Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition

Arsheed H. Sheikh; Iosif Zacharia; Alonso J. Pardal; Ana Dominguez-Ferreras; Daniela J. Sueldo; Jung Gun Kim; Alexi Balmuth; Jose R. Gutierrez; Brendon F. Conlan; Najeeb Ullah; Olivia M. Nippe; Anil M. Girija; Chih Hang Wu; Guido Sessa; Alexandra M.E. Jones; Murray R. Grant; Miriam L. Gifford; Mary Beth Mudgett; John P. Rathjen; Vardis Ntoukakis

doi:10.1038/s41467-023-38103-6

Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition

Arsheed H. Sheikh, Iosif Zacharia, Alonso J. Pardal, Ana Dominguez-Ferreras, Daniela J. Sueldo, Jung Gun Kim, Alexi Balmuth, Jose R. Gutierrez, Brendon F. Conlan, Najeeb Ullah, Olivia M. Nippe, Anil M. Girija, Chih Hang Wu, Guido Sessa, Alexandra M.E. Jones, Murray R. Grant, Miriam L. Gifford, Mary Beth Mudgett, John P. Rathjen, Vardis Ntoukakis^*

^*Corresponding author for this work

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

17 Scopus citations

Abstract

In both plants and animals, nucleotide-binding leucine-rich repeat (NLR) immune receptors play critical roles in pathogen recognition and activation of innate immunity. In plants, NLRs recognise pathogen-derived effector proteins and initiate effector-triggered immunity (ETI). However, the molecular mechanisms that link NLR-mediated effector recognition and downstream signalling are not fully understood. By exploiting the well-characterised tomato Prf/Pto NLR resistance complex, we identified the 14-3-3 proteins TFT1 and TFT3 as interacting partners of both the NLR complex and the protein kinase MAPKKKα. Moreover, we identified the helper NRC proteins (NLR-required for cell death) as integral components of the Prf /Pto NLR recognition complex. Notably our studies revealed that TFTs and NRCs interact with distinct modules of the NLR complex and, following effector recognition, dissociate facilitating downstream signalling. Thus, our data provide a mechanistic link between activation of immune receptors and initiation of downstream signalling cascades.

Original language	English
Article number	2568
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-38103-6
State	Published - Dec 2023

Funding

Funders	Funder number
University of Warwick
EPSRC funded Warwick Integrative Synthetic Biology Centre
Royal Society
Biotechnology and Biological Sciences Research Council	BB/V01627X/1, BB/M017982/1, BB/L019345/1
National Science Foundation	IOS-2026368
Midlands Integrative Biosciences Training Partnership	BB/M01116X/1
United States-Israel Binational Science Foundation	BB/H109502/1, 2015062, BB/P002145/1, 2011069

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Sheikh, A. H., Zacharia, I., Pardal, A. J., Dominguez-Ferreras, A., Sueldo, D. J., Kim, J. G., Balmuth, A., Gutierrez, J. R., Conlan, B. F., Ullah, N., Nippe, O. M., Girija, A. M., Wu, C. H., Sessa, G., Jones, A. M. E., Grant, M. R., Gifford, M. L., Mudgett, M. B., Rathjen, J. P., & Ntoukakis, V. (2023). Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition. Nature Communications, 14(1), Article 2568. https://doi.org/10.1038/s41467-023-38103-6

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title = "Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition",

abstract = "In both plants and animals, nucleotide-binding leucine-rich repeat (NLR) immune receptors play critical roles in pathogen recognition and activation of innate immunity. In plants, NLRs recognise pathogen-derived effector proteins and initiate effector-triggered immunity (ETI). However, the molecular mechanisms that link NLR-mediated effector recognition and downstream signalling are not fully understood. By exploiting the well-characterised tomato Prf/Pto NLR resistance complex, we identified the 14-3-3 proteins TFT1 and TFT3 as interacting partners of both the NLR complex and the protein kinase MAPKKKα. Moreover, we identified the helper NRC proteins (NLR-required for cell death) as integral components of the Prf /Pto NLR recognition complex. Notably our studies revealed that TFTs and NRCs interact with distinct modules of the NLR complex and, following effector recognition, dissociate facilitating downstream signalling. Thus, our data provide a mechanistic link between activation of immune receptors and initiation of downstream signalling cascades.",

author = "Sheikh, \{Arsheed H.\} and Iosif Zacharia and Pardal, \{Alonso J.\} and Ana Dominguez-Ferreras and Sueldo, \{Daniela J.\} and Kim, \{Jung Gun\} and Alexi Balmuth and Gutierrez, \{Jose R.\} and Conlan, \{Brendon F.\} and Najeeb Ullah and Nippe, \{Olivia M.\} and Girija, \{Anil M.\} and Wu, \{Chih Hang\} and Guido Sessa and Jones, \{Alexandra M.E.\} and Grant, \{Murray R.\} and Gifford, \{Miriam L.\} and Mudgett, \{Mary Beth\} and Rathjen, \{John P.\} and Vardis Ntoukakis",

note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",

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doi = "10.1038/s41467-023-38103-6",

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Sheikh, AH, Zacharia, I, Pardal, AJ, Dominguez-Ferreras, A, Sueldo, DJ, Kim, JG, Balmuth, A, Gutierrez, JR, Conlan, BF, Ullah, N, Nippe, OM, Girija, AM, Wu, CH, Sessa, G, Jones, AME, Grant, MR, Gifford, ML, Mudgett, MB, Rathjen, JP & Ntoukakis, V 2023, 'Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition', Nature Communications, vol. 14, no. 1, 2568. https://doi.org/10.1038/s41467-023-38103-6

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AU - Sheikh, Arsheed H.

AU - Zacharia, Iosif

AU - Pardal, Alonso J.

AU - Dominguez-Ferreras, Ana

AU - Sueldo, Daniela J.

AU - Kim, Jung Gun

AU - Balmuth, Alexi

AU - Gutierrez, Jose R.

AU - Conlan, Brendon F.

AU - Ullah, Najeeb

AU - Nippe, Olivia M.

AU - Girija, Anil M.

AU - Wu, Chih Hang

AU - Sessa, Guido

AU - Jones, Alexandra M.E.

AU - Grant, Murray R.

AU - Gifford, Miriam L.

AU - Mudgett, Mary Beth

AU - Rathjen, John P.

AU - Ntoukakis, Vardis

PY - 2023/12

Y1 - 2023/12

N2 - In both plants and animals, nucleotide-binding leucine-rich repeat (NLR) immune receptors play critical roles in pathogen recognition and activation of innate immunity. In plants, NLRs recognise pathogen-derived effector proteins and initiate effector-triggered immunity (ETI). However, the molecular mechanisms that link NLR-mediated effector recognition and downstream signalling are not fully understood. By exploiting the well-characterised tomato Prf/Pto NLR resistance complex, we identified the 14-3-3 proteins TFT1 and TFT3 as interacting partners of both the NLR complex and the protein kinase MAPKKKα. Moreover, we identified the helper NRC proteins (NLR-required for cell death) as integral components of the Prf /Pto NLR recognition complex. Notably our studies revealed that TFTs and NRCs interact with distinct modules of the NLR complex and, following effector recognition, dissociate facilitating downstream signalling. Thus, our data provide a mechanistic link between activation of immune receptors and initiation of downstream signalling cascades.

AB - In both plants and animals, nucleotide-binding leucine-rich repeat (NLR) immune receptors play critical roles in pathogen recognition and activation of innate immunity. In plants, NLRs recognise pathogen-derived effector proteins and initiate effector-triggered immunity (ETI). However, the molecular mechanisms that link NLR-mediated effector recognition and downstream signalling are not fully understood. By exploiting the well-characterised tomato Prf/Pto NLR resistance complex, we identified the 14-3-3 proteins TFT1 and TFT3 as interacting partners of both the NLR complex and the protein kinase MAPKKKα. Moreover, we identified the helper NRC proteins (NLR-required for cell death) as integral components of the Prf /Pto NLR recognition complex. Notably our studies revealed that TFTs and NRCs interact with distinct modules of the NLR complex and, following effector recognition, dissociate facilitating downstream signalling. Thus, our data provide a mechanistic link between activation of immune receptors and initiation of downstream signalling cascades.

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Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition

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