Trichoderma harzianum T39 induces resistance against downy mildew by priming for defense without costs for grapevine

Downy mildew caused by Plasmopara viticola is one of the most destructive grapevine diseases worldwide. The biocontrol agent Trichoderma harzianum T39 (T39) has previously been shown to be an inducer of grapevine resistance, and we aimed at characterizing the molecular mechanisms activated by T39 and the energy costs of the induced resistance in terms of plant growth. Here, we showed that T39 reduced downy mildew severity on susceptible grapevines under controlled greenhouse conditions by a direct modulation of defense-related genes and the activation of priming for enhanced expression of these genes after pathogen inoculation. The stronger local than systemic modulation of defense-related genes corresponded to an higher local than systemic disease control in T39-treated plants. The activation of a priming state was confirmed by the absence of any negative effect of T39 on grapevine growth, shoot and root weight, leaf dimension and chlorophyll content, in contrast to benzothiadiazole (BTH) applications. Priming of defense gene expression was greater in T. harzianum T39- than in BTH-treated plants. The modulation of marker genes suggested the involvement of jasmonic acid and ethylene signals in the defense processes induced by T39, in contrast to the salicylic acid pathway activated by BTH. These results offer a greater understanding of the mechanisms underlying the grapevine induced resistance and indicate that T. harzianum T39 can be used to control downy mildew without apparent costs for grapevine growth.