Early Soybean–Nematode Interactions: Transcriptomic Responses of <i>Meloidogyne incognita</i> at the Preparasitic Stage and Metabolomic Profiling of Root Exudates
Yuewen Dou, Ye Jiang, Minghui Huang, Dan Jiang, Doudou Chang, Lili Wu, Qilan Wang, Lei Guo, Liuli Wei, Bo Xu, Chunjie Li, Congli Wang
Abstract
Understanding the molecular and metabolic interplay between Meloidogyne incognita and soybean ( Glycine max) root exudates is essential for unraveling plant–nematode interactions. This study investigates the transcriptomic responses of M. incognita during the preparasitic stage and the metabolomic changes in soybean root exudates influenced by nematode activity. Transcriptomic analysis identified 846 differentially expressed genes in nematodes exposed to root exudates (S-Mi) compared with nematodes alone (Mi). Upregulated genes, including those encoding sensory receptors such as G-protein-coupled receptors, nuclear hormone receptors, acetylcholine receptors, and key effectors, indicate a shift toward parasitic readiness. The downregulation of detoxification genes (e.g., cytochrome P450) and the upregulation of lysosome-related genes, such as cathepsins L-like cysteine proteases suggest metabolic reprogramming to support infection. Metabolomic profiling identified 781 metabolites across S-Mi, Mi, and Soy (root exudates alone), with enriched pathways such as tyrosine metabolism and cytochrome P450-related detoxification. Interestingly, amino acids such as L-threonine and arginylthreonine were upregulated in S-Mi, suggesting their role in nematode attraction. Additionally, lipid-like metabolites, such as 3-epipapyriferic acid and physagulin F, were elevated, potentially influencing nematode behavior and modulating plant defense response. An integrated cellular model illustrates how nematode sensory receptors detect root signals, activating cyclic adenosine monophosphate, phospholipase C, and mitogen-activated protein kinase signaling cascades, as well as acetylcholine receptor-mediated ion channels, leading to effector gene activation and metabolic shifts. This study reveals a bidirectional interaction at the preparasitic stage, where soybean root exudates reprogram nematode metabolism, and nematodes, in turn, modify root exudates to influence plant defenses, offering novel targets for sustainable nematode management.