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

The study determined the effect of endophyte colonization and nematode parasitism on the transcriptional responses of roots of sweet pepper, Capsicum annuum (cv “Crusco di Senise”), colonized by the fungus Pochonia chlamydosporia (Pc), either alone or in combination with the root-knot nematode Meloidogyne incognita (RKN). Pc-inoculation allowed significant growth enhancements, increased the number of leaves, chlorophyll content, height, and biomass. Transcriptome analyses showed most pronounced gene expression changes 14 days after inoculation (dai). Activation of plant defense and suppression of energy metabolism indicated a trade-off between growth and defense. Pc alone suppressed ethylene signaling, hydrolases, proteases, and terpenoid biosynthesis, the latter being induced under RKN parasitism. The combined Pc+RKN treatment showed activation of phenylpropanoid biosynthesis, secondary metabolism, fungal response, and broad defense mechanisms. Gene expression in the Pc+RKN treatment largely reflected RKN-induced responses, as nematode-induced stress dominated the transcriptional landscape. Nevertheless, Pc modulated specific secondary metabolism and activated key transcription factors which persisted when the nematode was present, keeping defense and growth responses under combined stress. The findings highlight Pc dual role in promoting growth and enhancing resilience against RKN, supporting and integrating its potential as a biocontrol agent. The study also identified candidate genes useful in pepper breeding programs aimed at improving resistance to biotic stress, with insights into the molecular dynamics between beneficial fungi and parasitic nematodes.