Plant growth promotion mediated by volatile organic compounds during the <i>Gongronella butleri</i> –plant interaction

Early-diverging Mucoromycotina fungi are widely recognized for promoting plant growth and development. However, the specific volatile organic compounds (VOCs) involved and their underlying mechanisms remain largely unknown. In this study, we used a non-contact co-culture system to investigate the effects of VOCs emitted during the interaction between the beneficial fungus Gongronella butleri w5 (w5) and plants. Using solid-phase microextraction gas chromatography-mass spectrometry, we identified 1H-indole-4-carboxaldehyde (4-IC) and 4-methylbenzyl alcohol (4-MB) as the predominant VOCs detected in the w5-plant co-culture headspace. These interaction-associated volatiles were found to promote lateral root development in a dose-dependent and synergistic manner. Mechanistically, physiological assays using hormone signaling mutants (ETR1, COI1, CRE1), combined with transcriptomic and metabolomic profiling, revealed that 4-IC and 4-MB enhance the biosynthesis of ethylene, jasmonic acid, and trans-zeatin. Changes in hormone levels subsequently regulate plant signaling pathways, directing root morphogenesis. This study demonstrates that early-diverging Mucoromycotina fungi can promote plant growth through aromatic VOCs detected during fungal-plant interactions, highlighting their potential ecological roles in plant-microbe interactions and offering new insights into the chemical basis of fungal-mediated plant growth promotion.