Transcriptomic insights into the tripartite plant–pathogen–mycoparasite interaction reveal novel mechanisms involving fungal secretomes and plant amino acid metabolism
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The tomato– Cladosporium fulvum (syn. Fulvia fulva ) pathosystem has served as a model for the gene-for-gene concept of effectors and resistance proteins, but this binary framework does not include the potential influence of other microbial participants. Here, we discovered a unique mechanism involved in the tripartite interaction among C. fulvum , its mycoparasitic fungus Hansfordia pulvinata , and host tomato plant.
Transcriptomic analyses of under mycoparasitic conditions in planta and in vitro revealed that in H. pulvinata genes encoding small secreted proteins were upregulated during mycoparasitism. Notably, a Nep1-like protein (HpNlp1) lacked typical necrosis-inducing activity but induced the accumulation of antifungal substances in the plant apoplast, inhibiting spore germination of C. fulvum .
In C. fulvum parasitized by H. pulvinata , effector genes were highly expressed. Strikingly, effector protein Ecp2 was found to share structural similarity with pathogen killer toxin 4 proteins and had broad-spectrum antifungal activity, indicating a dual function in fungal competition and Cf-ECP2 -mediated plant resistance.
In tomato plants, when C. fulvum was parasitized by H. pulvinata , amino acid biosynthetic pathways and defense-related genes were exclusively activated. These results suggest that in the tripartite molecular network, the mycoparasite simultaneously suppressed the pathogen and induced plant resistance. In this newly discovered multilayered molecular network, the mycoparasite coordinates pathogen suppression and plant defense within the tripartite interaction.
