Adenylate cyclase activity of TIR1/AFB auxin receptors in plants

Linlin Qi; Mateusz Kwiatkowski; Huihuang Chen; Lukas Hoermayer; Scott Sinclair; Minxia Zou; Charo del Genio; Martin Kubeš; Richard Napier; Krzysztof Jaworski; Jiří Friml

doi:10.1038/s41586-022-05369-7

Adenylate cyclase activity of TIR1/AFB auxin receptors in plants

Linlin Qi, Mateusz Kwiatkowski, Huihuang Chen, Lukas Hoermayer, Scott Sinclair, Minxia Zou, Charo del Genio, Martin Kubeš, Richard Napier, Krzysztof Jaworski, Jiří Friml

Research Centre for Fluid and Complex Systems

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Abstract

The phytohormone auxin is the major coordinative signal in plant development, 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. 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.

Original language	English
Pages (from-to)	133-138
Number of pages	6
Journal	Nature
Volume	611
Early online date	26 Oct 2022
DOIs	https://doi.org/10.1038/s41586-022-05369-7
Publication status	E-pub ahead of print - 26 Oct 2022

Bibliographical note

Funding Information:
This research was supported by the Lab Support Facility (LSF) and the Imaging and Optics Facility (IOF) of IST Austria. We thank C. Gehring for suggestions and advice; and K. U. Torii and G. Stacey for seeds and plasmids. This project was funded by a European Research Council Advanced Grant (ETAP-742985). M.F.K. and R.N. acknowledge the support of the EU MSCA-IF project CrysPINs (792329). M.K. was supported by the project POWR.03.05.00-00-Z302/17 Universitas Copernicana Thoruniensis in Futuro–IDS “Academia Copernicana”. CIDG acknowledges support from UKRI under Future Leaders Fellowship grant number MR/T020652/1.

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.

Funder

Funding Information: This research was supported by the Lab Support Facility (LSF) and the Imaging and Optics Facility (IOF) of IST Austria. We thank C. Gehring for suggestions and advice; and K. U. Torii and G. Stacey for seeds and plasmids. This project was funded by a European Research Council Advanced Grant (ETAP-742985). M.F.K. and R.N. acknowledge the support of the EU MSCA-IF project CrysPINs (792329). M.K. was supported by the project POWR.03.05.00-00-Z302/17 Universitas Copernicana Thoruniensis in Futuro–IDS “Academia Copernicana”. CIDG acknowledges support from UKRI under Future Leaders Fellowship grant number MR/T020652/1. .

Keywords

Adenylyl Cyclases - genetics - metabolism
Arabidopsis - enzymology - metabolism
Arabidopsis Proteins - genetics - metabolism
Cyclic AMP - metabolism
F-Box Proteins - genetics - metabolism
Gene Expression Regulation, Plant
Gravitropism
Indoleacetic Acids - metabolism - pharmacology
Mutation
Plant Growth Regulators - pharmacology - metabolism
Plant Roots - growth & development
Receptors, Cell Surface - genetics - metabolism
Second Messenger Systems

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title = "Adenylate cyclase activity of TIR1/AFB auxin receptors in plants",

abstract = "The phytohormone auxin is the major coordinative signal in plant development, 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. 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.",

keywords = "Adenylyl Cyclases - genetics - metabolism, Arabidopsis - enzymology - metabolism, Arabidopsis Proteins - genetics - metabolism, Cyclic AMP - metabolism, F-Box Proteins - genetics - metabolism, Gene Expression Regulation, Plant, Gravitropism, Indoleacetic Acids - metabolism - pharmacology, Mutation, Plant Growth Regulators - pharmacology - metabolism, Plant Roots - growth & development, Receptors, Cell Surface - genetics - metabolism, Second Messenger Systems",

author = "Linlin Qi and Mateusz Kwiatkowski and Huihuang Chen and Lukas Hoermayer and Scott Sinclair and Minxia Zou and {del Genio}, Charo and Martin Kube{\v s} and Richard Napier and Krzysztof Jaworski and Ji{\v r}{\'i} Friml",

note = "Funding Information: This research was supported by the Lab Support Facility (LSF) and the Imaging and Optics Facility (IOF) of IST Austria. We thank C. Gehring for suggestions and advice; and K. U. Torii and G. Stacey for seeds and plasmids. This project was funded by a European Research Council Advanced Grant (ETAP-742985). M.F.K. and R.N. acknowledge the support of the EU MSCA-IF project CrysPINs (792329). M.K. was supported by the project POWR.03.05.00-00-Z302/17 Universitas Copernicana Thoruniensis in Futuro–IDS “Academia Copernicana”. CIDG acknowledges support from UKRI under Future Leaders Fellowship grant number MR/T020652/1. Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature Limited.",

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AU - Kwiatkowski, Mateusz

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AU - Hoermayer, Lukas

AU - Sinclair, Scott

AU - Zou, Minxia

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AU - Kubeš, Martin

AU - Napier, Richard

AU - Jaworski, Krzysztof

AU - Friml, Jiří

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N2 - The phytohormone auxin is the major coordinative signal in plant development, 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. 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.

AB - The phytohormone auxin is the major coordinative signal in plant development, 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. 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.

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KW - Gene Expression Regulation, Plant

KW - Gravitropism

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KW - Mutation

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KW - Plant Roots - growth & development

KW - Receptors, Cell Surface - genetics - metabolism

KW - Second Messenger Systems

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Adenylate cyclase activity of TIR1/AFB auxin receptors in plants

Abstract

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Keywords

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