LRR conservation mapping to predict functional sites within protein leucine-rich repeat domains

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Helft, Laura ^a   Reddy, Vignyan ^b   Chen, Xiyang ^a,e   Koller, Teresa ^a   Federici, Luca ^c   Fernández Recio, Juan ^d   Gupta, Rishabh ^b   Bent, Andrew ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Madison   (United States)

^c UNIVERSITY OF CHIETI   (Italy)

^d BARCELONA SUPERCOMPUTING CENTER   (Spain)

^e Purdue University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; EF TU RECEPTOR; FLAGELLIN SENSING 2 RECEPTOR; LEUCINE RICH REPEAT DOMAIN PROTEIN; MICROBE ASSOCIATED MOLECULAR PATTERN RECEPTOR; UNCLASSIFIED DRUG; EFR PROTEIN, ARABIDOPSIS; FLS2 PROTEIN, ARABIDOPSIS; LEUCINE RICH REPEAT PROTEINS; LEUCINE-RICH REPEAT PROTEINS; LIGAND; PATTERN RECOGNITION RECEPTOR; PGIP PROTEIN, PLANT; PROTEIN; PROTEIN KINASE; VEGETABLE PROTEIN;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BINDING SITE; COMPUTER PREDICTION; COMPUTER PROGRAM; CONTROLLED STUDY; IN VIVO STUDY; LEUCINE RICH REPEAT DOMAIN; LIGAND BINDING; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MOLECULAR DOCKING; NONHUMAN; PROTEIN DOMAIN; REPEAT CONSERVATION MAPPING; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; STRUCTURAL BIOINFORMATICS; VALIDATION PROCESS; WEB BROWSER; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REPRODUCIBILITY; X RAY CRYSTALLOGRAPHY;

ANIMALIA; ARABIDOPSIS THALIANA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PLANT PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN KINASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECEPTORS, PATTERN RECOGNITION; REPETITIVE SEQUENCES, AMINO ACID; REPRODUCIBILITY OF RESULTS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 79960613863     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021614     Document Type: Article

References (90)

1. Kobe B, Kajava AV, (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732.
2. Schmitz-Linneweber C, Small I, (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: 663-670.
3. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY, (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13: 1435-1448.
4. Finn R, Mistry J, Tate J, Coggill P, Heger A, et al. (2009) The Pfam protein families database. Nucl Acids Res 38: D211-222.
5. Sigrist C, Cerutti L, De Castro E, Langendijk-Genevaux P, Bulliard V, et al. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucl Acids Res 38: D161-166.
6. Napier R, (2004) Plant hormone binding sites. Annals Botany 93: 227-233.
7. Mercer A, Fleming S, Ueda N, (2005) F-box-like domains are present in most poxvirus ankyrin repeat proteins. Virus Genes 31: 127-133.
8. Van Loy T, Vandersmissen H, Van Hiel M, Poels J, Verlinden H, et al. (2008) Comparative genomics of leucine-rich repeats containing G protein-coupled receptors and their ligands. General Comparative Endocrinology 155: 14-21.
9. Shanmugam V, (2005) Role of extracytoplasmic leucine rich repeat proteins in plant defence mechanisms. Microbiol Res 160: 83-94.
10. Padmanabhan M, Cournoyer P, Dinesh-Kumar SP, (2009) The leucine-rich repeat domain in plant innate immunity: a wealth of possibilities. Cell Microbiol 11: 191-198.
11. Eitas TK, Dangl JL, (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13: 472-477.
12. Herrin BR, Cooper MD, (2010) Alternative adaptive immunity in jawless vertebrates. J Immunol 185: 1367-1374.
13. Tasumi S, Velikovsky CA, Xu G, Gai SA, Wittrup KD, et al. (2009) High-affinity lamprey VLRA and VLRB monoclonal antibodies. Proc Natl Acad Sci U S A 106: 12891-12896.
14. Velikovsky CA, Deng L, Tasumi S, Iyer LM, Kerzic MC, et al. (2009) Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen. Nature Struct and Mol Biol 16: 725-730.
15. Bella J, Hindle KL, McEwan PA, Lovell SC, (2008) The leucine-rich repeat structure. Cell Mol Life Sci 65: 2307-2333.
16. Kajander T, Cortajarena AL, Regan L, (2006) Consensus design as a tool for engineering repeat proteins. Methods Mol Biol 340: 151-170.
17. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
18. Boller T, Felix G, (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
19. Nicaise V, Roux M, Zipfel C, (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150: 1638-1647.
20. Schwessinger B, Zipfel C, (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11: 389-395.
21. Shiu SH, Bleecker AB, (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132: 530-543.
22. Torii KU, (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234: 1-46.
23. Morillo SA, Tax FE, (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9: 460-469.
24. Takeda K, Akira S, (2005) Toll-like receptors in innate immunity. Int Immunol 17: 1-14.
25. Ye Z, Ting J, (2008) NLR, the nucleotide-binding domain leucine-rich repeat containing gene family. Curr Opin Immunol 20: 3-9.
26. Rafiqi M, Bernoux M, Ellis J, Dodds P, (2009) In the trenches of plant pathogen recognition: Role of NB-LRR proteins. Semin Cell Dev Biol 20: 1017-1024.
27. Shaw M, Reimer T, Kim Y, Nuñez G, (2008) NOD-like receptors (NLRs): bona fide intracellular microbial sensors. Curr Opinion Immunol 20: 377-382.
28. Proell M, Riedl S, Fritz J, Rojas A, Schwarzenbacher R, (2008) The Nod-like receptor (NLR) family: a tale of similarities and differences. PLoS ONE 3: e2119.
29. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276.
30. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, et al. (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496-3507.
31. Gómez-Gómez L, Boller T, (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011.
32. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, et al. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.
33. Chinchilla D, Boller T, Robatzek S, (2007) Flagellin signalling in plant immunity. Curr Topics Innate Immunity pp. 358-371.
34. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G, (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465-476.
35. Dunning FM, Sun W, Jansen KL, Helft L, Bent AF, (2007) Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. Plant Cell 19: 3297-3313.
36. Albert M, Jehle AK, Mueller K, Eisele C, Lipschis M, et al. (2010) Arabidopsis thaliana pattern recognition receptors for bacterial elongation factor Tu and flagellin can be combined to form functional chimeric receptors. J Biol Chem 285: 19035-19042.
37. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.
38. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, et al. (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnology 28: 365-369.
39. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, et al. (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481.
40. Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, et al. (2010) Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J 64: 343-354.
41. Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, et al. (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci U S A 101: 15811-15816.
42. Forsyth A, Mansfield J, Grabov N, Sinapidou E, de Torres M, et al. (2010) Genetic Dissection of Basal Resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol Plant-Microbe Interactions 23: 1545-1552.
43. Zhou L, Cheung M, Zhang Q, Lei C, Zhang S, et al. (2009) A novel simple extracellular leucine-rich repeat (eLRR) domain protein from rice (OsLRR1) enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1. Plant Cell Environm 32: 1804-1820.
44. Suzuki Y, (2004) Three-dimensional window analysis for detecting positive selection at structural regions of proteins. Mol Biol Evol 21: 2352-2359.
45. Innis CA, Anand AP, Sowdhamini R, (2004) Prediction of functional sites in proteins using conserved functional group analysis. J Mol Biol 337: 1053-1068.
46. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
47. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, et al. (2002) The Pfam protein families database. Nucl Acids Res 30: 276-280.
48. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, et al. (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91: 821-832.
49. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucl Acids Res 38: W529-533.
50. Fernández-Recio J, Totrov M, Skorodumov C, Abagyan R, (2005) Optimal docking area: a new method for predicting protein-protein interaction sites. Proteins Struct Function Bioinformatics 58: 134-143.
51. Wilbur W, Lipman D, (1983) Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A 80: 726-730.
52. Myers E, Miller W, (1988) Optimal alignments in linear space. Comput Appl Biosci 4: 11-17.
53. Dolan J, Walshe K, Alsbury S, Hokamp K, O'Keeffe S, et al. (2007) The extracellular leucine-rich repeat superfamily; a comparative survey and analysis of evolutionary relationships and expression patterns. BMC Genomics 8: 320-343.
54. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
55. Casasoli M, Federici L, Spinelli F, Di Matteo A, Vella N, et al. (2009) Integration of evolutionary and desolvation energy analysis identifies functional sites in a plant immunity protein. Proc Natl Acad Sci U S A 106: 7666-7671.
56. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, et al. (2003) The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci U S A 100: 10124-10128.
57. van der Hoorn RA, Wulff BB, Rivas S, Durrant MC, van der Ploeg A, et al. (2005) Structure-function analysis of Cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17: 1000-1015.
58. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
59. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
60. Laskowski RA, Moss DS, Thornton JM, (1993) Main-chain bond lengths and bond angles in protein structures. J Mol Biol 231: 1049-1067.
61. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41.
62. Adams-Phillips L, Briggs AG, Bent AF, (2009) Disruption of poly(ADP-ribosyl)ation mechanisms alters responses of Arabidopsis to biotic stress. Plant Physiol 152: 267-280.
63. Gómez-Gómez L, Felix G, Boller T, (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284.
64. D'ovidio R, Raiola A, Capodicasa C, Devoto A, Pontiggia D, et al. (2004) Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol 135: 2424-2435.
65. Leckie F, Mattei B, Capodicasa C, Hemmings A, Nuss L, et al. (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed beta-strand/beta-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J 18: 2352-2363.
66. Papageorgiou AC, Shapiro R, Acharya KR, (1997) Molecular recognition of human angiogenin by placental ribonuclease inhibitor-an X-ray crystallographic study at 2.0 A resolution. EMBO J 16: 5162-5177.
67. Kobe B, Deisenhofer J, (1996) Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A. J Mol Biol 264: 1028-1043.
68. Tan X, Calderon-Villalobos L, Sharon M, Zheng C, Robinson C, et al. (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446: 640-645.
69. Fan Q, Hendrickson W, (2005) Structure of human follicle-stimulating hormone in complex with its receptor. Nature 433: 269-277.
70. Celikel R, McClintock R, Roberts J, Mendolicchio G, Ware J, et al. (2003) Modulation of α-thrombin function by distinct interactions with platelet glycoprotein Ibα. Science 301: 218-221.
71. Hao B, Zheng N, Schulman BA, Wu G, Miller JJ, et al. (2005) Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase. Mol Cell 20: 9-19.
72. Morlot C, Thielens N, Ravelli R, Hemrika W, Romijn R, et al. (2007) Structural insights into the Slit-Robo complex. Proc Natl Acad Sci U S A 104: 14923-14928.
73. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, et al. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130: 1071-1082.
74. Kang J, Nan X, Jin M, Youn S, Ryu Y, et al. (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31: 873-884.
75. Park B, Song D, Kim H, Choi B, Lee H, et al. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458: 1191-1195.
76. Liu L, Botos I, Wang Y, Leonard J, Shiloach J, et al. (2008) Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320: 379-381.
77. Dickson K, Haigis M, Raines R, (2005) Ribonuclease inhibitor: structure and function. Prog Nucl Acid Res Mol Biol 80: 349-374.
78. Dharmasiri N, Dharmasiri S, Estelle M, (2005) The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
79. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, et al. (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9: 109-119.
80. Kepinski S, Leyser O, (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
81. Walsh T, Neal R, Merlo A, Honma M, Hicks G, et al. (2006) Mutations in an auxin receptor homolog AFB5 and in SGT1b confer resistance to synthetic picolinate auxins and not to 2, 4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis. Plant Physiol 142: 542-552.
82. Zipfel C, (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12: 414-420.
83. Couvreur TL, Franzke A, Al-Shehbaz IA, Bakker FT, Koch MA, et al. (2010) Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol 27: 55-71.
84. Federici L, Di Matteo A, Fernández-Recio J, Tsernoglou D, Cervone F, (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 11: 65-70.
85. Sicilia F, Fernández-Recio J, Caprari C, De Lorenzo G, Tsernoglou D, et al. (2005) The polygalacturonase-inhibiting protein PGIP2 of Phaseolus vulgaris has evolved a mixed mode of inhibition of endopolygalacturonase PG1 of Botrytis cinerea. Plant Physiol 139: 1380-1388.
86. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, et al. (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 U S A 103: 8888-8893.
87. Krasileva KV, Dahlbeck D, Staskawicz BJ, (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.
88. Clark LB, Viswanathan P, Quigley G, Chiang YC, McMahon JS, et al. (2004) Systematic mutagenesis of the leucine-rich repeat (LRR) domain of CCR4 reveals specific sites for binding to CAF1 and a separate critical role for the LRR in CCR4 deadenylase activity. J Biol Chem 279: 13616-13623.
89. Häweker H, Rips S, Koiwa H, Salomon S, Saijo Y, et al. (2010) Pattern recognition receptors require N-glycosylation to mediate plant immunity. J Biol Chem 285: 4629-4636.
90. Binz H, Stumpp M, Forrer P, Amstutz P, Plückthun A, (2003) Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J Mol Biol 332: 489-503.