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Rhizosphere microorganisms interact with plant roots by producing chemical signals that regulate root development. However, the distinct bioactive compounds and signal transduction pathways remain to be identified. Here, we showed that sesquiterpenes are the main volatile compounds produced by plant‐beneficial Trichoderma guizhouense NJAU4742. Inhibition of sesquiterpene biosynthesis eliminated the promoting effect of this strain on root growth, indicating its involvement in plant‐fungus cross‐kingdom signalling. Sesquiterpene component analysis identified cedrene, a highly abundant sesquiterpene in strain NJAU4742, to stimulate plant growth and root development. Genetic analysis and auxin transport inhibition showed that the TIR1 and AFB2 auxin receptors, IAA14 auxin‐responsive protein, and ARF7 and ARF19 transcription factors affected the response of lateral roots to cedrene. Moreover, the AUX1 auxin influx carrier and PIN2 efflux carrier were also found to be indispensable for cedrene‐induced lateral root formation. Confocal imaging showed that cedrene affected the expression of pPIN2:PIN2:GFP and pPIN3:PIN3:GFP, which might be related to the effect of cedrene on root morphology. These results suggested that a novel sesquiterpene molecule from plant‐beneficial T. guizhouense regulates plant root development through the transport and signalling of auxin. Summary Statement: From the volatile compounds produced by a plant beneficial fungus, we identified a novel component cedrene that can promote plant root development. We revealed the role of auxin signalling and transport in the process of cedrene‐promoted root development. This study complements the lack of identification of distinct bioactive compounds from microbial sources and provides a helpful tool to study and decipher the underlying cellular and molecular reactions and mechanism occurring in microbe‐plant interactions. [ABSTRACT FROM AUTHOR]

Lateral root formation is coordinated by both endogenous and external factors. As biotic factors, plant growth‐promoting rhizobacteria can affect lateral root formation, while the regulation mechanism is unclear. In this study, by applying various marker lines, we found that volatile compounds (VCs) from Bacillus amyloliquefaciens SQR9 induced higher frequency of DR5 oscillation and prebranch site formation, accelerated the development and emergence of the lateral root primordia and thus promoted lateral root development in Arabidopsis. We demonstrated a critical role of auxin on B. amyloliquefaciens VCs‐induced lateral root formation via respective mutants and pharmacological experiments. Our results showed that auxin biosynthesis, polar transport and signalling pathway are involved in B. amyloliquefaciens VCs‐induced lateral roots formation. We further showed that acetoin, a major component of B. amyloliquefaciens VCs, is less active in promoting root development compared to VC blends from B. amyloliquefaciens, indicating the presence of yet uncharacterized/unknown VCs might contribute to B. amyloliquefaciens effect on lateral root formation. In summary, our study revealed an auxin‐dependent mechanism of B. amyloliquefaciens VCs in regulating lateral root branching in a non‐contact manner, and further efforts will explore useful VCs to promote plant root development. The volatile compounds from Bacillus spp. increase the frequency of prebranch site formation and further accelerated the emergence of lateral root primordia (LRP) from the primary root (PR) in Arabidopsis, resulting in a denser lateral root (LR) along the PR spatially. This process is dependent on auxin signaling pathway; fully functional machinery of YUCs‐mediated auxin biosynthesis and polar auxin transport are also required. [ABSTRACT FROM AUTHOR]