Adenylate cyclase activity of TIR1/AFB auxin receptors in plants

• Published in: Nature (London) 2022-11, Vol.611 (7934), p.133-138
• Main Authors: Qi, Linlin, Kwiatkowski, Mateusz, Chen, Huihuang, Hoermayer, Lukas, Sinclair, Scott, Zou, Minxia, del Genio, Charo I., Kubeš, Martin F., Napier, Richard, Jaworski, Krzysztof, Friml, Jiří
• Format: Article
• Language: English
• Subjects: 14/19; 38/35; 38/77; 42/34; 631/449/1659; 631/449/1741/1576; 631/449/2491/2046; 631/449/2675; 82/1; 82/16; 82/58; 82/80; 82/83; 96/44; Adenylate cyclase; Adenylyl Cyclases - genetics; Adenylyl Cyclases - metabolism; Arabidopsis - enzymology; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Auxins; Cyclic AMP; Cyclic AMP - metabolism; E coli; Enzyme kinetics; F-Box Proteins - genetics; F-Box Proteins - metabolism; Gene Expression Regulation, Plant; Gene regulation; Gravitropism; Humanities and Social Sciences; Indoleacetic Acids - metabolism; Indoleacetic Acids - pharmacology; multidisciplinary; Mutation; Plant growth; Plant Growth Regulators - metabolism; Plant Growth Regulators - pharmacology; Plant hormones; Plant Roots - growth & development; Proteins; Receptor mechanisms; Receptors; Receptors, Cell Surface - genetics; Receptors, Cell Surface - metabolism; Repressors; Science; Science (multidisciplinary); Second Messenger Systems; Signal transduction; Signaling; Transcription; Transcription factors; Ubiquitin; Ubiquitin-protein ligase
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-022-05369-7

The phytohormone auxin is the major coordinative signal in plant development 1 , mediating transcriptional reprogramming by a well-established canonical signalling pathway. TRANSPORT INHIBITOR RESPONSE 1 (TIR1)/AUXIN-SIGNALING F-BOX (AFB) auxin receptors are F-box subunits of ubiquitin ligase complexes. In response to auxin, they associate with Aux/IAA transcriptional repressors and target them for degradation via ubiquitination 2 , 3 . Here we identify adenylate cyclase (AC) activity as an additional function of TIR1/AFB receptors across land plants. Auxin, together with Aux/IAAs, stimulates cAMP production. Three separate mutations in the AC motif of the TIR1 C-terminal region, all of which abolish the AC activity, each render TIR1 ineffective in mediating gravitropism and sustained auxin-induced root growth inhibition, and also affect auxin-induced transcriptional regulation. These results highlight the importance of TIR1/AFB AC activity in canonical auxin signalling. They also identify a unique phytohormone receptor cassette combining F-box and AC motifs, and the role of cAMP as a second messenger in plants. Adenylate cyclase activity in TIR1/AFB, the canonical auxin receptor, has an essential role in auxin-mediated root growth inhibition in land plants.