Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana

Wen R H Huang; Ciska Braam; Carola Kretschmer; Sergio Landeo Villanueva; Huan Liu; Filiz Ferik; Aranka M van der Burgh; Jinbin Wu; Lisha Zhang; Thorsten Nürnberger; Yulu Wang; Michael F Seidl; Edouard Evangelisti; Johannes Stuttmann; Matthieu H A J Joosten

doi:10.1038/s41467-024-48313-1

Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana

Wen R H Huang^*, Ciska Braam, Carola Kretschmer, Sergio Landeo Villanueva, Huan Liu, Filiz Ferik, Aranka M van der Burgh, Jinbin Wu, Lisha Zhang, Thorsten Nürnberger, Yulu Wang, Michael F Seidl, Edouard Evangelisti, Johannes Stuttmann, Matthieu H A J Joosten^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Cell-surface receptors form the front line of plant immunity. The leucine-rich repeat (LRR)-receptor-like kinases SOBIR1 and BAK1 are required for the functionality of the tomato LRR-receptor-like protein Cf-4, which detects the secreted effector Avr4 of the pathogenic fungus Fulvia fulva. Here, we show that the kinase domains of SOBIR1 and BAK1 directly phosphorylate each other and that residues Thr522 and Tyr469 of the kinase domain of Nicotiana benthamiana SOBIR1 are required for its kinase activity and for interacting with signalling partners, respectively. By knocking out multiple genes belonging to different receptor-like cytoplasmic kinase (RLCK)-VII subfamilies in N. benthamiana:Cf-4, we show that members of RLCK-VII-6, -7, and -8 differentially regulate the Avr4/Cf-4-triggered biphasic burst of reactive oxygen species. In addition, members of RLCK-VII-7 play an essential role in resistance against the oomycete pathogen Phytophthora palmivora. Our study provides molecular evidence for the specific roles of RLCKs downstream of SOBIR1/BAK1-containing immune complexes.

Original language	English
Article number	4339
Pages (from-to)	1-18
Number of pages	18
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-48313-1
Publication status	Published - 21 May 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

Funding

The authors thank Bert Essenstam from Unifarm for excellent plant care. Laurens Deurhof and Gabriel Lorencini Fiorin are acknowledged for technical assistance. We thank Xiaoqian Shi-Kunne for her help with retrieving the protein sequences of the SOBIR1 homologues from different plant species. We thank Jim Renema, Max Pluis, Agnes Omabour Hagan and Amber van Loosbroek for their help with performing some of the experiments. W.R.H. Huang is supported by the China Scholarship Council (CSC) (201706990001). S.L.V. is supported by the Peruvian Council for Science, Technology and Technological Innovation (CONCYTEC) and its executive unit FONDECYT (119-2017-FONDECYT).

Funders	Funder number
Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica
Peruvian Council for Science, Technology and Technological Innovation
China Scholarship Council	201706990001
China Scholarship Council
Fondo Nacional de Desarrollo Científico y Tecnológico	119-2017-FONDECYT
Fondo Nacional de Desarrollo Científico y Tecnológico

Keywords

Gene Expression Regulation, Plant
Nicotiana/immunology
Phosphorylation
Phytophthora/pathogenicity
Plant Diseases/microbiology
Plant Immunity/genetics
Plant Proteins/metabolism
Protein Kinases/metabolism
Protein Serine-Threonine Kinases/metabolism
Reactive Oxygen Species/metabolism
Signal Transduction

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s41467-024-48313-1Final published version, 2.17 MBLicence: CC BY

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Huang, W. R. H., Braam, C., Kretschmer, C., Villanueva, S. L., Liu, H., Ferik, F., van der Burgh, A. M., Wu, J., Zhang, L., Nürnberger, T., Wang, Y., Seidl, M. F., Evangelisti, E., Stuttmann, J., & Joosten, M. H. A. J. (2024). Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana. Nature Communications, 15(1), 1-18. Article 4339. https://doi.org/10.1038/s41467-024-48313-1

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title = "Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana",

abstract = "Cell-surface receptors form the front line of plant immunity. The leucine-rich repeat (LRR)-receptor-like kinases SOBIR1 and BAK1 are required for the functionality of the tomato LRR-receptor-like protein Cf-4, which detects the secreted effector Avr4 of the pathogenic fungus Fulvia fulva. Here, we show that the kinase domains of SOBIR1 and BAK1 directly phosphorylate each other and that residues Thr522 and Tyr469 of the kinase domain of Nicotiana benthamiana SOBIR1 are required for its kinase activity and for interacting with signalling partners, respectively. By knocking out multiple genes belonging to different receptor-like cytoplasmic kinase (RLCK)-VII subfamilies in N. benthamiana:Cf-4, we show that members of RLCK-VII-6, -7, and -8 differentially regulate the Avr4/Cf-4-triggered biphasic burst of reactive oxygen species. In addition, members of RLCK-VII-7 play an essential role in resistance against the oomycete pathogen Phytophthora palmivora. Our study provides molecular evidence for the specific roles of RLCKs downstream of SOBIR1/BAK1-containing immune complexes.",

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author = "Huang, {Wen R H} and Ciska Braam and Carola Kretschmer and Villanueva, {Sergio Landeo} and Huan Liu and Filiz Ferik and {van der Burgh}, {Aranka M} and Jinbin Wu and Lisha Zhang and Thorsten N{\"u}rnberger and Yulu Wang and Seidl, {Michael F} and Edouard Evangelisti and Johannes Stuttmann and Joosten, {Matthieu H A J}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

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Huang, WRH, Braam, C, Kretschmer, C, Villanueva, SL, Liu, H, Ferik, F, van der Burgh, AM, Wu, J, Zhang, L, Nürnberger, T, Wang, Y, Seidl, MF, Evangelisti, E, Stuttmann, J & Joosten, MHAJ 2024, 'Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana', Nature Communications, vol. 15, no. 1, 4339, pp. 1-18. https://doi.org/10.1038/s41467-024-48313-1

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AU - Huang, Wen R H

AU - Braam, Ciska

AU - Kretschmer, Carola

AU - Villanueva, Sergio Landeo

AU - Liu, Huan

AU - Ferik, Filiz

AU - van der Burgh, Aranka M

AU - Wu, Jinbin

AU - Zhang, Lisha

AU - Nürnberger, Thorsten

AU - Wang, Yulu

AU - Seidl, Michael F

AU - Evangelisti, Edouard

AU - Stuttmann, Johannes

AU - Joosten, Matthieu H A J

N1 - Publisher Copyright: © The Author(s) 2024.

PY - 2024/5/21

Y1 - 2024/5/21

N2 - Cell-surface receptors form the front line of plant immunity. The leucine-rich repeat (LRR)-receptor-like kinases SOBIR1 and BAK1 are required for the functionality of the tomato LRR-receptor-like protein Cf-4, which detects the secreted effector Avr4 of the pathogenic fungus Fulvia fulva. Here, we show that the kinase domains of SOBIR1 and BAK1 directly phosphorylate each other and that residues Thr522 and Tyr469 of the kinase domain of Nicotiana benthamiana SOBIR1 are required for its kinase activity and for interacting with signalling partners, respectively. By knocking out multiple genes belonging to different receptor-like cytoplasmic kinase (RLCK)-VII subfamilies in N. benthamiana:Cf-4, we show that members of RLCK-VII-6, -7, and -8 differentially regulate the Avr4/Cf-4-triggered biphasic burst of reactive oxygen species. In addition, members of RLCK-VII-7 play an essential role in resistance against the oomycete pathogen Phytophthora palmivora. Our study provides molecular evidence for the specific roles of RLCKs downstream of SOBIR1/BAK1-containing immune complexes.

AB - Cell-surface receptors form the front line of plant immunity. The leucine-rich repeat (LRR)-receptor-like kinases SOBIR1 and BAK1 are required for the functionality of the tomato LRR-receptor-like protein Cf-4, which detects the secreted effector Avr4 of the pathogenic fungus Fulvia fulva. Here, we show that the kinase domains of SOBIR1 and BAK1 directly phosphorylate each other and that residues Thr522 and Tyr469 of the kinase domain of Nicotiana benthamiana SOBIR1 are required for its kinase activity and for interacting with signalling partners, respectively. By knocking out multiple genes belonging to different receptor-like cytoplasmic kinase (RLCK)-VII subfamilies in N. benthamiana:Cf-4, we show that members of RLCK-VII-6, -7, and -8 differentially regulate the Avr4/Cf-4-triggered biphasic burst of reactive oxygen species. In addition, members of RLCK-VII-7 play an essential role in resistance against the oomycete pathogen Phytophthora palmivora. Our study provides molecular evidence for the specific roles of RLCKs downstream of SOBIR1/BAK1-containing immune complexes.

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KW - Phosphorylation

KW - Phytophthora/pathogenicity

KW - Plant Diseases/microbiology

KW - Plant Immunity/genetics

KW - Plant Proteins/metabolism

KW - Protein Kinases/metabolism

KW - Protein Serine-Threonine Kinases/metabolism

KW - Reactive Oxygen Species/metabolism

KW - Signal Transduction

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ER -

Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana

Abstract

Bibliographical note

Funding

Keywords

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Correction to: Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana (Nature Communications, (2024), 15, 1, (4339), 10.1038/s41467-024-48313-1)

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