Diversity and variability of NOD-like receptors in fungi

Genome Biology and Evolution

Volumn 6, Issue 12, 2014, Pages 3137-3158

  Dyrka, Witold ^a   Lamacchia, Marina ^a   Durrens, Pascal ^a   Kobe, Bostjan ^b   Daskalov, Asen ^a   Paoletti, Matthieu ^a   Sherman, David J ^a   Saupe, Sven J ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Fungi; Immunity; NACHT; NLR

Indexed keywords

CELL SURFACE RECEPTOR; FUNGAL PROTEIN;

AMINO ACID SEQUENCE; CHEMISTRY; FUNGAL GENOME; FUNGUS; GENETIC POLYMORPHISM; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; FUNGI; GENOME, FUNGAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE;

EID: 84924047678     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu251     Document Type: Article

References (107)

1. Alaidarous M, et al. 2014. Mechanism of bacterial interference with TLR4 signaling by Brucella Toll/interleukin-1 receptor domain-containing protein TcpB. J Biol Chem. 289:654-668.
2. Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Asplund-Samuelsson J, Bergman B, Larsson J. 2012. Prokaryotic caspase homologs: phylogenetic patterns and functional characteristics reveal considerable diversity. PLoS One 7:e49888.
4. Atkinson GC, Tenson T, Hauryliuk V. 2011. The RelA/SpoT homolog (RSH) superfamily: distribution and functional evolution of ppGpp synthetases and hydrolases across the tree of life. PLoS One 6:e23479.
5. Ausubel FM. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6:973-979.
6. Bastiaans E, et al. 2014. Natural variation of heterokaryon incompatibility gene het-c in Podospora anserina reveals diversifying selection. Mol Biol Evol. 31:962-974.
7. Bidard F, Clave C, Saupe SJ. 2013. The transcriptional response to nonself in the fungus Podospora anserina. G3 3:1015-1030.
8. Blackwell M. 2011. The fungi: 1, 2, 3... 5.1 million species? Am J Bot 98:426-438.
9. Bleuler-Martinez S, et al. 2011. A lectin-mediated resistance of higher fungi against predators and parasites. Mol Ecol. 20:3056-3070.
10. Bonardi V, Cherkis K, Nishimura MT, Dangl JL. 2012. A new eye on NLR proteins: focused on clarity or diffused by complexity? Curr Opin Immunol 24:41-50.
11. Boutte CC, Crosson S. 2013. Bacterial lifestyle shapes stringent response activation. Trends Microbiol. 21:174-180.
12. Burmester A, et al. 2011. Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol. 12:R7.
13. Cacas JL, et al. 2009. A novel patatin-like protein from cotton plant, GhPat1, is co-expressed with GhLox1 during Xanthomonas campestris-mediated hypersensitive cell death. Plant Cell Rep. 28:155-164.
14. Cai X, et al. 2014. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell 156:1207-1222.
15. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972-1973.
16. Chan SL, et al. 2009. Molecular mimicry in innate immunity: crystal structure of a bacterial TIR domain. J Biol Chem. 284:21386-21392.
17. Chevanne D, et al. 2009. Identification of the het-r vegetative incompatibility gene of Podospora anserina as a member of the fast evolving HNWD gene family. Curr Genet. 55:93-102.
18. Chevanne D, Saupe SJ, Clave C, Paoletti M. 2010. WD-repeat instability and diversification of the Podospora anserina hnwd non-self recognition gene family. BMC Evol Biol. 10:134.
19. Chevenet F, Brun C, Banuls AL, Jacq B, Christen R. 2006. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439.
20. Choi GH, et al. 2012. Molecular characterization of vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus Cryphonectria parasitica. Genetics 190:113-127.
21. Chu H, Mazmanian SK. 2013. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat Immunol. 14:668-675.
22. Corbalan-Garcia S, Gomez-Fernandez JC. 2014. Signaling through C2 domains: more than one lipid target. Biochim Biophys Acta. 1838:1536-1547.
23. Danot O, Marquenet E, Vidal-Ingigliardi D, Richet E. 2009. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure 17:172-182.
24. Daskalov A, Paoletti M, Ness F, Saupe SJ. 2012. Genomic clustering and homology between HET-S and the NWD2 STAND protein in various fungal genomes. PLoS One 7:e34854.
25. Dereeper A, et al. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-469.
26. Druzhinina IS, et al. 2011. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol. 9:749-759.
27. Durbin R, Eddy SR, Krogh A, Mitchison G. 1998. Biological sequence analysis. Probabilistic models of proteins and nucleic acids. Cambridge (United Kingdom): Cambridge University Press.
28. Eddy SR. 2011. Accelerated profile HMM searches. PLoS Comput Biol. 7:e1002195.
29. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
30. Fedorova ND, et al. 2008. Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet. 4:e1000046.
31. Finn RD, et al. 2014. Pfam: the protein families database. Nucleic Acids Res. 42:D222-230.
32. Gansner ER, North SC. 2000. An open graph visualization system and its applications to software engineering. Soft Pract Exp. 30:1203-1233.
33. Graziani S, Silar P, Daboussi MJ. 2004. Bistability and hysteresis of the 'Secteur' differentiation are controlled by a two-gene locus in Nectria haematococca. BMC Biol. 2:18.
34. Greenwald J, et al. 2010. The mechanism of prion inhibition by HET-S. Mol Cell. 38:889-899.
35. Grigoriev IV, et al. 2014. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 42:D699-D704.
36. Guindon S, et al. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59:307-321.
37. Hamada M, et al. 2013. The complex NOD-like receptor repertoire of the coral Acropora digitifera includes novel domain combinations. Mol Biol Evol. 30:167-176.
38. He D, et al. 2014. An alternative root for the eukaryote tree of life. Curr Biol. 24:465-470.
39. Heger A, Holm L. 2000. Rapid automatic detection and alignment of repeats in protein sequences. Proteins 41:224-237.
40. Hulsen T, De Vlieg J, Alkema W. 2008. BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488.
41. Iotti M, et al. 2012. Self/nonself recognition in Tuber melanosporum is not mediated by a heterokaryon incompatibility system. Fungal Biol. 116:261-275.
42. Jacob F, Vernaldi S, Maekawa T. 2013. Evolution and conservation of plant NLR functions. Front Immunol. 4:297.
43. Javadi Y, Itzhaki LS. 2013. Tandem-repeat proteins: regularity plus modularity equals design-ability. Curr Opin Struct Biol. 23:622-631.
44. Jernigan KK, Bordenstein SR. 2014. Ankyrin domains across the tree of life. PeerJ. 2:e264.
45. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323-329.
46. Jorda J, Kajava AV. 2009. T-REKS: identification of Tandem REpeats in sequences with a K-meanS based algorithm. Bioinformatics 25:2632-2638.
47. Joshi RK, Nayak S. 2013. Perspectives of genomic diversification and molecular recombination towards-gene evolution in plants. Physiol Mol Biol Plants. 19:1-9.
48. Kadota Y, Shirasu K, Guerois R. 2010. NLR sensors meet at the SGT1-HSP90 crossroad. Trends Biochem Sci. 35:199-207.
49. Kanneganti TD, Lamkanfi M, Nunez G. 2007. Intracellular NOD-like receptors in host defense and disease. Immunity 27:549-559.
50. Kaplan-Turkoz B, et al. 2013. Structure of the Toll/interleukin 1 receptor (TIR) domain of the immunosuppressive Brucella effector BtpA/Btp1/TcpB. FEBS Lett. 587:3412-3416.
51. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 30:772-780.
52. Kim DS, Jeun Y, Hwang BK. 2014. The pepper patatin-like phospholipase CaPLP1 functions in plant cell death and defense signaling. Plant Mol Biol. 84:329-344.
53. Koonin EV, Aravind L. 2000. The NACHT family - a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci. 25:223-224.
54. Kubicek CP, et al. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12:R40.
55. La Camera S, et al. 2009. The Arabidopsis patatin-like protein 2 (PLP2) plays an essential role in cell death execution and differentially affects biosynthesis of oxylipins and resistance to pathogens. Mol Plant Microbe Interact. 22:469-481.
56. Lange C, et al. 2011. Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol Biol Evol. 28:1687-1702.
57. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
58. Leipe DD, Koonin EV, Aravind L. 2004. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol. 343:1-28.
59. Leveau JH, Preston GM. 2008. Bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol. 177:859-876.
60. Lu A, et al. 2014. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 156:1193-1206.
61. Maekawa T, Kufer TA, Schulze-Lefert P. 2011. NLR functions in plant and animal immune systems: so far and yet so close. Nat Immunol. 12:817-826.
62. Martin F, et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88-92.
63. Mathur V, Seuring C, Riek R, Saupe SJ, Liebman SW. 2012. Localization of HET-S to the cell periphery, not to [Het-s] aggregates, is associated with [Het-s]-HET-S toxicity. Mol Cell Biol. 32:139-153.
64. Messier-Solek C, Buckley KM, Rast JP. 2010. Highly diversified innate receptor systems and new forms of animal immunity. Semin Immunol. 22:39-47.
65. O'Neill LA, Bowie AG. 2007. The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat Rev Immunol. 7:353-364.
66. Pagani I, et al. 2012. The Genomes OnLine Database (GOLD) v. 4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res. 40:D571-579.
67. Palsson-McDermott EM, O'Neill LA. 2007. Building an immune system from nine domains. Biochem Soc Trans. 35:1437-1444.
68. Paoletti M, Castroviejo M, Begueret J, Clave C. 2001. Identification and characterization of a gene encoding a subtilisin-like serine protease induced during the vegetative incompatibility reaction in Podospora anserina. Curr Genet. 39:244-252.
69. Paoletti M, Clave C. 2007. The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryot Cell. 6:2001-2008.
70. Paoletti M, Saupe SJ. 2009. Fungal incompatibility: evolutionary origin in pathogen defense? Bioessays 31:1201-1210.
71. Paoletti M, Saupe SJ, Clave C. 2007. Genesis of a fungal non-self recognition repertoire. PLoS One 2:e283.
72. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
73. Parveen N, Cornell KA. 2011. Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism. Mol Microbiol. 79:7-20.
74. Pearson MN, Beever RE, Boine B, Arthur K. 2009. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol. 10:115-128.
75. Petnicki-Ocwieja T, et al. 2009. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A. 106:15813-15818.
76. Pinan-Lucarre B, Paoletti M, Clave C. 2007. Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol. 17:101-111.
77. Pond SL, Frost SD. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531-2533.
78. Pond SL, Frost SD, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
79. Porollo AA, Adamczak R, Meller J. 2004. POLYVIEW: a flexible visualization tool for structural and functional annotations of proteins. Bioinformatics 20:2460-2462.
80. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16:276-277.
81. Sabotic J, et al. 2012. Structural basis of trypsin inhibition and entomotoxicity of cospin, serine protease inhibitor involved in defense of Coprinopsis cinerea fruiting bodies. J Biol Chem. 287:3898-3907.
82. Saleh M. 2011. The machinery of Nod-like receptors: refining the paths to immunity and cell death. Immunol Rev. 243:235-246.
83. Saupe S, Turcq B, Begueret J. 1995. A gene responsible for vegetative incompatibility in the fungus Podospora anserina encodes a protein with a GTP-binding motif and G beta homologous domain. Gene 162:135-139.
84. Saupe SJ, Daskalov A. 2012. The [Het-s] Prion, an amyloid fold as a cell death activation trigger. PLoS Pathog. 8:e1002687.
85. Scheffler K, Martin DP, Seoighe C. 2006. Robust inference of positive selection from recombining coding sequences. Bioinformatics 22:2493-2499.
86. Schliep KP. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27:592-593.
87. Selker EU. 1990. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet. 24:579-613.
88. Seuring C, et al. 2012. The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLoS Biol. 10:e1001451.
89. Sievers F, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 7:539.
90. Siozios S, et al. 2013. The diversity and evolution of Wolbachia ankyrin repeat domain genes. PLoS One 8:e55390.
91. Smith ML, et al. 2000. Vegetative incompatibility in the het-6 region of Neurospora crassa is mediated by two linked genes. Genetics 155:1095-1104.
92. Snyder GA, et al. 2014. Crystal structures of the Toll/Interleukin-1 receptor (TIR) domains from the Brucella protein TcpB and host adaptor TIRAP reveal mechanisms of molecular mimicry. J Biol Chem. 289:669-679.
93. Soanes DM, Talbot NJ. 2010. Comparative genome analysis reveals an absence of leucine-rich repeat pattern-recognition receptor proteins in the kingdom Fungi. PLoS One 5:e12725.
94. Soding J, Remmert M, Biegert A, Lupas AN. 2006. HHsenser: exhaustive transitive profile search using HMM-HMM comparison. Nucleic Acids Res. 34:W374-378.
95. Stein C, Caccamo M, Laird G, Leptin M. 2007. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol. 8:R251.
96. Stirnimann CU, Petsalaki E, Russell RB, Muller CW. 2010. WD40 proteins propel cellular networks. Trends Biochem Sci. 35:565-574.
97. Tamura K, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739.
98. Thompson JD, Plewniak F, Ripp R, Thierry JC, Poch O. 2001. Towards a reliable objective function for multiple sequence alignments. J Mol Biol. 314:937-951.
99. Van Der Gaag M, Debets AJ, Osiewacz HD, Hoekstra RF. 1998. The dynamics of pAL2-1 homologous linear plasmids in Podospora anserina. Mol Gen Genet. 258:521-529.
100. Van Der Nest MA, et al. 2014. Distribution and evolution of het gene homologs in the basidiomycota. Fungal Genet Biol. 64:45-57.
101. Veneault-Fourrey C, Martin F. 2011. Mutualistic interactions on a knifeedge between saprotrophy and pathogenesis. Curr Opin Plant Biol. 14:444-450.
102. Wortmann SB, et al. 2012. Mutations in the phospholipid remodeling gene SERAC1 impair mitochondrial function and intracellular cholesterol trafficking and cause dystonia and deafness. Nat Genet. 44:797-802.
103. Wu H. 2013. Higher-order assemblies in a new paradigm of signal transduction. Cell 153:287-292.
104. Xue JY, et al. 2012. A primary survey on bryophyte species reveals two novel classes of nucleotide-binding site (NBS) genes. PLoS One 7:e36700.
105. Yue JX, Meyers BC, Chen JQ, Tian D, Yang S. 2012. Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol. 193:1049-1063.
106. Yuen B, Bayes JM, Degnan SM. 2014. The characterization of sponge nlrs provides insight into the origin and evolution of this innate immune gene family in animals. Mol Biol Evol. 31:106-120.
107. Zuccaro A, et al. 2011. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Pi. indica. PLoS Pathog. 7:e1002290.