The fungal volatile organic compound 6-pentyl-alpha-pyrone primes dwarf bean for enhanced drought tolerance

Abstract

Drought stress is a major constraint on crop production. While Trichoderma fungi are widely recognized for enhancing plant tolerance to abiotic stresses, the fungal molecules responsible for these protective effects remain poorly defined. In this study, we investigated the role of 6-pentyl-α-pyrone (6PP), a volatile compound produced by diverse Trichoderma spp., in modulating plant responses to water deficit. Dwarf bean (Phaseolus vulgaris) seedlings grown from seeds coated with a carrier polymer delivering 6PP were significantly more tolerant to drought stress than seedlings from seeds coated with the polymer alone (control), exhibiting increased leaf area, root length, chlorophyll content, and photosynthetic rate. To elucidate the mechanisms induced by this molecule, comparative transcriptome analyses were performed in the presence and absence of 6PP under both well-watered and drought conditions; only 49 DEGs were detected under well-watered conditions. In contrast, 476 expressed genes were identified in drought-stressed plants grown from 6PP-coated seeds, indicating substantial transcriptional reprogramming. 6PP treatment reprogrammed stress-responsive gene networks, including pathways associated with photosynthesis, carbohydrate metabolism, phosphorylation-mediated signaling, defense responses, and oxidative stress regulation. In addition, drought-stressed plants treated with 6PP exhibited enhanced MAPK phosphorylation, providing protein-level evidence for activation of phosphorylation-mediated signaling pathways associated with stress tolerance. Functional enrichment analyses further highlight secondary metabolite pathways, including those for phenylpropanoid and flavonoid biosynthesis, suggesting enhanced production of protective compounds and maintenance of photosynthetic activity under drought stress. Several stress-related genes were modulated prior to drought exposure, indicating a possible priming effect. Collectively, our findings identify 6PP as a potential signaling molecule contributing to enhanced drought resilience and provide new insights into the molecular basis of Trichoderma-mediated stress protection.