IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38103-6.html
   My bibliography  Save this article

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

Author

Listed:
  • Arsheed H. Sheikh

    (University of Warwick
    King Abdullah University of Science and Technology)

  • Iosif Zacharia

    (University of Warwick)

  • Alonso J. Pardal

    (University of Warwick)

  • Ana Dominguez-Ferreras

    (University of Warwick)

  • Daniela J. Sueldo

    (University of Warwick
    Norwegian University of Science and Technology)

  • Jung-Gun Kim

    (Stanford University)

  • Alexi Balmuth

    (J.R. Simplot Company
    Norwich Research Park)

  • Jose R. Gutierrez

    (Norwich Research Park)

  • Brendon F. Conlan

    (The Australian National University)

  • Najeeb Ullah

    (University of Warwick)

  • Olivia M. Nippe

    (University of Warwick)

  • Anil M. Girija

    (Tel-Aviv University)

  • Chih-Hang Wu

    (Norwich Research Park)

  • Guido Sessa

    (Tel-Aviv University)

  • Alexandra M. E. Jones

    (University of Warwick)

  • Murray R. Grant

    (University of Warwick)

  • Miriam L. Gifford

    (University of Warwick
    University of Warwick)

  • Mary Beth Mudgett

    (Stanford University)

  • John P. Rathjen

    (The Australian National University)

  • Vardis Ntoukakis

    (University of Warwick
    University of Warwick)

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.

Suggested Citation

  • 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. Nip, 2023. "Dynamic changes of the Prf/Pto tomato resistance complex following effector recognition," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38103-6
    DOI: 10.1038/s41467-023-38103-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38103-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38103-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Simon B. Saucet & Yan Ma & Panagiotis F. Sarris & Oliver J. Furzer & Kee Hoon Sohn & Jonathan D.G. Jones, 2015. "Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4," Nature Communications, Nature, vol. 6(1), pages 1-12, May.
    2. Smyth Gordon K, 2004. "Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 3(1), pages 1-28, February.
    3. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Fabien Lonjon & Yan Lai & Nasrin Askari & Niharikaa Aiyar & Cedoljub Bundalovic-Torma & Bradley Laflamme & Pauline W. Wang & Darrell Desveaux & David S. Guttman, 2024. "The effector-triggered immunity landscape of tomato against Pseudomonas syringae," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Deepak D. Bhandari & Dae Kwan Ko & Sang-Jin Kim & Kinya Nomura & Sheng Yang He & Federica Brandizzi, 2023. "Defense against phytopathogens relies on efficient antimicrobial protein secretion mediated by the microtubule-binding protein TGNap1," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Aaron C Ericsson & J Wade Davis & William Spollen & Nathan Bivens & Scott Givan & Catherine E Hagan & Mark McIntosh & Craig L Franklin, 2015. "Effects of Vendor and Genetic Background on the Composition of the Fecal Microbiota of Inbred Mice," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-19, February.
    3. Hossain, Ahmed & Beyene, Joseph & Willan, Andrew R. & Hu, Pingzhao, 2009. "A flexible approximate likelihood ratio test for detecting differential expression in microarray data," Computational Statistics & Data Analysis, Elsevier, vol. 53(10), pages 3685-3695, August.
    4. Xiaohong Li & Guy N Brock & Eric C Rouchka & Nigel G F Cooper & Dongfeng Wu & Timothy E O’Toole & Ryan S Gill & Abdallah M Eteleeb & Liz O’Brien & Shesh N Rai, 2017. "A comparison of per sample global scaling and per gene normalization methods for differential expression analysis of RNA-seq data," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-22, May.
    5. Paul Vincelli, 2016. "Genetic Engineering and Sustainable Crop Disease Management: Opportunities for Case-by-Case Decision-Making," Sustainability, MDPI, vol. 8(5), pages 1-22, May.
    6. Ambroise Jérôme & Bearzatto Bertrand & Robert Annie & Macq Benoit & Gala Jean-Luc, 2012. "Combining Multiple Laser Scans of Spotted Microarrays by Means of a Two-Way ANOVA Model," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 11(3), pages 1-20, February.
    7. J. McClatchy & R. Strogantsev & E. Wolfe & H. Y. Lin & M. Mohammadhosseini & B. A. Davis & C. Eden & D. Goldman & W. H. Fleming & P. Conley & G. Wu & L. Cimmino & H. Mohammed & A. Agarwal, 2023. "Clonal hematopoiesis related TET2 loss-of-function impedes IL1β-mediated epigenetic reprogramming in hematopoietic stem and progenitor cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Alexandra Gyurdieva & Stefan Zajic & Ya-Fang Chang & E. Andres Houseman & Shan Zhong & Jaegil Kim & Michael Nathenson & Thomas Faitg & Mary Woessner & David C. Turner & Aisha N. Hasan & John Glod & Ro, 2022. "Biomarker correlates with response to NY-ESO-1 TCR T cells in patients with synovial sarcoma," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    9. Yu Lianbo & Gulati Parul & Fernandez Soledad & Pennell Michael & Kirschner Lawrence & Jarjoura David, 2011. "Fully Moderated T-statistic for Small Sample Size Gene Expression Arrays," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 10(1), pages 1-22, September.
    10. Sinan Xiong & Jianbiao Zhou & Tze King Tan & Tae-Hoon Chung & Tuan Zea Tan & Sabrina Hui-Min Toh & Nicole Xin Ning Tang & Yunlu Jia & Yi Xiang See & Melissa Jane Fullwood & Takaomi Sanda & Wee-Joo Chn, 2024. "Super enhancer acquisition drives expression of oncogenic PPP1R15B that regulates protein homeostasis in multiple myeloma," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    11. Chaofeng Yuan & Wensheng Zhu & Xuming He & Jianhua Guo, 2019. "A mixture factor model with applications to microarray data," TEST: An Official Journal of the Spanish Society of Statistics and Operations Research, Springer;Sociedad de Estadística e Investigación Operativa, vol. 28(1), pages 60-76, March.
    12. Nott, David J. & Yu, Zeming & Chan, Eva & Cotsapas, Chris & Cowley, Mark J. & Pulvers, Jeremy & Williams, Rohan & Little, Peter, 2007. "Hierarchical Bayes variable selection and microarray experiments," Journal of Multivariate Analysis, Elsevier, vol. 98(4), pages 852-872, April.
    13. Rongrong Zhang & Yu Wu & Xiangru Qu & Wenjuan Yang & Qin Wu & Lin Huang & Qiantao Jiang & Jian Ma & Yazhou Zhang & Pengfei Qi & Guoyue Chen & Yunfeng Jiang & Youliang Zheng & Xiaojie Wang & Yuming Wei, 2024. "The RING-finger ubiquitin E3 ligase TaPIR1 targets TaHRP1 for degradation to suppress chloroplast function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    14. Alexander Kaever & Manuel Landesfeind & Kirstin Feussner & Burkhard Morgenstern & Ivo Feussner & Peter Meinicke, 2014. "Meta-Analysis of Pathway Enrichment: Combining Independent and Dependent Omics Data Sets," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-12, February.
    15. Farhan Ali & Qingchun Pan & Genshen Chen & Kashif Rafiq Zahid & Jianbing Yan, 2013. "Evidence of Multiple Disease Resistance (MDR) and Implication of Meta-Analysis in Marker Assisted Selection," PLOS ONE, Public Library of Science, vol. 8(7), pages 1-12, July.
    16. Iqbal Mahmud & Guimei Tian & Jia Wang & Tarun E. Hutchinson & Brandon J. Kim & Nikee Awasthee & Seth Hale & Chengcheng Meng & Allison Moore & Liming Zhao & Jessica E. Lewis & Aaron Waddell & Shangtao , 2023. "DAXX drives de novo lipogenesis and contributes to tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    17. Erminia Donnarumma & Michael Kohlhaas & Elodie Vimont & Etienne Kornobis & Thibault Chaze & Quentin Giai Gianetto & Mariette Matondo & Maryse Moya-Nilges & Christoph Maack & Timothy Wai, 2022. "Mitochondrial Fission Process 1 controls inner membrane integrity and protects against heart failure," Nature Communications, Nature, vol. 13(1), pages 1-24, December.
    18. Soohyun Oh & Myung-Shin Kim & Hui Jeong Kang & Taewon Kim & Junhyeong Kong & Doil Choi, 2024. "Conserved effector families render Phytophthora species vulnerable to recognition by NLR receptors in nonhost plants," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    19. J. T. Gene Hwang & Jing Qiu & Zhigen Zhao, 2009. "Empirical Bayes confidence intervals shrinking both means and variances," Journal of the Royal Statistical Society Series B, Royal Statistical Society, vol. 71(1), pages 265-285, January.
    20. Karine de Guillen & Diana Ortiz-Vallejo & Jérome Gracy & Elisabeth Fournier & Thomas Kroj & André Padilla, 2015. "Structure Analysis Uncovers a Highly Diverse but Structurally Conserved Effector Family in Phytopathogenic Fungi," PLOS Pathogens, Public Library of Science, vol. 11(10), pages 1-27, October.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38103-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.