The brassinosteroid receptor BRI1 can generate cGMP enabling cGMP‐dependent downstream signaling

Summary The brassinosteroid receptor brassinosteroid insensitive 1 (BRI1) is a member of the leucine‐rich repeat receptor‐like kinase family. The intracellular kinase domain of BRI1 is an active kinase and also encapsulates a guanylate cyclase catalytic centre. Using liquid chromatography tandem mass spectrometry, we confirmed that the recombinant cytoplasmic domain of BRI1 generates pmol amounts of cGMP per μg protein with a preference for magnesium over manganese as a co‐factor. Importantly, a functional BRI1 kinase is essential for optimal cGMP generation. Therefore, the guanylate cyclase activity of BRI1 is modulated by the kinase while cGMP, the product of the guanylate cyclase, in turn inhibits BRI1 kinase activity. Furthermore, we show using Arabidopsis root cell cultures that cGMP rapidly potentiates phosphorylation of the downstream substrate brassinosteroid signaling kinase 1 (BSK1). Taken together, our results suggest that cGMP acts as a modulator that enhances downstream signaling while dampening signal generation from the receptor. Significance Statement The cytosolic part of the brassinosteroid receptor (BRI1) contains a kinase domain that encapsulates a guanylate cyclase (GC) catalytic centre whose activity is modulated by the kinase while cGMP in turn inhibits BRI1 kinase activity and potentiates phosphorylation of downstream substrates. We propose that cGMP modulates the brassinosteroid response by enhancing downstream signaling while at the same time dampening the signal generated by the receptor.