Streptomyces Volatiles Alter Auxin/Cytokinin Signaling, Root Architecture, and Growth Rate in Arabidopsis thaliana via Signaling Through the KISS ME DEADLY Gene Family

Microbial volatile metabolites can enhance plant growth, yet the mechanisms by which plants perceive and transduce these signals are unknown. Growth of Arabidopsis thaliana Col-0 seedlings was found to be stimulated by volatiles from the soil bacterium Streptomyces coelicolor. To investigate volatile-responding candidate signaling molecules and genes, cultivation of seedlings in gas-phase contact with S. coelicolor genotypes was combined with GC-MS and plant transcriptomics. Components potentially involved were further studied using pure compounds and A. thaliana T-DNA mutants. Application of volatiles from S. coelicolor enhanced the growth of A. thaliana seedlings primarily by stimulating lateral root growth rate and inhibiting primary root extension. Concurrently, a family-wide induction of the Kelch-repeat F-box gene family KISS ME DEADLY (KMD) was observed. A. thaliana genotypes with a loss of function for the KMD family or other alterations of auxin/cytokinin signaling homeostasis suppressed the root response to both S. coelicolor total volatiles and the common microbial volatile 3-octanone. The results reveal a novel function of KMDs in mediating plant growth stimulation in response to volatile stimulation that alters auxin/cytokinin signaling and emphasize rhizospheric microbials as potential indicators of soil status to plants.