Multilayered defense responses in sugarcane against Pratylenchus zeae revealed by comparative transcriptomics

The root-lesion nematode <i>Pratylenchus zeae</i> ranks among the most pervasive soilborne threats to global sugarcane (<i>Saccharum</i> spp.) production; however, the molecular basis of host resistance to this pathogen remains largely unexplored. Using comparative transcriptomics 15 days after inoculation, we profiled root response patterns of a resistant cultivar (RB966928) and a susceptible cultivar (CTC9001). Analysis of differentially expressed genes (DEGs) identified 3,385 DEGs (1,426 up, 1,959 down) in the susceptible CTC9001 and 8,689 DEGs (5,334 up, 3,355 down) in the resistant RB966928 when comparing control and inoculated plants, revealing distinct genotype-specific defense strategies. The resistant genotype mounted a coordinated, multilayered defense marked by dramatic transcriptional reprogramming, including intensified glycolysis and fatty-acid biosynthesis, elevated oxidoreductase/reactive oxygen species activity, and concurrent activation of jasmonic and salicylic acid-associated pathways, with strong induction of multiple pathogenesis-related protein 1 homologs. RB966928 also showed pre-primed and inducible resistance gene analogs and targeted cell-wall reinforcement through xyloglucan fucosylation. By contrast, CTC9001 displayed a delayed or attenuated response characterized by cell-proliferation signatures and broad activation of callose-related defenses (1,3-β-D-glucan synthesis) that appear insufficient to limit nematode progression. Gene ontology enrichment analysis revealed that the resistant response was dominated by biological processes linked to carbohydrate and lipid metabolism, oxidoreductase activity, hormone signaling, and cell-wall organization, whereas the susceptible response was enriched in stress-related pathways lacking coordinated metabolic and structural reinforcement. Collectively, these findings indicate that durable resistance to <i>P. zeae</i> is unlikely to arise from a single mechanism, and effective protection will require stacking complementary defense layers, including early metabolic reprogramming, robust hormone-mediated signaling, and reinforced cell-wall barriers. The candidate RGAs, PR1 homologs, and cell-wall remodeling enzymes identified here, together with the GO-enriched pathways, provide concrete targets for marker-assisted breeding and gene editing strategies aimed at developing sugarcane cultivars with durable nematode resistance.