Tanespimycin and rapamycin exhibit antifungal activity against Colletotrichum gloeosporioides and enhance mango resistance to anthracnose via differentially modulating heat shock response

Abstract

Postharvest mango (Mangifera indica L.) fruit suffer tremendous loss due to anthracnose inflicted by Colletotrichum spp. Fungicides and heat treatment are often used to control the disease, while biocontrol agents are eco-friendly alternatives. Streptomyces are antagonistic organisms against plant pathogens; however, the mechanisms and active components are unclear. Here, we evaluated the antifungal actions of S. hygroscopicus metabolites tanespimycin and rapamycin against anthracnose. Within the range of 0.01–0.1 μM, tanespimycin and rapamycin reduced fungal growth by at least 60.4% and 40.4%, respectively in vitro. In mango fruit, tanespimycin upregulated MiHSP101, MiHSP90, MiHSP70, and MiHSP18.2 by 5.8-, 1.9-, 4.8-, and 3.3-fold, respectively, and increased HSP101 and HSP70 protein by 2.2-fold. On the other hand, rapamycin did not affect HSP expression. Pathogen-challenge assays revealed tanespimycin and rapamycin exerted antifungal and defense-eliciting dual actions, where pre-challenge treatment of tanespimycin and rapamycin inhibited pathogen growth by 73.7% and 78.4%, respectively in mango 5 d post infection. Finally, in a 20 °C storage experiment, tanespimycin and rapamycin extended the fruit shelf life by 6 d and exerted comparable antifungal effects as hot water treatment without deteriorating fruit quality. In conclusion, we elucidated the antifungal and defense-eliciting actions of S. hygroscopicus metabolites and revealed mechanistic discrepancies regarding HSP regulation. These findings support the development of new disease management strategies and advance the knowledge regarding the roles of HSP in crop defense.