Fungal volatiles affect lateral root formation and increase plant tolerance to osmotic stress

Abstract

Symbiotic fungi communicate with plants via volatile organic compounds (VOCs), even before physical contact. While fungal VOCs are known to promote plant development under control conditions, their effects under abiotic stress remain poorly characterized. Here, we exposed Arabidopsis thaliana seedlings to VOCs from the ectomycorrhizal fungi Laccaria bicolor and Hebeloma cylindrosporum, and the endophyte Serendipita indica, under osmotic stress. Time-course transcriptional analysis revealed a rapid, transient induction of auxin transport genes within 3 days of VOC exposure, with minimal early cytokinin modulation. Using auxin-(aux1-7, axr1-3) and cytokinin-resistant (cre1, arr1-4) mutants, we show that this early response bypasses classic auxin/cytokinin antagonism, promoting lateral root proliferation by day 10 under both control and stress conditions. Transcriptomic profiling indicated that fungal VOCs modulate glucosinolate and leucine metabolism and regulate potassium (HAK5) and iron (IRT1) transporters. Genetic and phenotypic analyses of hak5-2 and akt1-2 mutants, together with nitric oxide signaling components, revealed that potassium transport and nitric oxide-dependent IRT1 regulation are essential for translating VOC perception into developmental responses. These findings underscore the multifaceted mechanisms by which fungal VOCs coordinate plant development and abiotic stress tolerance. Highlight Fungal volatile organic compounds reprogram auxin and cytokinin signaling, ion transporters, and defense metabolism to enhance root development and osmotic stress tolerance in Arabidopsis seedlings.