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

Arsheed Hussain 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 Hussain 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

Biological, Environmental Sciences and Engineering

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

11 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 (US)
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-38103-6
State	Published - May 4 2023

Bibliographical note

KAUST Repository Item: Exported on 2023-05-08
Acknowledgements: We thank Professor Sophien Kamoun for critically reading the manuscript and for providing materials. We also thank all members of the Ntoukakis’ laboratory for fruitful discussions and helpful comments. This research was funded by the Biotechnology and Biological Science Research Council grants (BB/L019345/1) awarded to V.N. and BB/V01627X/1 awarded to M.R.G. and V.N. I.Z, A.J.P. and O.M.N. were funded by the University of Warwick through the Biotechnology and Biological Sciences Research Council, Midlands Integrative Biosciences Training Partnership (BB/M01116X/1). N.U. was funded by the University of Warwick through the Chancellors’ International Scholarship scheme. A.D.-F. was supported by the BBSRC/EPSRC funded Warwick Integrative Synthetic Biology Centre (BB/M017982/1) awarded to V.N. G.S. was supported by United States-Israel Binational Science Foundation Grants 2011069 and 2015062. M.L.G. was supported by BBSRC grants BB/H109502/1 and BB/P002145/1. M.B.M was supported by United States-Israel Binational Science Foundation Grant 2015062 and National Science Foundation Grant IOS-2026368. V. N. is also supported by the Royal Society.

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology
General Chemistry
General Physics and Astronomy

Access to Document

10.1038/s41467-023-38103-6

https://repository.kaust.edu.sa/bitstream/10754/691519/1/s41467-023-38103-6.pdf

Cite this

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). https://doi.org/10.1038/s41467-023-38103-6

@article{c93e471625ea44eb9ab99c11d39680ce,

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 Hussain} and Iosif Zacharia and Pardal, {Alonso J} and Ana Dominguez-Ferreras and Sueldo, {Daniela J} and Jung-Gun Kim and Alexi Balmuth and Gutierrez, {Jose R} and Conlan, {Brendon F} and Najeeb Ullah and Nippe, {Olivia M} and Girija, {Anil M} and Chih-Hang Wu 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 = "KAUST Repository Item: Exported on 2023-05-08 Acknowledgements: We thank Professor Sophien Kamoun for critically reading the manuscript and for providing materials. We also thank all members of the Ntoukakis{\textquoteright} laboratory for fruitful discussions and helpful comments. This research was funded by the Biotechnology and Biological Science Research Council grants (BB/L019345/1) awarded to V.N. and BB/V01627X/1 awarded to M.R.G. and V.N. I.Z, A.J.P. and O.M.N. were funded by the University of Warwick through the Biotechnology and Biological Sciences Research Council, Midlands Integrative Biosciences Training Partnership (BB/M01116X/1). N.U. was funded by the University of Warwick through the Chancellors{\textquoteright} International Scholarship scheme. A.D.-F. was supported by the BBSRC/EPSRC funded Warwick Integrative Synthetic Biology Centre (BB/M017982/1) awarded to V.N. G.S. was supported by United States-Israel Binational Science Foundation Grants 2011069 and 2015062. M.L.G. was supported by BBSRC grants BB/H109502/1 and BB/P002145/1. M.B.M was supported by United States-Israel Binational Science Foundation Grant 2015062 and National Science Foundation Grant IOS-2026368. V. N. is also supported by the Royal Society.",

year = "2023",

month = may,

day = "4",

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

language = "English (US)",

volume = "14",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

Sheikh, AH, Zacharia, I, Pardal, AJ, Dominguez-Ferreras, A, Sueldo, DJ, Kim, J-G, Balmuth, A, Gutierrez, JR, Conlan, BF, Ullah, N, Nippe, OM, Girija, AM, Wu, C-H, 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. https://doi.org/10.1038/s41467-023-38103-6

TY - JOUR

T1 - Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition.

AU - Sheikh, Arsheed Hussain

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

N1 - KAUST Repository Item: Exported on 2023-05-08 Acknowledgements: We thank Professor Sophien Kamoun for critically reading the manuscript and for providing materials. We also thank all members of the Ntoukakis’ laboratory for fruitful discussions and helpful comments. This research was funded by the Biotechnology and Biological Science Research Council grants (BB/L019345/1) awarded to V.N. and BB/V01627X/1 awarded to M.R.G. and V.N. I.Z, A.J.P. and O.M.N. were funded by the University of Warwick through the Biotechnology and Biological Sciences Research Council, Midlands Integrative Biosciences Training Partnership (BB/M01116X/1). N.U. was funded by the University of Warwick through the Chancellors’ International Scholarship scheme. A.D.-F. was supported by the BBSRC/EPSRC funded Warwick Integrative Synthetic Biology Centre (BB/M017982/1) awarded to V.N. G.S. was supported by United States-Israel Binational Science Foundation Grants 2011069 and 2015062. M.L.G. was supported by BBSRC grants BB/H109502/1 and BB/P002145/1. M.B.M was supported by United States-Israel Binational Science Foundation Grant 2015062 and National Science Foundation Grant IOS-2026368. V. N. is also supported by the Royal Society.

PY - 2023/5/4

Y1 - 2023/5/4

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.

UR - http://hdl.handle.net/10754/691519

UR - https://www.nature.com/articles/s41467-023-38103-6

U2 - 10.1038/s41467-023-38103-6

DO - 10.1038/s41467-023-38103-6

M3 - Article

C2 - 37142566

SN - 2041-1723

VL - 14

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

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

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this