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

The major developmental signal in plants, auxin is perceived by TIR1/AFB receptors. It triggers transcriptional reprogramming via well-established canonical mechanism but also elusive rapid, non-transcriptional responses. Here we demonstrate that TIR1/AFB receptors have, next to recently identified adenylate cyclase, also guanylate cyclase activity. Auxin perception activates independently the cAMP and cGMP production by TIR1/AFBs in vitro and increases cAMP and cGMP levels in planta with a slow and fast dynamics, respectively. Exogenous cGMP but not cAMP application induces rapid cytosolic Ca 2+ transients and root growth inhibition, suggesting that TIR1/AFB-derived cGMP mediates rapid auxin responses. This unprecedented combination of adenylate and guanylate cyclase activities in a hormone receptor provides a new paradigm for how a single perception mechanism can mediate a multitude of diverse downstream responses. One-Sentence Summary TIR1/AFB auxin receptors have guanylate cyclase activity, whose product, cGMP mediates rapid non-transcriptional auxin responses.