a key candidate for unravelling host defence strategies. In this study, we revealed that overexpression of IbPIF1 not only activates systemic immunity and strengthens physical barrier functions, but also drives the accumulation of phytoalexins, significantly enhancing nematode resistance in transgenic plants. Furthermore, IbPIF1 enhances the accumulation of defensive compounds, including lignin, callose and terpenoids, which are vital for the resilience of plants against stem nematode infection. Intriguingly, genetic and molecular analysis shows that IbMVD, a pivotal gene in the regulation of terpenoid synthesis, operates downstream of IbPIF1 in this defence network. Specifically, IbPIF1 directly binds to the promoter of IbMVD, inducing its expression and thereby modulating terpenoid-mediated resistance. These results suggest that IbPIF1 plays a pivotal regulatory role in a complex transcriptional network controlling the stem nematode response. This work advances our understanding of plant-nematode interactions and opens avenues for engineering nematode-resistant crops through genetic manipulation.