Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1

Oliver Johanndrees; Erin L Baggs; Charles Uhlmann; Federica Locci; Henriette L Läßle; Katharina Melkonian; Kiara Käufer; Joram A Dongus; Hirofumi Nakagami; Ksenia V Krasileva; Jane E Parker; Dmitry Lapin

doi:10.1093/plphys/kiac480

Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1

Oliver Johanndrees, Erin L Baggs, Charles Uhlmann, Federica Locci, Henriette L Läßle, Katharina Melkonian, Kiara Käufer, Joram A Dongus, Hirofumi Nakagami, Ksenia V Krasileva, Jane E Parker, Dmitry Lapin

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

Abstract

Toll/Interleukin-1 receptor (TIR) domains are integral to immune systems across all kingdoms. In plants, TIRs are present in nucleotide-binding leucine-rich repeat (NLR) immune receptors, NLR-like, and TIR-only proteins. Although TIR-NLR and TIR signaling in plants require the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) protein family, TIRs persist in species that have no EDS1 members. To assess whether particular TIR groups evolved with EDS1, we searched for TIR-EDS1 co-occurrence patterns. Using a large-scale phylogenetic analysis of TIR domains from 39 algal and land plant species, we identified 4 TIR families that are shared by several plant orders. One group occurred in TIR-NLRs of eudicots and another in TIR-NLRs across eudicots and magnoliids. Two further groups were more widespread. A conserved TIR-only group co-occurred with EDS1 and members of this group elicit EDS1-dependent cell death. In contrast, a maize (Zea mays) representative of TIR proteins with tetratricopeptide repeats was also present in species without EDS1 and induced EDS1-independent cell death. Our data provide a phylogeny-based plant TIR classification and identify TIRs that appear to have evolved with and are dependent on EDS1, while others have EDS1-independent activity.

Original language	English
Pages (from-to)	626-642
Number of pages	17
Journal	Plant Physiology
Volume	191
Issue number	1
Early online date	13 Oct 2022
DOIs	https://doi.org/10.1093/plphys/kiac480
Publication status	Published - Jan 2023

Bibliographical note

Publisher Copyright:
VC The Author(s) 2022.

Funding

We thank Jonathan Jones (Sainsbury Laboratory, Norwich UK) for sharing N. tabacum RNAi:EDS1 seeds. We also thank Artem Pankin (formerly MPIPZ) for advice on phylogenetic analyses and the Earlham Institute Scientific Computing group alongside the Norwich BioScience Institutes Partnership Computing infrastructure for Science (CiS) group for access to high–performance computing resources. This work was supported by the Max-Planck Society (J.E.P. and F.L.), Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) SFB-1403–414786233 (J.E.P., D.L., O.J., and H.L.), DFG/Agence Nationale de la Recherche Trilateral “RADAR” grant ANR-15-CE20-0016-01 (J.E.P. and J.A.D.), DFG SPP “DeCrypt” PA-917/8-1 (J.E.P. and C.U.), Germany’s Excellence Strategy CEPLAS (EXC-2048/1, Project 390686111) (J.E.P.), the Biotechnology and Biological Sciences Research Council (BBSRC Doctoral Training Program BB/M011216/1 to ELB), the EC j European Research Council (grant ERC-2016-STG-716233-MIREDI to K.V.K.) and NIH Director’s Award (1DP2AT011967-01 to K.V.K. and E.L.B.). O.J. is a member of the International Max-Planck PhD Research School (IMPRS). H.N. was supported within the framework of MadLand (http://madland.science; DFG priority program 2237). This work was supported by the Max-Planck Society (J.E.P. and F.L.), Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) SFB-1403–414786233 (J.E.P., D.L., O.J., and H.L.), DFG/Agence Nationale de la Recherche Trilateral “RADAR” grant ANR-15-CE20-0016-01 (J.E.P. and J.A.D.), DFG SPP “DeCrypt” PA-917/8-1 (J.E.P. and C.U.), Germany’s Excellence Strategy CEPLAS (EXC-2048/1, Project 390686111) (J.E.P.), the Biotechnology and Biological Sciences Research Council (BBSRC Doctoral Training Program BB/M011216/1 to ELB), the EC | European Research Council (grant ERC-2016-STG-716233-MIREDI to K.V.K.) and NIH Director’s Award (1DP2AT011967-01 to K.V.K. and E.L.B.). O.J. is a member of the International Max-Planck PhD Research School (IMPRS). H.N. was supported within the framework of MadLand (http://madland.science; DFG priority program 2237).

Funders	Funder number
Agence Nationale de la Recherche Trilateral	ANR-15-CE20-0016-01
CEPLAS	390686111, EXC-2048/1
DFG SPP	PA-917/8-1
Norwich UK
Sainsbury Laboratory
National Institutes of Health	1DP2AT011967-01
California Department of Fish and Game
Biotechnology and Biological Sciences Research Council	BB/M011216/1
European Commission
European Research Council	ERC-2016-STG-716233-MIREDI
Deutsche Forschungsgemeinschaft	SFB-1403–414786233
Max-Planck-Gesellschaft
International Max Planck Research School for Advanced Methods in Process and Systems Engineering

Keywords

Structural basis
Pathogen effector
Tir domains
Self-association
Resistance protein
Evolution
Family
Cell-death
Nad(+) cleavage activity
Defense

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kiac480Final published version, 1.88 MBLicence: CC BY

Cite this

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title = "Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1",

abstract = "Toll/Interleukin-1 receptor (TIR) domains are integral to immune systems across all kingdoms. In plants, TIRs are present in nucleotide-binding leucine-rich repeat (NLR) immune receptors, NLR-like, and TIR-only proteins. Although TIR-NLR and TIR signaling in plants require the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) protein family, TIRs persist in species that have no EDS1 members. To assess whether particular TIR groups evolved with EDS1, we searched for TIR-EDS1 co-occurrence patterns. Using a large-scale phylogenetic analysis of TIR domains from 39 algal and land plant species, we identified 4 TIR families that are shared by several plant orders. One group occurred in TIR-NLRs of eudicots and another in TIR-NLRs across eudicots and magnoliids. Two further groups were more widespread. A conserved TIR-only group co-occurred with EDS1 and members of this group elicit EDS1-dependent cell death. In contrast, a maize (Zea mays) representative of TIR proteins with tetratricopeptide repeats was also present in species without EDS1 and induced EDS1-independent cell death. Our data provide a phylogeny-based plant TIR classification and identify TIRs that appear to have evolved with and are dependent on EDS1, while others have EDS1-independent activity.",

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note = "Publisher Copyright: VC The Author(s) 2022.",

year = "2023",

month = jan,

doi = "10.1093/plphys/kiac480",

language = "English",

volume = "191",

pages = "626--642",

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T1 - Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1

AU - Johanndrees, Oliver

AU - Baggs, Erin L

AU - Uhlmann, Charles

AU - Locci, Federica

AU - Läßle, Henriette L

AU - Melkonian, Katharina

AU - Käufer, Kiara

AU - Dongus, Joram A

AU - Nakagami, Hirofumi

AU - Krasileva, Ksenia V

AU - Parker, Jane E

AU - Lapin, Dmitry

N1 - Publisher Copyright: VC The Author(s) 2022.

PY - 2023/1

Y1 - 2023/1

N2 - Toll/Interleukin-1 receptor (TIR) domains are integral to immune systems across all kingdoms. In plants, TIRs are present in nucleotide-binding leucine-rich repeat (NLR) immune receptors, NLR-like, and TIR-only proteins. Although TIR-NLR and TIR signaling in plants require the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) protein family, TIRs persist in species that have no EDS1 members. To assess whether particular TIR groups evolved with EDS1, we searched for TIR-EDS1 co-occurrence patterns. Using a large-scale phylogenetic analysis of TIR domains from 39 algal and land plant species, we identified 4 TIR families that are shared by several plant orders. One group occurred in TIR-NLRs of eudicots and another in TIR-NLRs across eudicots and magnoliids. Two further groups were more widespread. A conserved TIR-only group co-occurred with EDS1 and members of this group elicit EDS1-dependent cell death. In contrast, a maize (Zea mays) representative of TIR proteins with tetratricopeptide repeats was also present in species without EDS1 and induced EDS1-independent cell death. Our data provide a phylogeny-based plant TIR classification and identify TIRs that appear to have evolved with and are dependent on EDS1, while others have EDS1-independent activity.

AB - Toll/Interleukin-1 receptor (TIR) domains are integral to immune systems across all kingdoms. In plants, TIRs are present in nucleotide-binding leucine-rich repeat (NLR) immune receptors, NLR-like, and TIR-only proteins. Although TIR-NLR and TIR signaling in plants require the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) protein family, TIRs persist in species that have no EDS1 members. To assess whether particular TIR groups evolved with EDS1, we searched for TIR-EDS1 co-occurrence patterns. Using a large-scale phylogenetic analysis of TIR domains from 39 algal and land plant species, we identified 4 TIR families that are shared by several plant orders. One group occurred in TIR-NLRs of eudicots and another in TIR-NLRs across eudicots and magnoliids. Two further groups were more widespread. A conserved TIR-only group co-occurred with EDS1 and members of this group elicit EDS1-dependent cell death. In contrast, a maize (Zea mays) representative of TIR proteins with tetratricopeptide repeats was also present in species without EDS1 and induced EDS1-independent cell death. Our data provide a phylogeny-based plant TIR classification and identify TIRs that appear to have evolved with and are dependent on EDS1, while others have EDS1-independent activity.

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KW - Self-association

KW - Resistance protein

KW - Evolution

KW - Family

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KW - Nad(+) cleavage activity

KW - Defense

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SN - 0032-0889

VL - 191

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EP - 642

JO - Plant Physiology

JF - Plant Physiology

IS - 1

ER -

Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1

Abstract

Bibliographical note

Funding

Keywords

Access to Document

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