Single-cell multi-omic characterization of the soybean root response to cyst nematode infection
Soybean cyst nematodes parasitize soybean roots by inducing the formation of multinucleate syncytia to feed and complete their life cycle. However, the molecular basis of syncytia initiation and development remains limited. Here, we generated an integrated single-nucleus RNA and chromatin accessibility profile of soybean roots from infected and uninfected plants. We profiled 56,448 high-quality nuclei and identified all major root cell types, including distinct subpopulations enriched with syncytial nuclei. Transcriptomic and chromatin accessibility analyses support their procambium cell signature that progresses through distinct stages associated with immune suppression, cell fusion, and endoreduplication. Integrative gene expression and transcription factor motif chromatin accessibility analyses identified CAMTA1, as a key transcriptional repressor of defense-related genes including receptor-like kinases (RLKs), whereas MYB, MYB-related, and E2F as transcriptional activators that coordinate cell wall remodeling, chromatin modification and DNA replication, respectively, across developmental trajectories. These findings provide mechanistic insights into host reprogramming during nematode parasitism and a foundational resource for engineering nematode-resistant soybean. Overall design: To dissect the molecular responses of soybean roots to SCN infection and track syncytium development, we performed snRNA-seq and scATAC-seq on mock-inoculated and SCN-infected soybean roots from the susceptible genotype Williams 82 at 5 days post-inoculation (DPI) with two biological replicates. The soybean roots were inoculated with infective J2 and allowed to infect the roots for 24 hours after which the roots were washed to remove any J2 that had not yet penetrated the roots. This step allowed for the collection of root tissue with a higher percentage of sedentary life stages of SCN enabling the capture of a mix of initial syncytial cells through developing syncytia up to a maximum of ~4 days old.