Horizontal Transfer of a Subtilisin Gene from Plants into an Ancestor of the Plant Pathogenic Fungal Genus Colletotrichum

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Armijos Jaramillo, Vinicio Danilo ^a   Vargas, Walter Alberto ^a   Sukno, Serenella Ana ^a   Thon, Michael R ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; SUBTILISIN;

ARTICLE; COLLETOTRICHUM; CONTROLLED STUDY; FUNGAL GENE; FUNGAL GENOME; FUNGAL PLANT DISEASE; GENE EXPRESSION REGULATION; GENE STRUCTURE; GENE TRANSFER; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC LINE; GENETIC SIMILARITY; GLOMERELLA CINGULATA; GLOMERELLA GRAMINICOLA; MAIZE; MOLECULAR MIMICRY; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT FUNGUS INTERACTION; PLANT GENE; SEQUENCE ALIGNMENT; SUBTILISIN GENE;

AMINO ACID SEQUENCE; COLLETOTRICHUM; GENE EXPRESSION; GENE TRANSFER, HORIZONTAL; HOST-PATHOGEN INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANTS; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE ALIGNMENT; SUBTILISIN;

EID: 84875024755     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059078     Document Type: Article

References (90)

1. Latunde-Dada AO, (2001) Colletotrichum: tales of forcible entry, stealth, transient confinement and breakout. Mol Plant Pathol 2: 187-198 doi:10.1046/j.1464-6722.2001.00069.x.
2. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, et al. (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44: 1060-1065 doi:10.1038/ng.2372.
3. Perfect SE, Green JR, (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2: 101-108 doi:10.1046/j.1364-3703.2001.00055.x.
4. Takano Y, (2004) Molecular genetic studies on infection mechanism in Colletotrichum lagenarium. J Gen Plant Pathol 70: 390-390 doi:10.1007/s10327-004-0147-2.
5. Dunaevsky YE, Matveeva AR, Beliakova GA, Domash VI, Belozersky MA, (2007) Extracellular alkaline proteinase of Colletotrichum gloeosporioides. Biochemistry Mosc 72: 345-350.
6. Kleemann J, Takahara H, Stüber K, O'Connell R, (2008) Identification of soluble secreted proteins from appressoria of Colletotrichum higginsianum by analysis of expressed sequence tags. Microbiology 154: 1204-1217 doi:10.1099/mic.0.2007/014944-0.
7. Siezen RJ, De Vos WM, Leunissen JA, Dijkstra BW, (1991) Homology modelling and protein engineering strategy of subtilases, the family of subtilisin-like serine proteinases. Protein Eng 4: 719-737.
8. Withers-Martinez C, Suarez C, Fulle S, Kher S, Penzo M, et al. (2012) Plasmodium subtilisin-like protease 1 (SUB1): insights into the active-site structure, specificity and function of a pan-malaria drug target. Int J Parasitol 42: 597-612 doi:10.1016/j.ijpara.2012.04.005.
9. Rawlings ND, Barrett AJ, Bateman A, (2011) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucl Acids Res 40: D343-D350 doi:10.1093/nar/gkr987.
10. Siezen RJ, Leunissen JA, (1997) Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci 6: 501-523.
11. Tripathi LP, Sowdhamini R, (2006) Cross genome comparisons of serine proteases in Arabidopsis and rice. BMC Genomics 7: 200 doi:10.1186/1471-2164-7-200.
12. Van Loon L, Pierpoint W, Boller T, Conejero V, (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12: 245-264 doi:10.1007/BF02668748.
13. Tornero P, Conejero V, Vera P, (1996) Primary structure and expression of a pathogen-induced protease (PR-P69) in tomato plants: Similarity of functional domains to subtilisin-like endoproteases. Proc Natl Acad Sci USA 93: 6332-6337.
14. Tornero P, Conejero V, Vera P, (1997) Identification of a new pathogen-induced member of the subtilisin-like processing protease family from plants. J Biol Chem 272: 14412-14419.
15. Jorda L, Coego A, Conejero V, Vera P, (1999) A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J Biol Chem 274: 2360-2365.
16. Muszewska A, Taylor JW, Szczesny P, Grynberg M, (2011) Independent subtilases expansions in fungi associated with animals. Mol Biol Evol 28: 3395-3404 doi:10.1093/molbev/msr176.
17. Saeki K, Okuda M, Hatada Y, Kobayashi T, Ito S, et al. (2000) Novel oxidatively stable subtilisin-like serine proteases from alkaliphilic Bacillus spp.: enzymatic properties, sequences, and evolutionary relationships. Biochem Biophys Res Commun 279: 313-319 doi:10.1006/bbrc.2000.3931.
18. Bryant MK, Schardl CL, Hesse U, Scott B, (2009) Evolution of a subtilisin-like protease gene family in the grass endophytic fungus Epichloë festucae. BMC Evol Biol 9: 168 doi:10.1186/1471-2148-9-168.
19. Ochman H, Lawrence JG, Groisman EA, (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304 doi:10.1038/35012500.
20. Dutta C, Pan A, (2002) Horizontal gene transfer and bacterial diversity. J Biosci 27: 27-33.
21. Heuer H, Smalla K, (2007) Horizontal gene transfer between bacteria. Environ Biosafety Res 6: 3-13 doi:10.1051/ebr:2007034.
22. Kim SE, Moon JS, Choi WS, Lee SH, Kim SU, (2012) Monitoring of horizontal gene transfer from agricultural microorganisms to soil bacteria and analysis of microbial community in soils. J Microbiol Biotechnol 22: 563-566.
23. Techtmann SM, Lebedinsky AV, Colman AS, Sokolova TG, Woyke T, et al. (2012) Evidence for horizontal gene transfer of anaerobic carbon monoxide dehydrogenases. Front Microbiol 3: 132 doi:10.3389/fmicb.2012.00132.
24. Keeling PJ, Palmer JD, (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605-618 doi:10.1038/nrg2386.
25. Fitzpatrick DA, (2011) Horizontal gene transfer in fungi. FEMS Microbiol Lett 329: 1-8 doi:10.1111/j.1574-6968.2011.02465.x.
26. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, et al. (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38: 953-956 doi:10.1038/ng1839.
27. Choi I-G, Kim S-H, (2007) Global extent of horizontal gene transfer. Proc Natl Acad Sci USA 104: 4489-4494 doi:10.1073/pnas.0611557104.
28. Slot JC, Rokas A, (2010) Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc Natl Acad Sci USA 107: 10136-10141 doi:10.1073/pnas.0914418107.
29. Tiburcio RA, Costa GGL, Carazzolle MF, Mondego JMC, Schuster SC, et al. (2010) Genes acquired by horizontal transfer are potentially involved in the evolution of phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, two of the major pathogens of cacao. J Mol Evol 70: 85-97 doi:10.1007/s00239-009-9311-9.
30. Rosewich UL, Kistler HC, (2000) Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38: 325-363 doi:10.1146/annurev.phyto.38.1.325.
31. Gogarten JP, (2003) Gene transfer: gene swapping craze reaches eukaryotes. Curr Biol 13: R53-54.
32. De Jonge R, Van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, et al. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109: 5110-5115 doi:10.1073/pnas.1119623109.
33. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, et al. (2009) Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21: 1897-1911 doi:10.1105/tpc.109.065805.
34. Katoh K, Misawa K, Kuma K, Miyata T, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066 doi:10.1093/nar/gkf436.
35. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2011) Geneious v5.5. Available: http://www.geneious.com.
36. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
37. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
38. Schmidt HA, Strimmer K, Vingron M, Von Haeseler A, (2002) TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504 doi:10.1093/bioinformatics/18.3.502.
39. Shimodaira, Hasegawa M, (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246-1247.
40. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2011) GenBank. Nucleic Acids Res 39: D32-37 doi:10.1093/nar/gkq1079.
41. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T, (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973 doi:10.1093/bioinformatics/btp348.
42. Talavera G, Castresana J, (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564-577 doi:10.1080/10635150701472164.
43. Stamatakis A, (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690 doi:10.1093/bioinformatics/btl446.
44. Anisimova M, Gascuel O, (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55: 539-552 doi:10.1080/10635150600755453.
45. Bell CD, Soltis DE, Soltis PS, (2005) The age of the angiosperms: a molecular timescale without a clock. Evolution 59: 1245-1258 doi:10.1111/j.0014-3820.2005.tb01775.x.
46. Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH, (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86: 6201-6205.
47. Chaw S-M, Chang C-C, Chen H-L, Li W-H, (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58: 424-441 doi:10.1007/s00239-003-2564-9.
48. Leebens-Mack J, Raubeson LA, Cui L, Kuehl JV, Fourcade MH, et al. (2005) Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one's way out of the Felsenstein zone. Mol Biol Evol 22: 1948-1963 doi:10.1093/molbev/msi191.
49. Smith SA, Beaulieu JM, Donoghue MJ, (2010) An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Natl Acad Sci USA 107: 5897-5902 doi:10.1073/pnas.1001225107.
50. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-W587 doi:10.1093/nar/gkm259.
51. Petersen TN, Brunak S, Von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786 doi:10.1038/nmeth.1701.
52. Mi H, Dong Q, Muruganujan A, Gaudet P, Lewis S, et al. (2009) PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 38: D204-D210 doi:10.1093/nar/gkp1019.
53. Finn RD, Clements J, Eddy SR, (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37 doi:10.1093/nar/gkr367.
54. Nembaware V, Seoighe C, Sayed M, Gehring C, (2004) A plant natriuretic peptide-like gene in the bacterial pathogen Xanthomonas axonopodis may induce hyper-hydration in the plant host: a hypothesis of molecular mimicry. BMC Evol Biol 4: 10 doi:10.1186/1471-2148-4-10.
55. Ottmann C, Rose R, Huttenlocher F, Cedzich A, Hauske P, et al. (2009) Structural basis for Ca2+-independence and activation by homodimerization of tomato subtilase 3. Proc Natl Acad Sci USA 106: 17223-17228 doi:10.1073/pnas.0907587106.
56. Rose R, Schaller A, Ottmann C, (2010) Structural features of plant subtilases. Plant Signal Behav 5: 180-183.
57. Kelley LA, Sternberg MJE, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371 doi:10.1038/nprot.2009.2.
58. Holm L, Rosenstrom P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-W549 doi:10.1093/nar/gkq366.
59. Schrödinger L (2010) The PyMOL molecular graphics system, Version 1.3r1.
60. Cedzich A, Huttenlocher F, Kuhn BM, Pfannstiel J, Gabler L, et al. (2009) The protease-associated domain and c-terminal extension are required for zymogen processing, sorting within the secretory pathway, and activity of tomato subtilase 3 (SLSBT3). J Biol Chem 284: 14068-14078 doi:10.1074/jbc.M900370200.
61. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, et al. (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56: 181-195 doi:10.1111/j.1365-313X.2008.03590.x.
62. Vargas WA, Martín JMS, Rech GE, Rivera LP, Benito EP, et al. (2012) Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol 158: 1342-1358 doi:10.1104/pp.111.190397.
63. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ, (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 16: 1857-1864 doi:10.1016/j.cub.2006.07.052.
64. Brown JR, (2003) Ancient horizontal gene transfer. Nat Rev Genet 4: 121-132 doi:10.1038/nrg1000.
65. Rolland T, Neuvéglise C, Sacerdot C, Dujon B, (2009) Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes. PLoS ONE 4: e6515 doi:10.1371/journal.pone.0006515.
66. Marcet-Houben M, Gabaldón T, (2010) Acquisition of prokaryotic genes by fungal genomes. Trends Genet 26: 5-8 doi:10.1016/j.tig.2009.11.007.
67. Elde NC, Malik HS, (2009) The evolutionary conundrum of pathogen mimicry. Nature Rev Microbiol 7: 787-797 doi:10.1038/nrmicro2222.
68. Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB, (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci USA 103: 2851-2856 doi:10.1073/pnas.0507892103.
69. Abramovitch RB, Kim Y-J, Chen S, Dickman MB, Martin GB, (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22: 60-69 doi:10.1093/emboj/cdg006.
70. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, et al. (2011) Metabolic priming by a secreted fungal effector. Nature 478: 395-398 doi:10.1038/nature10454.
71. Nakagawa M, Ueyama M, Tsuruta H, Uno T, Kanamaru K, et al. (2010) Functional analysis of the cucumisin propeptide as a potent inhibitor of its mature enzyme. J Biol Chem 285: 29797-29807 doi:10.1074/jbc.M109.083162.
72. Ikemura H, Inouye M, (1988) In vitro processing of pro-subtilisin produced in Escherichia coli. J Biol Chem 263: 12959-12963.
73. Ohta Y, Inouye M, (1990) Pro-subtilisin E: purification and characterization of its autoprocessing to active subtilisin E in vitro. Mol Microbiol 4: 295-304.
74. Bryan P, Wang L, Hoskins J, Ruvinov S, Strausberg S, et al. (1995) Catalysis of a protein folding reaction: Mechanistic implications of the 2.0 ANG. structure of the subtilisin-prodomain complex. Biochemistry 34: 10310-10318 doi:10.1021/bi00032a026.
75. Coffeen WC, Wolpert TJ, (2004) Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16: 857-873 doi:10.1105/tpc.017947.
76. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
77. Broad Institute of Harvard and MIT (n.d.) Colletotrichum Sequencing Project. Available: http://www.broadinstitute.org/. Accessed 27 October 2012.
78. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO, (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6: 29 doi:10.1186/1471-2148-6-29.
79. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2011) The Pfam protein families database. Nucl Acids Res 40: D290-D301 doi:10.1093/nar/gkr1065.
80. Hasegawa H, Holm L, (2009) Advances and pitfalls of protein structural alignment. Curr Opin Struct Biol 19: 341-348 doi:10.1016/j.sbi.2009.04.003.
81. Takeda N, Sato S, Asamizu E, Tabata S, Parniske M, (2009) Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus. Plant J 58: 766-777 doi:10.1111/j.1365-313X.2009.03824.x.
82. Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI, et al. (2010) Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J 29: 1149-1161 doi:10.1038/emboj.2010.1.
83. Pearce G, Yamaguchi Y, Barona G, Ryan CA, (2010) A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA 107: 14921-14925 doi:10.1073/pnas.1007568107.
84. Jorda L, Coego A, Conejero V, Vera P, (1999) A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J Biol Chem 274: 2360-2365.
85. Meichtry J, Amrhein N, Schaller A, (1999) Characterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill.). Plant Mol Biol 39: 749-760.
86. Hamilton JMU, Simpson DJ, Hyman SC, Ndimba BK, Slabas AR, (2003) Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localization. Biochem J 370: 57-67 doi:10.1042/BJ20021125.
87. Donatti AC, Furlaneto-Maia L, Fungaro MHP, Furlaneto MC, (2008) Production and regulation of cuticle-degrading proteases from Beauveria bassiana in the presence of Rhammatocerus schistocercoides cuticle. Curr Microbiol 56: 256-260 doi:10.1007/s00284-007-9071-y.
88. Sreedhar L, Kobayashi DY, Bunting TE, Hillman BI, Belanger FC, (1999) Fungal proteinase expression in the interaction of the plant pathogen Magnaporthe poae with its host. Gene 235: 121-129 doi:10.1016/S0378-1119(99)00201-2.
89. Yang J, Huang X, Tian B, Wang M, Niu Q, et al. (2005) Isolation and characterization of a serine protease from the nematophagous fungus, Lecanicillium psalliotae, displaying nematicidal activity. Biotechnol Lett 27: 1123-1128 doi:10.1007/s10529-005-8461-0.
90. Reddy PV, Lam CK, Belanger FC, (1996) Mutualistic fungal endophytes express a proteinase that is homologous to proteases suspected to be important in fungal pathogenicity. Plant Physiol 111: 1209-1218.