Guanylate cyclase activity of TIR1/AFB auxin receptors mediates rapid auxin responses

Abstract

The plant hormone auxin is perceived by TIR1/AFB receptors, which mediate transcriptional reprogramming via a ubiquitination- and cAMP-dependent mechanism. Same receptors mediate also rapid, non-transcriptional growth responses that are mechanistically less well understood. Here, we demonstrate that TIR1/AFB receptors possess not only adenylate cyclase but also guanylate cyclase activity. Auxin perception independently activates cAMP and cGMP production by TIR1/AFBs in vitro and elevates both cAMP and cGMP levels in planta. Genetic and synthetic biology approaches revealed that AFB1 guanylate cyclase activity is required for the rapid cytosolic Ca2+ transients and root growth inhibition. This unprecedented combination of adenylate and guanylate cyclase activities within a single hormone receptor establishes a new paradigm for how one perception mechanism can mediate distinct downstream responses. One-Sentence SummaryTIR1/AFB auxin receptors possess both, adenylate and guanylate cyclase activities, mediating transcriptional reprogramming and rapid Ca2+-dependent growth responses, respectively.