Comparative analysis of the flax immune receptors L6 and L7 suggests an equilibrium-based switch activation model

Plant Cell

Volumn 28, Issue 1, 2016, Pages 146-159

  Bernoux, Maud ^a   Burdett, Hayden ^b   Williams, Simon J ^c   Zhang, Xiaoxiao ^a   Chen, Chunhong ^a   Newell, Kim ^a   Lawrence, Gregory J ^a   Kobe, Bostjan ^c   Ellis, Jeffrey G ^a   Anderson, Peter A ^b   Dodds, Peter N ^a  

^a CSIRO   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CELL SURFACE RECEPTOR; PLANT PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CELL DEATH; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; FLAX; GENETIC POLYMORPHISM; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CELL DEATH; FLAX; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PLANT PROTEINS; POLYMORPHISM, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

EID: 84957808868     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00303     Document Type: Article

References (69)

1. Axtell, M.J., and Staskawicz, B.J. (2003). Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
2. Bao, Q., Riedl, S.J., and Shi, Y. (2005). Structure of Apaf-1 in the auto-inhibited form: a critical role for ADP. Cell Cycle 4: 1001-1003.
3. Bendahmane, A., Farnham, G., Moffett, P., and Baulcombe, D.C. (2002). Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 32: 195-204.
4. Bent, A.F., Kunkel, B.N., Dahlbeck, D., Brown, K.L., Schmidt, R., Giraudat, J., Leung, J., and Staskawicz, B.J. (1994). RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856-1860.
5. Bernoux, M., Ellis, J.G., and Dodds, P.N. (2011a). New insights in plant immunity signaling activation. Curr. Opin. Plant Biol. 14: 512-518.
6. Bernoux, M., Timmers, T., Jauneau, A., Brière, C., de Wit, P.J., Marco, Y., and Deslandes, L. (2008). 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.
7. Bernoux, M., Ve, T., Williams, S., Warren, C., Hatters, D., Valkov, E., Zhang, X., Ellis, J.G., Kobe, B., and Dodds, P.N. (2011b). 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.
8. Chapman, S., Stevens, L.J., Boevink, P.C., Engelhardt, S., Alexander, C.J., Harrower, B., Champouret, N., McGeachy, K., Van Weymers, P.S., Chen, X., Birch, P.R., and Hein, I. (2014). Detection of the virulent form of AVR3a from Phytophthora infestans following artificial evolution of potato resistance gene R3a. PLoS One 9: e110158.
9. Collier, S.M., Hamel, L.P., and Moffett, P. (2011). Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol. Plant Microbe Interact. 24: 918-931.
10. Dangl, J.L., and Jones, J.D. (2001). Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
11. Danot, O. (2015). How ‘arm-twisting’ by the inducer triggers activation of the MalT transcription factor, a typical signal transduction ATPase with numerous domains (STAND). Nucleic Acids Res. 43: 3089-3099.
12. Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Ayliffe, M.A., and Ellis, J.G. (2004). The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16: 755-768.
13. Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Teh, T., Wang, C.I., Ayliffe, M.A., Kobe, B., and Ellis, J.G. (2006). Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA 103: 8888-8893.
14. Dodds, P.N., and Rathjen, J.P. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11: 539-548.
15. Duncan, J.A., Bergstralh, D.T., Wang, Y., Willingham, S.B., Ye, Z., Zimmermann, A.G., and Ting, J.P. (2007). Cryopyrin/NALP3 binds ATP/dATP, is an ATPase, and requires ATP binding to mediate in-flammatory signaling. Proc. Natl. Acad. Sci. USA 104: 8041-8046.
16. Ellis, J.G., Lawrence, G.J., Luck, J.E., and Dodds, P.N. (1999). Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11: 495-506.
17. Faustin, B., Lartigue, L., Bruey, J.M., Luciano, F., Sergienko, E., Bailly-Maitre, B., Volkmann, N., Hanein, D., Rouiller, I., and Reed, J.C. (2007). Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 25: 713-724.
18. Flor, H.H. (1954). Seed-flax improvement. III. Flax rust. Adv. Agron. 6: 152-161.
19. Frost, D., Way, H., Howles, P., Luck, J., Manners, J., Hardham, A., Finnegan, J., and Ellis, J. (2004). Tobacco transgenic for the flax rust resistance gene L expresses allele-specific activation of defense responses. Mol. Plant Microbe Interact. 17: 224-232.
20. Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., Innes, R.W., and Dangl, J.L. (1995). Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846.
21. Growney, J.D., and Dietrich, W.F. (2000). High-resolution genetic and physical map of the Lgn1 interval in C57BL/6J implicates Naip2 or Naip5 in Legionella pneumophila pathogenesis. Genome Res. 10: 1158-1171.
22. Harris, C.J., Slootweg, E.J., Goverse, A., and Baulcombe, D.C. (2013). Stepwise artificial evolution of a plant disease resistance gene. Proc. Natl. Acad. Sci. USA 110: 21189-21194.
23. Howles, P., Lawrence, G., Finnegan, J., McFadden, H., Ayliffe, M., Dodds, P., and Ellis, J. (2005). Autoactive alleles of the flax L6 rust resistance gene induce non-race-specific rust resistance associated with the hypersensitive response. Mol. Plant Microbe Interact. 18: 570-582.
24. Hu, Z., et al. (2013). Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341: 172-175.
25. Inohara, N., Koseki, T., del Peso, L., Hu, Y., Yee, C., Chen, S., Carrio, R., Merino, J., Liu, D., Ni, J., and Núñez, G. (1999). Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-kappaB. J. Biol. Chem. 274: 14560-14567.
26. Inohara, N., and Nuñez, G. (2003). NODs: intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol. 3: 371-382.
27. Islam, M.R., and Mayo, G.M.E. (1990). A compendium on host genes in flax conferring resistance to flax rust. Plant Breed. 104: 89-100.
28. Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323-329.
29. Kim, H.E., Du, F., Fang, M., and Wang, X. (2005). Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1. Proc. Natl. Acad. Sci. USA 102: 17545-17550.
30. Krasileva, K.V., Dahlbeck, D., and Staskawicz, B.J. (2010). 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.
31. Kushnirov, V.V. (2000). Rapid and reliable protein extraction from yeast. Yeast 16: 857-860.
32. Lawrence, G.J., Finnegan, E.J., Ayliffe, M.A., and Ellis, J.G. (1995). The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195-1206.
33. Lawrence, G.J., Mayo, G.M.E., and Shepherd, K.W. (1981). Inter-actions between genes controlling pathogenicity in the flax rust fungus. Phytopathology 71: 12-19.
34. Luck, J.E., Lawrence, G.J., Dodds, P.N., Shepherd, K.W., and Ellis, J.G. (2000). Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 12: 1367-1377.
35. Lukasik-Shreepaathy, E., Slootweg, E., Richter, H., Goverse, A., Cornelissen, B.J., and Takken, F.L. (2012). Dual regulatory roles of the extended N terminus for activation of the tomato MI-1 2 resistance protein. Mol. Plant Microbe Interact. 25: 1045-1057.
36. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R., and Dangl, J.L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
37. Maekawa, T., et al. (2011). Coiled-coil domain-dependent homo-dimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9: 187-199.
38. Marquenet, E., and Richet, E. (2007). How integration of positive and negative regulatory signals by a STAND signaling protein depends on ATP hydrolysis. Mol. Cell 28: 187-199.
39. McIntosh, R.A., Wellings, C.R., and Park, R.F. (1995). Wheat Rusts, an Atlas of Resistance Genes. (Australia: CSIRO Publications).
40. Michael Weaver, L., Swiderski, M.R., Li, Y., and Jones, J.D. (2006). The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant J. 47: 829-840.
41. Mindrinos, M., Katagiri, F., Yu, G.L., and Ausubel, F.M. (1994). The thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099.
42. A. Motlagh, H.N., Wrabl, J.O., Li, J., and Hilser, V.J. (2014). The ensemble nature of allostery. Nature 508: 331-339.
43. Ogura, Y., Inohara, N., Benito, A., Chen, F.F., Yamaoka, S., and Nunez, G. (2001). Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-kappaB. J. Biol. Chem. 276: 4812-4818.
44. Qi, D., DeYoung, B.J., and Innes, R.W. (2012). Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol. 158: 1819-1832.
45. Qi, S., et al. (2010). Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4. Cell 141: 446-457.
46. Rairdan, G.J., and Moffett, P. (2006). Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18: 2082-2093.
47. Ravensdale, M., Bernoux, M., Ve, T., Kobe, B., Thrall, P.H., Ellis, J.G., and Dodds, P.N. (2012). Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathog. 8: e1003004.
48. Reubold, T.F., Wohlgemuth, S., and Eschenburg, S. (2009). A new model for the transition of APAF-1 from inactive monomer to cas-pase-activating apoptosome. J. Biol. Chem. 284: 32717-32724.
49. Reubold, T.F., Wohlgemuth, S., and Eschenburg, S. (2011). Crystal structure of full-length Apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis. Structure 19: 1074-1083.
50. Riedl, S.J., Li, W., Chao, Y., Schwarzenbacher, R., and Shi, Y. (2005). Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 434: 926-933.
51. Schmidt, S.A., Williams, S.J., Wang, C.I., Sornaraj, P., James, B., Kobe, B., Dodds, P.N., Ellis, J.G., and Anderson, P.A. (2007). Purification of the M flax-rust resistance protein expressed in Pichia pastoris. Plant J. 50: 1107-1117.
52. Segretin, M.E., Pais, M., Franceschetti, M., Chaparro-Garcia, A., Bos, J.I., Banfield, M.J., and Kamoun, S. (2014). Single amino acid An Equilibrium-Based Model for TIR-NLR Activation 159 mutations in the potato immune receptor R3a expand response to Phytophthora effectors. Mol. Plant Microbe Interact. 27: 624-637.
53. Slootweg, E.J., Spiridon, L.N., Roosien, J., Butterbach, P., Pomp, R., Westerhof, L., Wilbers, R., Bakker, E., Bakker, J., Petrescu, A.J., Smant, G., and Goverse, A. (2013). Structural determinants at the interface of the ARC2 and leucine-rich repeat domains control the activation of the plant immune receptors Rx1 and Gpa2. Plant Physiol. 162: 1510-1528.
54. Steinbrenner, A.D., Goritschnig, S., and Staskawicz, B.J. (2015). Recognition and activation domains contribute to allele-specific responses of an Arabidopsis NLR receptor to an oomycete effector protein. PLoS Pathog. 11: e1004665.
55. Stirnweis, D., Milani, S.D., Jordan, T., Keller, B., and Brunner, S. (2014). Substitutions of two amino acids in the nucleotide-binding site domain of a resistance protein enhance the hypersensitive response and enlarge the PM3F resistance spectrum in wheat. Mol. Plant Microbe Interact. 27: 265-276.
56. Swiderski, M.R., Birker, D., and Jones, J.D. (2009). 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.
57. Takken, F.L., Albrecht, M., and Tameling, W.I. (2006). Resistance proteins: molecular switches of plant defence. Curr. Opin. Plant Biol. 9: 383-390.
58. Takken, F.L., and Goverse, A. (2012). How to build a pathogen detector: structural basis of NB-LRR function. Curr. Opin. Plant Biol. 15: 375-384.
59. Tameling, W.I., Elzinga, S.D., Darmin, P.S., Vossen, J.H., Takken, F.L., Haring, M.A., and Cornelissen, B.J. (2002). The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14: 2929-2939.
60. Tameling, W.I., Vossen, J.H., Albrecht, M., Lengauer, T., Berden, J.A., Haring, M.A., Cornelissen, B.J., and Takken, F.L. (2006). Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol. 140: 1233-1245.
61. Tang, C., Schwieters, C.D., and Clore, G.M. (2007). Open-to-closed transition in apo maltose-binding protein observed by paramagnetic NMR. Nature 449: 1078-1082.
62. Ueda, H., Yamaguchi, Y., and Sano, H. (2006). Direct interaction between the tobacco mosaic virus helicase domain and the ATP- bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol. Biol. 61: 31-45.
63. van der Biezen, E.A., and Jones, J.D. (1998). The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8: R226-R227.
64. van Ooijen, G., Mayr, G., Kasiem, M.M., Albrecht, M., Cornelissen, B.J., and Takken, F.L. (2008). Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J. Exp. Bot. 59: 1383-1397.
65. Wang, C.I., et al. (2007). Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 19: 2898-2912.
66. Wang, G.F., Ji, J., El-Kasmi, F., Dangl, J.L., Johal, G., and Balint-Kurti, P.J. (2015). Molecular and functional analyses of a maize autoactive NB-LRR protein identify precise structural requirements for activity. PLoS Pathog. 11: e1004674.
67. Whitham, S., Dinesh-Kumar, S.P., Choi, D., Hehl, R., Corr, C., and Baker, B. (1994). The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78: 1101-1115.
68. Williams, S.J., Sornaraj, P., deCourcy-Ireland, E., Menz, R.I., Kobe, B., Ellis, J.G., Dodds, P.N., and Anderson, P.A. (2011). An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. Mol. Plant Microbe Interact. 24: 897-906.
69. Williams, S.J., et al. (2014). Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344: 299-303.