Transcriptional re-programming of defense responses in Capsicum annuum roots induced by the interaction of the endophyte fungus Pochonia chlamydosporia and the plant-parasitic nematode Meloidogyne incognita

It is currently poorly understood how endophyte colonization and nematode parasitism affect host plants. To remedy this, we explored the transcriptional responses of sweet pepper ( Capsicum annuum L. cv “Crusco di Senise”) roots colonized by the endophytic and nematophagous fungus Pochonia chlamydosporia (Pc), either alone or in combination with the root-knot nematode Meloidogyne incognita (RKN). Biometric data from Pc-inoculation revealed significant growth enhancements, including increased leaf number, chlorophyll content, height, and biomass. Transcriptomic analyses highlighted most pronounced gene expression changes at 14 days after inoculation (DAI), with activation of plant defense and suppression of energy metabolism processes, indicating a trade-off between growth and defense. Functional over-representation analyses showed that Pc alone suppressed ethylene signaling, hydrolases, proteases, and terpenoid biosynthesis, the latter induced instead under RKN infection. The combined Pc+RKN treatment showed activation of phenylpropanoid biosynthesis, secondary metabolism, fungal response, and broad defense mechanisms. Despite Pc influence, gene expression patterns in the Pc+RKN treatment largely reflected RKN-induced responses, suggesting that nematode stress dominates the transcriptional landscape. Nevertheless, Pc modulated specific secondary metabolism pathways and activated key transcription factors which persisted when the nematode was present, involved in keeping defense and growth responses under combined stress. These findings highlight Pc dual role in promoting growth and enhancing resilience against RKN, supporting its potential as a biocontrol agent. The study also identifies candidate genes that could aid pepper breeding programs aimed at improving resistance to biotic stress, providing deeper insight into the molecular dynamics between beneficial fungi and parasitic nematodes in crop systems. • Pochonia chlamydosporia enhances growth and water use in pepper cv Senise roots • Early defense responses and metabolic reprogramming are primed by Pc • Pc+RKN interaction shows strong RKN-driven response, modulated by Pc presence • Pc mostly influences folate and carotenoid metabolism under combined stress • Key transcriptional hubs shared across Pc and Pc+RKN include NF-YA and BLH genes