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

6 Citations (Scopus)

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
Journal	Nature Communications
Volume	15
DOIs	https://doi.org/10.1038/s41467-024-48313-1
Publication status	Published - 21 May 2024

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6 Citations
1 Comment/Letter to the editor

Correction to: Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana
Huang, W. R. H., Braam, C., Kretschmer, C., Villanueva, S. L., Liu, H., Ferik, F., van der Burgh, A. M., Boeren, S., Wu, J., Zhang, L., Nürnberger, T., Wang, Y., Seidl, M. F., Evangelisti, E., Stuttmann, J. & Joosten, M. H. A. J., 10 Sept 2024, In: Nature Communications. 15, 7910.
Research output: Contribution to journal › Comment/Letter to the editor › Academic

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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, 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.",

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.}",

year = "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, 4339. https://doi.org/10.1038/s41467-024-48313-1

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T1 - Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana

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.

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.

U2 - 10.1038/s41467-024-48313-1

DO - 10.1038/s41467-024-48313-1

M3 - Article

C2 - 38773116

AN - SCOPUS:85193942902

SN - 2041-1723

VL - 15

JO - Nature Communications

JF - Nature Communications

M1 - 4339

ER -

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

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

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