The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ETHYLENE INSENSITIVE 2 functioning

Plants interact with root microbes via chemical signaling, which modulates competence or symbiosis. Although several volatile organic compounds (VOCs) from fungi may affect plant growth and development, the signal transduction pathways mediating VOC sensing are not fully understood. 6-pentyl-2H-pyran-2-one (6-PP) is a major VOC biosynthesized by Trichoderma spp. which is probably involved in plant-fungus cross-kingdom signaling. Using microscopy and confocal imaging, the effects of 6-PP on root morphogenesis were found to be correlated with DR5:GFP, DR5:VENUS, H2B::GFP, PIN1::PIN1::GFP, PIN2::PIN2::GFP, PIN3::PIN3::GFP and PIN7::PIN7::GFP gene expression. A genetic screen for primary root growth resistance to 6-PP in wild-type seedlings and auxin- and ethylene-related mutants allowed identification of genes controlling root architectural responses to this metabolite. Trichoderma atroviride produced 6-PP, which promoted plant growth and regulated root architecture, inhibiting primary root growth and inducing lateral root formation. 6-PP modulated expression of PIN auxin-transport proteins in a specific and dose-dependent manner in primary roots. TIR1, AFB2 and AFB3 auxin receptors and ARF7 and ARF19 transcription factors influenced the lateral root response to 6-PP, whereas EIN2 modulated 6-PP sensing in primary roots. These results indicate that root responses to 6-PP involve components of auxin transport and signaling and the ethylene-response modulator EIN2.