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Research Article

NAD+ cleavage activity by animal and plant TIR domains in cell death pathways

Shane Horsefield https://orcid.org/0000-0003-0786-3995, Hayden Burdett https://orcid.org/0000-0003-4803-9660, Xiaoxiao Zhang https://orcid.org/0000-0002-5417-6963, Mohammad K. Manik, Yun Shi https://orcid.org/0000-0003-3365-4679, Jian Chen https://orcid.org/0000-0001-8670-6984, Tiancong Qi, Jonathan Gilley, Jhih-Siang Lai https://orcid.org/0000-0001-5677-5890, Maxwell X. Rank https://orcid.org/0000-0001-6962-9235, Lachlan W. Casey https://orcid.org/0000-0002-4458-0137, Weixi Gu, Daniel J. Ericsson https://orcid.org/0000-0001-5101-9244, Gabriel Foley https://orcid.org/0000-0002-0487-2629, Robert O. Hughes, Todd Bosanac, Mark von Itzstein https://orcid.org/0000-0001-6302-7524, John P. Rathjen https://orcid.org/0000-0003-4073-8088, Jeffrey D. Nanson, Mikael Boden https://orcid.org/0000-0003-3548-268X, Ian B. Dry https://orcid.org/0000-0001-8900-4427, Simon J. Williams https://orcid.org/0000-0003-4781-6261, Brian J. Staskawicz https://orcid.org/0000-0002-9711-3962, Michael P. Coleman, Thomas Ve https://orcid.org/0000-0002-0113-1905 [email protected], Peter N. Dodds https://orcid.org/0000-0003-0620-5923 [email protected], and Bostjan Kobe https://orcid.org/0000-0001-9413-9166 [email protected]
Science • 23 Aug 2019 • Vol 365, Issue 6455 • pp. 793-799 • DOI: 10.1126/science.aax1911
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NAD depletion as pathogen response

One way that plants respond to pathogen infection is by sacrificing the infected cells. The nucleotide-binding leucine-rich repeat immune receptors responsible for this hypersensitive response carry Toll/interleukin-1 receptor (TIR) domains. In two papers, Horsefield et al. and Wan et al. report that these TIR domains cleave the metabolic cofactor nicotinamide adenine dinucleotide (NAD+) as part of their cell-death signaling in response to pathogens. Similar signaling links mammalian TIR-containing proteins to NAD+ depletion during Wallerian degeneration of neurons.
Science, this issue p. 793, p. 799

Abstract

SARM1 (sterile alpha and TIR motif containing 1) is responsible for depletion of nicotinamide adenine dinucleotide in its oxidized form (NAD+) during Wallerian degeneration associated with neuropathies. Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogen effector proteins and trigger localized cell death to restrict pathogen infection. Both processes depend on closely related Toll/interleukin-1 receptor (TIR) domains in these proteins, which, as we show, feature self-association–dependent NAD+ cleavage activity associated with cell death signaling. We further show that SARM1 SAM (sterile alpha motif) domains form an octamer essential for axon degeneration that contributes to TIR domain enzymatic activity. The crystal structures of ribose and NADP+ (the oxidized form of nicotinamide adenine dinucleotide phosphate) complexes of SARM1 and plant NLR RUN1 TIR domains, respectively, reveal a conserved substrate binding site. NAD+ cleavage by TIR domains is therefore a conserved feature of animal and plant cell death signaling pathways.
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References and Notes

1
T. Ve, S. J. Williams, B. Kobe, Structure and function of Toll/interleukin-1 receptor/resistance protein (TIR) domains. Apoptosis 20, 250–261 (2015).
2
N. J. Gay, M. F. Symmons, M. Gangloff, C. E. Bryant, Assembly and localization of Toll-like receptor signalling complexes. Nat. Rev. Immunol. 14, 546–558 (2014).
3
T. Ve, P. R. Vajjhala, A. Hedger, T. Croll, F. DiMaio, S. Horsefield, X. Yu, P. Lavrencic, Z. Hassan, G. P. Morgan, A. Mansell, M. Mobli, A. O’Carroll, B. Chauvin, Y. Gambin, E. Sierecki, M. J. Landsberg, K. J. Stacey, E. H. Egelman, B. Kobe, Structural basis of TIR-domain-assembly formation in MAL- and MyD88-dependent TLR4 signaling. Nat. Struct. Mol. Biol. 24, 743–751 (2017).
4
P. R. Vajjhala, T. Ve, A. Bentham, K. J. Stacey, B. Kobe, The molecular mechanisms of signaling by cooperative assembly formation in innate immunity pathways. Mol. Immunol. 86, 23–37 (2017).
5
M. Carty, R. Goodbody, M. Schröder, J. Stack, P. N. Moynagh, A. G. Bowie, The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat. Immunol. 7, 1074–1081 (2006).
6
J. M. Osterloh, J. Yang, T. M. Rooney, A. N. Fox, R. Adalbert, E. H. Powell, A. E. Sheehan, M. A. Avery, R. Hackett, M. A. Logan, J. M. MacDonald, J. S. Ziegenfuss, S. Milde, Y. J. Hou, C. Nathan, A. Ding, R. H. Brown Jr.., L. Conforti, M. Coleman, M. Tessier-Lavigne, S. Züchner, M. R. Freeman, dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337, 481–484 (2012).
7
Y. Kim, P. Zhou, L. Qian, J. Z. Chuang, J. Lee, C. Li, C. Iadecola, C. Nathan, A. Ding, MyD88-5 links mitochondria, microtubules, and JNK3 in neurons and regulates neuronal survival. J. Exp. Med. 204, 2063–2074 (2007).
8
J. Gerdts, E. J. Brace, Y. Sasaki, A. DiAntonio, J. Milbrandt, SARM1 activation triggers axon degeneration locally via NAD+ destruction. Science 348, 453–457 (2015).
9
P. N. Dodds, J. P. Rathjen, Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539–548 (2010).
10
J. Gerdts, D. W. Summers, J. Milbrandt, A. DiAntonio, Axon self-destruction: New links among SARM1, MAPKs, and NAD+ metabolism. Neuron 89, 449–460 (2016).
11
J. Wang, Q. Zhai, Y. Chen, E. Lin, W. Gu, M. W. McBurney, Z. He, A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 170, 349–355 (2005).
12
J. Gerdts, D. W. Summers, Y. Sasaki, A. DiAntonio, J. Milbrandt, Sarm1-mediated axon degeneration requires both SAM and TIR interactions. J. Neurosci. 33, 13569–13580 (2013).
13
K. Essuman, D. W. Summers, Y. Sasaki, X. Mao, A. DiAntonio, J. Milbrandt, The SARM1 Toll/interleukin-1 receptor domain possesses intrinsic NAD+ cleavage activity that promotes pathological axonal degeneration. Neuron 93, 1334–1343.e5 (2017).
14
X. Zhang, P. N. Dodds, M. Bernoux, What do we know about NOD-like receptors in plant immunity? Annu. Rev. Phytopathol. 55, 205–229 (2017).
15
X. Zhang, M. Bernoux, A. R. Bentham, T. E. Newman, T. Ve, L. W. Casey, T. M. Raaymakers, J. Hu, T. I. Croll, K. J. Schreiber, B. J. Staskawicz, P. A. Anderson, K. H. Sohn, S. J. Williams, P. N. Dodds, B. Kobe, Multiple functional self-association interfaces in plant TIR domains. Proc. Natl. Acad. Sci. U.S.A. 114, E2046–E2052 (2017).
16
M. T. Nishimura, R. G. Anderson, K. A. Cherkis, T. F. Law, Q. L. Liu, M. Machius, Z. L. Nimchuk, L. Yang, E. H. Chung, F. El Kasmi, M. Hyunh, E. Osborne Nishimura, J. E. Sondek, J. L. Dangl, TIR-only protein RBA1 recognizes a pathogen effector to regulate cell death in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 114, E2053–E2062 (2017).
17
L. Holm, L. M. Laakso, Dali server update. Nucleic Acids Res. 44, W351–W355 (2016).
18
Q. Zhang, C. M. Zmasek, X. Cai, A. Godzik, TIR domain-containing adaptor SARM is a late addition to the ongoing microbe-host dialog. Dev. Comp. Immunol. 35, 461–468 (2011).
19
G. Pergolizzi, J. N. Butt, R. P. Bowater, G. K. Wagner, A novel fluorescent probe for NAD-consuming enzymes. Chem. Commun. 47, 12655–12657 (2011).
20
Y. Gibon, F. Larher, Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium. Anal. Biochem. 251, 153–157 (1997).
21
N. Czudnochowski, A. L. Wang, J. Finer-Moore, R. M. Stroud, In human pseudouridine synthase 1 (hPus1), a C-terminal helical insert blocks tRNA from binding in the same orientation as in the Pus1 bacterial homologue TruA, consistent with their different target selectivities. J. Mol. Biol. 425, 3875–3887 (2013).
22
S. Nimma, T. Ve, S. J. Williams, B. Kobe, Towards the structure of the TIR-domain signalosome. Curr. Opin. Struct. Biol. 43, 122–130 (2017).
23
D. W. Summers, D. A. Gibson, A. DiAntonio, J. Milbrandt, SARM1-specific motifs in the TIR domain enable NAD+ loss and regulate injury-induced SARM1 activation. Proc. Natl. Acad. Sci. U.S.A. 113, E6271–E6280 (2016).
24
M. Bienz, Signalosome assembly by domains undergoing dynamic head-to-tail polymerization. Trends Biochem. Sci. 39, 487–495 (2014).
25
M. Bernoux, T. Ve, S. Williams, C. Warren, D. Hatters, E. Valkov, X. Zhang, J. G. Ellis, B. Kobe, P. N. Dodds, Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host Microbe 9, 200–211 (2011).
26
M. Wiermer, B. J. Feys, J. E. Parker, Plant immunity: The EDS1 regulatory node. Curr. Opin. Plant Biol. 8, 383–389 (2005).
27
A. Schultink, T. Qi, A. Lee, A. D. Steinbrenner, B. Staskawicz, Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J. 92, 787–795 (2017).
28
M. Bernoux, H. Burdett, S. J. Williams, X. Zhang, C. Chen, K. Newell, G. J. Lawrence, B. Kobe, J. G. Ellis, P. A. Anderson, P. N. Dodds, Comparative analysis of the flax immune receptors L6 and L7 suggests an equilibrium-based switch activation model. Plant Cell 28, 146–159 (2016).
29
J.-S. Lai, B. Rost, B. Kobe, M. Boden, Evolutionary model of protein secondary structure capable of revealing new biological relationships. bioRxiv 563452 [Preprint]. 28 February 2019; https://doi.org/10.1101/563452.
30
C. P. Ponting, R. R. Russell, The natural history of protein domains. Annu. Rev. Biophys. Biomol. Struct. 31, 45–71 (2002).
31
K. Essuman, D. W. Summers, Y. Sasaki, X. Mao, A. K. Y. Yim, A. DiAntonio, J. Milbrandt, TIR domain proteins are an ancient family of NAD+-consuming enzymes. Curr. Biol. 28, 421–430.e4 (2018).
32
Z. Y. Zhao, X. J. Xie, W. H. Li, J. Liu, Z. Chen, B. Zhang, T. Li, S. L. Li, J. G. Lu, L. Zhang, L. H. Zhang, Z. Xu, H. C. Lee, Y. J. Zhao, A cell-permeant mimetic of NMN activates SARM1 to produce cyclic ADP-ribose and induce non-apoptotic cell death. iScience 15, 452–466 (2019).
33
M. Matyszewski, W. Zheng, J. Lueck, B. Antiochos, E. H. Egelman, J. Sohn, Cryo-EM structure of the NLRC4CARD filament provides insights into how symmetric and asymmetric supramolecular structures drive inflammasome assembly. J. Biol. Chem. 293, 20240–20248 (2018).
34
J. Wang, M. Hu, J. Wang, J. Qi, Z. Han, G. Wang, Y. Qi, H. W. Wang, J. M. Zhou, J. Chai, Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364, eaav5870 (2019).
35
Q. Liu, R. Graeff, I. A. Kriksunov, H. Jiang, B. Zhang, N. Oppenheimer, H. Lin, B. V. Potter, H. C. Lee, Q. Hao, Structural basis for enzymatic evolution from a dedicated ADP-ribosyl cyclase to a multifunctional NAD hydrolase. J. Biol. Chem. 284, 27637–27645 (2009).
36
L. Hunt, F. Lerner, M. Ziegler, NAD–new roles in signalling and gene regulation in plants. New Phytol. 163, 31–44 (2004).
37
B. Gakière, J. Hao, L. De Bont, P. Pétriacq, A. Nunes-Nesi, A. R. Fernie, NAD+ biosynthesis and signaling in plants. Crit. Rev. Plant Sci. 2018, 1–49 (2018).
38
N. J. Oppenheimer, A. J. Handlon, in The Enzymes, D. S. Sigman, Ed. (Academic Press, 1992), pp. 453–505.
39
H. C. Lee, Structure and enzymatic functions of human CD38. Mol. Med. 12, 317–323 (2006).
40
L. Stols, M. Gu, L. Dieckman, R. Raffen, F. R. Collart, M. I. Donnelly, A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein Expr. Purif. 25, 8–15 (2002).
41
F. W. Studier, Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207–234 (2005).
42
T. Ve, S. Williams, E. Valkov, J. G. Ellis, P. N. Dodds, B. Kobe, Crystallization, X-ray diffraction analysis and preliminary structure determination of the TIR domain from the flax resistance protein L6. Acta Crystallogr. F 67, 237–240 (2011).
43
S. J. Williams, L. Yin, G. Foley, L. W. Casey, M. A. Outram, D. J. Ericsson, J. Lu, M. Boden, I. B. Dry, B. Kobe, Structure and function of the TIR domain from the grape NLR protein RPV1. Front. Plant Sci. 7, 1850 (2016).
44
K. J. Schreiber, A. Bentham, S. J. Williams, B. Kobe, B. J. Staskawicz, Multiple domain associations within the Arabidopsis immune receptor RPP1 regulate the activation of programmed cell death. PLOS Pathog. 12, e1005769 (2016).
45
L. Wan, X. Zhang, S. J. Williams, T. Ve, M. Bernoux, K. H. Sohn, J. D. Jones, P. N. Dodds, B. Kobe, Crystallization and preliminary X-ray diffraction analyses of the TIR domains of three TIR-NB-LRR proteins that are involved in disease resistance in Arabidopsis thaliana. Acta Crystallogr. F 69, 1275–1280 (2013).
46
N. C. Gassner, B. W. Matthews, Use of differentially substituted selenomethionine proteins in X-ray structure determination. Acta Crystallogr. D 55, 1967–1970 (1999).
47
T. M. McPhillips, S. E. McPhillips, H. J. Chiu, A. E. Cohen, A. M. Deacon, P. J. Ellis, E. Garman, A. Gonzalez, N. K. Sauter, R. P. Phizackerley, S. M. Soltis, P. Kuhn, Blu-Ice and the Distributed Control System: Software for data acquisition and instrument control at macromolecular crystallography beamlines. J. Synchrotron Radiat. 9, 401–406 (2002).
48
T. G. Battye, L. Kontogiannis, O. Johnson, H. R. Powell, A. G. Leslie, iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D 67, 271–281 (2011).
49
P. Evans, Scaling and assessment of data quality. Acta Crystallogr. D 62, 72–82 (2006).
50
M. D. Winn, C. C. Ballard, K. D. Cowtan, E. J. Dodson, P. Emsley, P. R. Evans, R. M. Keegan, E. B. Krissinel, A. G. Leslie, A. McCoy, S. J. McNicholas, G. N. Murshudov, N. S. Pannu, E. A. Potterton, H. R. Powell, R. J. Read, A. Vagin, K. S. Wilson, Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011).
51
P. D. Adams, D. Baker, A. T. Brunger, R. Das, F. DiMaio, R. J. Read, D. C. Richardson, J. S. Richardson, T. C. Terwilliger, Advances, interactions, and future developments in the CNS, Phenix, and Rosetta structural biology software systems. Annu. Rev. Biophys. 42, 265–287 (2013).
52
A. J. McCoy, Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D 63, 32–41 (2007).
53
P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
54
V. B. Chen, W. B. Arendall 3rd, J. J. Headd, D. A. Keedy, R. M. Immormino, G. J. Kapral, L. W. Murray, J. S. Richardson, D. C. Richardson, MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010).
55
W. Kabsch, XDS. Acta Crystallogr. D 66, 125–132 (2010).
56
N. Stein, CHAINSAW: A program for mutating pdb files used as templates in molecular replacement. J. Appl. Crystallogr. 41, 641–643 (2008).
57
A. Feechan, C. Anderson, L. Torregrosa, A. Jermakow, P. Mestre, S. Wiedemann-Merdinoglu, D. Merdinoglu, A. R. Walker, L. Cadle-Davidson, B. Reisch, S. Aubourg, N. Bentahar, B. Shrestha, A. Bouquet, A. F. Adam-Blondon, M. R. Thomas, I. B. Dry, Genetic dissection of a TIR-NB-LRR locus from the wild North American grapevine species Muscadinia rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine. Plant J. 76, 661–674 (2013).
58
M. Landau, I. Mayrose, Y. Rosenberg, F. Glaser, E. Martz, T. Pupko, N. Ben-Tal, ConSurf 2005: The projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33 (suppl. 2), W299–W302 (2005).
59
E. Krissinel, K. Henrick, Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007).
60
J. Wen, T. Arakawa, J. S. Philo, Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal. Biochem. 240, 155–166 (1996).
61
P. V. Konarev, M. V. Petoukhov, V. V. Volkov, D. I. Svergun, ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39, 277–286 (2006).
62
R. P. Rambo, J. A. Tainer, Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496, 477–481 (2013).
63
D. Franke, M. V. Petoukhov, P. V. Konarev, A. Panjkovich, A. Tuukkanen, H. D. T. Mertens, A. G. Kikhney, N. R. Hajizadeh, J. M. Franklin, C. M. Jeffries, D. I. Svergun, ATSAS 2.8: A comprehensive data analysis suite for small-angle scattering from macromolecular solutions. J. Appl. Crystallogr. 50, 1212–1225 (2017).
64
N. R. Hajizadeh, D. Franke, C. M. Jeffries, D. I. Svergun, Consensus Bayesian assessment of protein molecular mass from solution X-ray scattering data. Sci. Rep. 8, 7204 (2018).
65
J. Gilley, M. P. Coleman, Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLOS Biol. 8, e1000300 (2010).
66
C. Y. Chen, C. W. Lin, C. Y. Chang, S. T. Jiang, Y. P. Hsueh, Sarm1, a negative regulator of innate immunity, interacts with syndecan-2 and regulates neuronal morphology. J. Cell Biol. 193, 769–784 (2011).
67
H. Inoue, H. Nojima, H. Okayama, High efficiency transformation of Escherichia coli with plasmids. Gene 96, 23–28 (1990).
68
A. Buchholz, R. Takors, C. Wandrey, Quantification of intracellular metabolites in Escherichia coli K12 using liquid chromatographic-electrospray ionization tandem mass spectrometric techniques. Anal. Biochem. 295, 129–137 (2001).
69
M. Bernoux, T. Timmers, A. Jauneau, C. Brière, P. J. de Wit, Y. Marco, L. Deslandes, RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20, 2252–2264 (2008).
70
P. N. Dodds, G. J. Lawrence, A. M. Catanzariti, M. A. Ayliffe, J. G. Ellis, The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16, 755–768 (2004).
71
W. Sherman, T. Day, M. P. Jacobson, R. A. Friesner, R. Farid, Novel procedure for modeling ligand/receptor induced fit effects. J. Med. Chem. 49, 534–553 (2006).
72
R. A. Friesner, J. L. Banks, R. B. Murphy, T. A. Halgren, J. J. Klicic, D. T. Mainz, M. P. Repasky, E. H. Knoll, M. Shelley, J. K. Perry, D. E. Shaw, P. Francis, P. S. Shenkin, Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 47, 1739–1749 (2004).
73
T. A. Halgren, R. B. Murphy, R. A. Friesner, H. S. Beard, L. L. Frye, W. T. Pollard, J. L. Banks, Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J. Med. Chem. 47, 1750–1759 (2004).
74
M. P. Jacobson, R. A. Friesner, Z. Xiang, B. Honig, On the role of the crystal environment in determining protein side-chain conformations. J. Mol. Biol. 320, 597–608 (2002).
75
M. Abraham, T. Murtola, R. Schulz, S. Páll, J. C. Smith, B. Hess, E. Lindahl, GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1-2, 19–25 (2015).
76
V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, C. Simmerling, Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712–725 (2006).
77
S. Páll, B. Hess, A flexible algorithm for calculating pair interactions on SIMD architectures. Comput. Phys. Commun. 184, 2641–2650 (2013).
78
T. Darden, D. York, L. Pedersen, Particle mesh Ewald (PME): A N log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089–10092 (1993).
79
U. Essmann, L. Perera, M. L. Berkowitz, T. Darden, H. Lee, L. G. Pedersen, A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577–8593 (1995).
80
H. J. C. Berendsen, J. P. M. Postma, W. F. van Gunsteren, A. DiNola, J. R. Haak, Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690 (1984).
81
B. Hess, P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation. J. Chem. Theory Comput. 4, 116–122 (2008).
82
S. Unni, Y. Huang, R. M. Hanson, M. Tobias, S. Krishnan, W. W. Li, J. E. Nielsen, N. A. Baker, Web servers and services for electrostatics calculations with APBS and PDB2PQR. J. Comput. Chem. 32, 1488–1491 (2011).
83
S. J. Williams, K. H. Sohn, L. Wan, M. Bernoux, P. F. Sarris, C. Segonzac, T. Ve, Y. Ma, S. B. Saucet, D. J. Ericsson, L. W. Casey, T. Lonhienne, D. J. Winzor, X. Zhang, A. Coerdt, J. E. Parker, P. N. Dodds, B. Kobe, J. D. Jones, Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344, 299–303 (2014).
84
A. Prlić, S. Bliven, P. W. Rose, W. F. Bluhm, C. Bizon, A. Godzik, P. E. Bourne, Pre-calculated protein structure alignments at the RCSB PDB website. Bioinformatics 26, 2983–2985 (2010).
85
P. Mestre, D. C. Baulcombe, Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18, 491–501 (2006).
86
S. P. Dinesh-Kumar, W. H. Tham, B. J. Baker, Structure-function analysis of the tobacco mosaic virus resistance gene N. Proc. Natl. Acad. Sci. U.S.A. 97, 14789–14794 (2000).
87
M. R. Swiderski, D. Birker, J. D. Jones, The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol. Plant Microbe Interact. 22, 157–165 (2009).
88
K. V. Krasileva, D. Dahlbeck, B. J. Staskawicz, Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22, 2444–2458 (2010).

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Volume 365 | Issue 6455
23 August 2019

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Received: 28 February 2019
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Published in print: 23 August 2019

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We acknowledge the use of the University of Queensland Remote Operation Crystallization and X-Ray Diffraction (UQ-ROCX) Facility and the macromolecular crystallography (MX) and small/wide-angle X-ray scattering (SAXS/WAXS) beamlines at the Australian Synchrotron, Victoria, Australia. MD simulations were performed on the High Performance Computing cluster “Gowonda” at Griffith University. We thank V. Masic and N. Deerain for technical contributions. Funding: The work was supported by the National Health and Medical Research Council (NHMRC grants 1107804 and 1160570 to B.K. and T.V.. 1071659 to B.K., and 1108859 to T.V.), and the Australian Research Council (ARC grants DP160102244 and DP190102526 to B.K. and P.N.D.). B.K. was an NHMRC Principal Research Fellow (1110971) and ARC Laureate Fellow (FL180100109). T.V. received ARC DECRA (DE170100783) funding and S.J.W. received ARC DECRA DE160100893 funding. J.C. received a Chinese Scholarship Council (CSC) postgraduate scholarship. Y.S. was a Griffith University postdoctoral fellow. J.G. was supported by the UK Medical Research Council and M.P.C. was supported by the John and Lucille van Geest Foundation. M.K.M. was supported by the Australian Government Research Training Program (RTP). Author contributions: S.H., H.B., X.Z., M.K.M., Y.S., J.G., R.O.H., T.B., S.J.W., T.V., P.D., and B.K. designed the research; S.H., H.B., X.Z., M.K.M., Y.S., J.G., J.C., L.W.C., T.Q., J.S.L., W.G., M.X.R., D.J.E., G.F., R.O.H., T.B., and T.V. performed the research; S.H., H.B., X.Z., M.K.M., Y.S., J.G., L.W.C., R.O.H., T.B., J.S.L., M.X.R., D.J.E., G.F., M.v.I., J.P.R., J.D.N., M.B., I.B.D., B.J.S., S.J.W., M.P.C., T.V., P.N.D., and B.K. analyzed the data; S.H., H.B., X.Z., M.K.M., Y.S., T.V., and B.K. wrote the paper; all authors edited and contributed to writing. Competing interests: B.K. is a consultant for Disarm Therapeutics. B.K. and S.H. receive research funding from Disarm Therapeutics. Data and materials availability: Coordinates and structure factors for all crystal structures determined in this study have been deposited in the Protein Data Bank with IDs 6O0S, 6O0T, 6O0R, 6O0Q, 6O0U, 6O1B, 6O0V, and 6O0W.

Authors

Affiliations

Shane Horsefield* https://orcid.org/0000-0003-0786-3995
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Hayden Burdett* https://orcid.org/0000-0003-4803-9660
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Xiaoxiao Zhang* https://orcid.org/0000-0002-5417-6963
Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia.
Plant Sciences Division, Research School of Biology, The Australian National University, Canberra ACT 2601, Australia.
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Mohammad K. Manik*
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Yun Shi* https://orcid.org/0000-0003-3365-4679
Institute for Glycomics, Griffith University, Southport, QLD 4222, Australia.
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Jian Chen https://orcid.org/0000-0001-8670-6984
Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia.
Plant Sciences Division, Research School of Biology, The Australian National University, Canberra ACT 2601, Australia.
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Tiancong Qi
Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720, USA.
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Jonathan Gilley
John van Geest Centre for Brain Repair, Department of Clinical Neurosciences, University of Cambridge, ED Adrian Building, Forvie Site, Robinson Way, Cambridge CB2 0PY, UK.
Babraham Institute, Babraham, Cambridge CB22 3AT, UK.
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Jhih-Siang Lai https://orcid.org/0000-0001-5677-5890
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Maxwell X. Rank https://orcid.org/0000-0001-6962-9235
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Lachlan W. Casey https://orcid.org/0000-0002-4458-0137
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
Centre for Microscopy and Microanalysis, University of Queensland, Brisbane, QLD 4072, Australia.
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Weixi Gu
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Daniel J. Ericsson https://orcid.org/0000-0001-5101-9244
Macromolecular Crystallography (MX) Beamlines, Australian Synchrotron, Melbourne, VIC 3168, Australia.
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Gabriel Foley https://orcid.org/0000-0002-0487-2629
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Robert O. Hughes
Disarm Therapeutics, 400 Technology Square, Cambridge, MA 02139, USA.
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Todd Bosanac
Disarm Therapeutics, 400 Technology Square, Cambridge, MA 02139, USA.
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Mark von Itzstein https://orcid.org/0000-0001-6302-7524
Institute for Glycomics, Griffith University, Southport, QLD 4222, Australia.
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John P. Rathjen https://orcid.org/0000-0003-4073-8088
Plant Sciences Division, Research School of Biology, The Australian National University, Canberra ACT 2601, Australia.
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Jeffrey D. Nanson
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Mikael Boden https://orcid.org/0000-0003-3548-268X
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Ian B. Dry https://orcid.org/0000-0001-8900-4427
Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Urrbrae, SA 5064, Australia.
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Simon J. Williams https://orcid.org/0000-0003-4781-6261
Plant Sciences Division, Research School of Biology, The Australian National University, Canberra ACT 2601, Australia.
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Brian J. Staskawicz https://orcid.org/0000-0002-9711-3962
Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720, USA.
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Michael P. Coleman
John van Geest Centre for Brain Repair, Department of Clinical Neurosciences, University of Cambridge, ED Adrian Building, Forvie Site, Robinson Way, Cambridge CB2 0PY, UK.
Babraham Institute, Babraham, Cambridge CB22 3AT, UK.
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Thomas Ve† https://orcid.org/0000-0002-0113-1905 [email protected]
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
Institute for Glycomics, Griffith University, Southport, QLD 4222, Australia.
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Peter N. Dodds† https://orcid.org/0000-0003-0620-5923 [email protected]
Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia.
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Bostjan Kobe† https://orcid.org/0000-0001-9413-9166 [email protected]
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, QLD 4072, Australia.
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Funding Information

Australian Research Council: DP160102244, DP190102526
Australian Research Council: DP160102244, DP190102526

Notes

*
These authors contributed equally to this work.
†Corresponding author. Email: [email protected] (B.K.); [email protected] (T.V.); [email protected] (P.N.D.)

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