Brassinosteriod is a plant hormone which controls plant growth and development and in Arabidopsis is perceived by the single membrane spaning leucine-rich repeat receptor kinase BRASSINOSTERIOD RECEPTOR (BRI1). The kinase domain of BRI1 is within the cytoplasmic region and encapsulates a guanylate cyclase (GC) catalytic centre. We investigated the intramolecular regulation of this domain architecture. Using mutational studies in the kinase domain and guanylate cyclase centres we show that kinase active proteins are essential to generate cGMP. cGMP in turn down regulates BRI1 kinase activity. cGMP also potentiates phosphorylation of downstream substrates in Arabidopsis root cell cultures. Hence we show that cGMP modulates the brassinosteroid response by enhancing downstream signalling while at the same time dampening the signal generated by the receptor.