Reactive oxygen species and reactive carbonyl species constitute a feed‐forward loop in auxin signaling for lateral root formation

Summary In auxin‐stimulated roots, production of reactive oxygen species (ROS) via the hormone‐induced activation of respiratory burst oxidase homologous NADPH oxidases facilitates lateral root (LR) formation. In this study, in order to verify that ROS can modulate auxin signaling, we examined the involvement of the lipid peroxide‐derived agents known as reactive carbonyl species (RCS) in LR formation. When auxin was added to Arabidopsis thaliana roots, the levels of RCS, for example acrolein, 4‐hydroxynonenal and crotonaldehyde, were increased prior to LR formation. Addition of the carbonyl scavenger carnosine suppressed auxin‐induced LR formation. Addition of RCS to the roots induced the expression of the auxin‐responsive DR5 promoter and the TIR1, IAA14, ARF7, LBD16 and PUCHI genes and facilitated LR formation without increasing the endogenous auxin level. DR5 and LBD16 were activated in the LR primordia. The auxin signaling‐deficient mutants arf7 arf19 and slr‐1 did not respond – and tir1 afb2 appeared to show a poor response – to RCS. When given to the roots RCS promoted the disappearance of the AXR3NT–GUS fusion protein, i.e. the degradation of the auxin/indole‐3‐acetic acid protein, as did auxin. These results indicate that the auxin‐induced production of ROS and their downstream products RCS modulate the auxin signaling pathway in a feed‐forward manner. RCS are key agents that connect the ROS signaling and the auxin signaling pathways. Significance Statement Auxin induces the formation of reactive oxygen species (ROS), which promote lateral root (LR) formation. We show that ROS and lipid peroxide‐derived reactive carbonyl species (RCS), signal mediators downstream of ROS, facilitate the degradation of the auxin/indole‐3‐acetic acid repressor, and thereby enforce the auxin signal for LR formation. Specifically, ROS and RCS constitute a feed‐forward pathway to modulate the auxin signaling for LR formation. The RCS provide a connection between the ROS signal and auxin signaling pathways.