Inhibition of bacterial quorum sensing by extracts from aquatic fungi: First report from marine endophytes

Marine Drugs

Volumn 12, Issue 11, 2014, Pages 5503-5526

  Martín Rodríguez, Alberto J ^a,b   Reyes, Fernando ^c   Martín, Jesús ^c   Pérez Yépez, Juan ^a   León Barrios, Milagros ^a   Couttolenc, Alan ^d   Espinoza, César ^d   Trigos, Ángel ^d   Martín, Víctor S ^a   Norte, Manuel ^a   Fernández, José J ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b OCEANIC PLATFORM OF THE CANARY ISLANDS   (Spain)

^c Health Sciences Technology Park   (Spain)

^d UNIVERSIDAD VERACRUZANA   (Mexico)

Author keywords

Antifouling; Biofouling; Chromobacterium violaceum; Endophytes; Fungi; LC HRMS; Metabolic profile; Quorum sensing

Indexed keywords

EPICOCCUM EXTRACT; FUNGAL EXTRACT; FUSARIUM EXTRACT; KHUSKIA EXTRACT; SAROCLADIUM EXTRACT; UNCLASSIFIED DRUG; RIBOSOME RNA;

ANTIBACTERIAL ACTIVITY; ARTICLE; CHROMOBACTERIUM VIOLACEUM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DETERMINATION; ENDOPHYTIC FUNGUS; EPICOCCUM; FUNGAL STRAIN; FUNGUS IDENTIFICATION; FUNGUS ISOLATION; FUSARIUM; KHUSKIA; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; QUORUM SENSING; SAMPLING; SAROCLADIUM; AQUATIC SPECIES; CHROMOBACTERIUM; ENDOPHYTE; FUNGUS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PROCEDURES; SECONDARY METABOLISM;

ANTHOZOA; BACTERIA (MICROORGANISMS); CHROMOBACTERIUM VIOLACEUM; DIPLORIA STRIGOSA; EPICOCCUM; FUNGI; FUSARIUM; SAROCLADIUM;

AQUATIC ORGANISMS; CHROMATOGRAPHY, LIQUID; CHROMOBACTERIUM; ENDOPHYTES; FUNGI; MASS SPECTROMETRY; QUORUM SENSING; RNA, RIBOSOMAL; SECONDARY METABOLISM;

EID: 84915818590     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12115503     Document Type: Article

References (87)

1. Marques, J.C.; Lamosa, P.; Russell, C.; Ventura, R.; Maycock, C.; Semmelhack, M.F.; Miller, S.T.; Xavier, K.B. Processing the interspecies quorum-sensing signal autoinducer-2 (AI-2): Characterization of phospho-(S)-4, 5-dihydroxy-2, 3-pentanedione isomerization by LsrG protein. J. Biol. Chem. 2011, 286, 18331-18343.
2. Ryan, R.P.; Dow, J.M. Communication with a growing family: Diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol. 2011, 19, 145-152.
3. Williams, P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 2007, 153, 3923-3938.
4. Brachmann, A.O.; Brameyer, S.; Kresovic, D.; Hitkova, I.; Kopp, Y.; Manske, C.; Schubert, K.; Bode, H.B.; Heermann, R. Pyrones as bacterial signaling molecules. Nat. Chem. Biol. 2013, 9, 573-578.
5. Schulz, S. A new bacterial chemical signal: Mapping the chemical space used for communication. Chembiochem 2014, 15, 498-500.
6. Galloway, W.R.J.D.; Hodgkinson, J.T.; Bowden, S.D.; Welch, M.; Spring, D.R. Quorum sensing in Gram-negative bacteria: Small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem. Rev. 2011, 111, 28-67.
7. Rutherford, S.T.; Bassler, B.L. Bacterial quorum sensing: Its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2012, 2, a012427.
8. Huang, Y.-L.; Dobretsov, S.; Xiong, H.; Qian, P.-Y. Effect of biofilm formation by Pseudoalteromonas spongiae on induction of larval settlement of the polychaete Hydroides elegans. Appl. Environ. Microbiol. 2007, 73, 6284-6288.
9. Yang, J.-L.; Shen, P.-J.; Liang, X.; Li, Y.-F.; Bao, W.-Y.; Li, J.-L. Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms. Biofouling 2013, 29, 247-259.
10. Twigg, M.S.; Tait, K.; Williams, P.; Atkinson, S.; Cámara, M. Interference with the germination and growth of Ulva zoospores by quorum-sensing molecules from Ulva-associated epiphytic bacteria. Environ. Microbiol. 2013, 16, 445-453.
11. Tait, K.; Havenhand, J. Investigating a possible role for the bacterial signal molecules N-acylhomoserine lactones in Balanus improvisus cyprid settlement. Mol. Ecol. 2013, 22, 2588-2602.
12. Weinberger, F.; Beltran, J.; Correa, J.A.; Lion, U.; Pohnert, G.; Kumar, N.; Steinberg, P.; Kloareg, B.; Potin, P. Spore release in Acrochaetium sp. (Rhodophyta) is bacterially controlled. J. Phycol. 2007, 43, 235-241.
13. Rasmussen, T.B.; Manefield, M.; Andersen, J.B.; Eberl, L.; Anthoni, U.; Christophersen, C.; Steinberg, P.; Kjelleberg, S.; Givskov, M. How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 2000, 146, 3237-3244.
14. Janssens, J.C.A.; Steenackers, H.; Robijns, S.; Gellens, E.; Levin, J.; Zhao, H.; Hermans, K.; De Coster, D.; Verhoeven, T.L.; Marchal, K.; et al. Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 2008, 74, 6639-6648.
15. Chen, F.; Gao, Y.; Chen, X.; Yu, Z.; Li, X. Quorum quenching enzymes and their application in degrading signal molecules to block quorum sensing-dependent infection. Int. J. Mol. Sci. 2013, 14, 17477-17500.
16. Schlingmann, G.; Milne, L.; Carter, G. Isolation and identification of antifungal polyesters from the marine fungus Hypoxylon oceanicum LL-15G256. Tetrahedron 2002, 58, 6825-6835.
17. Bugni, T.S.; Ireland, C.M. Marine-derived fungi: A chemically and biologically diverse group of microorganisms. Nat. Prod. Rep. 2004, 21, 143-163.
18. Bhadury, P.; Mohammad, B.T.; Wright, P.C. The current status of natural products from marine fungi and their potential as anti-infective agents. J. Ind. Microbiol. Biotechnol. 2006, 33, 325-337.
19. Qian, P.-Y.; Xu, Y.; Fusetani, N. Natural products as antifouling compounds: Recent progress and future perspectives. Biofouling 2010, 26, 223-234.
20. Fusetani, N. Antifouling marine natural products. Nat. Prod. Rep. 2011, 28, 400-410.
21. Hausmann, R.; Vitello, M.P.; Leitermann, F.; Syldatk, C. Advances in the production of sponge biomass Aplysina aerophoba-a model sponge for ex situ sponge biomass production. J. Biotechnol. 2006, 124, 117-127.
22. Proksch, P.; Putz, A.; Ortlepp, S.; Kjer, J.; Bayer, M. Bioactive natural products from marine sponges and fungal endophytes. Phytochem. Rev. 2010, 9, 475-489.
23. Kobayashi, D.Y.; Crouch, J.A. Bacterial/Fungal interactions: From pathogens to mutualistic endosymbionts. Ann. Rev. Phytopathol. 2009, 47, 63-82.
24. Tarkka, M.T.; Sarniguet, A.; Frey-Klett, P. Inter-kingdom encounters: Recent advances in molecular bacterium-fungus interactions. Curr. Genet. 2009, 55, 233-243.
25. Frey-Klett, P.; Burlinson, P.; Deveau, A.; Barret, M.; Tarkka, M.; Sarniguet, A. Bacterial-fungal interactions: Hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol. Biol. Rev. 2011, 75, 583-609.
26. Rasmussen, T.B.; Skindersoe, M.E.; Bjarnsholt, T.; Phipps, R.K.; Christensen, K.B.; Jensen, P.O.; Andersen, J.B.; Koch, B.; Larsen, T.O.; Hentzer, M.; et al. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 2005, 151, 1325-1340.
27. Cugini, C.; Calfee, M.W.; Farrow, J.M.; Morales, D.K.; Pesci, E.C.; Hogan, D.A. Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol. Microbiol. 2007, 65, 896-906.
28. Hogan, D.A.; Vik, A.; Kolter, R. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 2004, 54, 1212-1223.
29. Watanabe, M.; Yonezawa, T.; Lee, K.; Kumagai, S.; Sugita-Konishi, Y.; Goto, K.; Hara-Kudo, Y. Molecular phylogeny of the higher and lower taxonomy of the Fusarium genus and differences in the evolutionary histories of multiple genes. BMC Evol. Biol. 2011, 11, 322.
30. Maréchal, J.-P.; Hellio, C. Challenges for the development of new non-toxic antifouling solutions. Int. J. Mol. Sci. 2009, 10, 4623-4637.
31. Dobretsov, S.; Dahms, H.-U.; Qian, P.-Y. Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 2006, 22, 43-54.
32. Li, D.; Xu, Y.; Shao, C.-L.; Yang, R.-Y.; Zheng, C.-J.; Chen, Y.-Y.; Fu, X.-M.; Qian, P.-Y.; She, Z.-G.; de Voogd, N.J.; et al. Antibacterial bisabolane-type sesquiterpenoids from the sponge-derived fungus Aspergillus sp. Mar. Drugs 2012, 10, 234-241.
33. Qi, S.-H.; Xu, Y.; Xiong, H.-R.; Qian, P.-Y.; Zhang, S. Antifouling and antibacterial compounds from a marine fungus Cladosporium sp. F14. World J. Microbiol. Biotechnol. 2008, 25, 399-406.
34. He, F.; Liu, Z.; Yang, J.; Fu, P.; Peng, J.; Zhu, W.-M.; Qi, S.-H. A novel antifouling alkaloid from halotolerant fungus Penicillium sp. OUCMDZ-776. Tetrahedron Lett. 2012, 53, 2280-2283.
35. Bao, J.; Sun, Y.-L.; Zhang, X.-Y.; Han, Z.; Gao, H.-C.; He, F.; Qian, P.-Y.; Qi, S.-H. Antifouling and antibacterial polyketides from marine gorgonian coral-associated fungus Penicillium sp. SCSGAF 0023. J. Antibiot. 2013, 66, 219-223.
36. Kwong, T.F.N.; Miao, L.; Li, X.; Qian, P.-Y. Novel antifouling and antimicrobial compound from a marine-derived fungus Ampelomyces sp. Mar. Biotechnol. 2006, 8, 634-640.
37. Qian, P-Y.; Li, X.; Kwong, N.; Yang, H.; Dobretsov, S. Use of marine fungus originated compounds as antifouling agents. U.S. Patent 2006/0147410A1, 2006.
38. Shearer, C.A.; Descals, E.; Kohlmeyer, B.; Kohlmeyer, J.; Marvanová, L.; Padgett, D.; Porter, D.; Raja, H.A.; Schmit, J.P.; Thorton, H.A.; et al. Fungal biodiversity in aquatic habitats. Biodivers. Conserv. 2006, 16, 49-67.
39. Jones, E.B.G. Are there more marine fungi to be described? Bot. Mar. 2011, 54, 343-354.
40. Khot, M.; Kamat, S.; Zinjarde, S.; Pant, A.; Chopade, B.; Ravikumar, A. Single cell oil of oleaginous fungi from the tropical mangrove wetlands as a potential feedstock for biodiesel. Microb. Cell Fact. 2012, 11, 71.
41. Smedsgaard, J.; Nielsen, J. Metabolite profiling of fungi and yeast: From phenotype to metabolome by MS and informatics. J. Exp. Bot. 2005, 56, 273-286.
42. Coleman, J.J.; Ghosh, S.; Okoli, I.; Mylonakis, E. Antifungal activity of microbial secondary metabolites. PLoS One 2011, 6, e25321.
43. Cueto, M.; Jensen, P.R.; Kauffman, C.; Fenical, W.; Lobkovsky, E.; Clardy, J. Pestalone, a new antibiotic produced by a marine fungus in response to bacterial challenge. J. Nat. Prod. 2001, 64, 1444-1446.
44. Miao, L.; Kwong, T.F.N.; Qian, P.-Y. Effect of culture conditions on mycelial growth, antibacterial activity, and metabolite profiles of the marine-derived fungus Arthrinium c.f. saccharicola. Appl. Microbiol. Biotechnol. 2006, 72, 1063-1073.
45. Lema, K.A.; Willis, B.L.; Bourne, D.G. Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl. Environ. Microbiol. 2012, 78, 3136-3144.
46. Skindersoe, M.E.; Ettinger-Epstein, P.; Rasmussen, T.B.; Bjarnsholt, T.; de Nys, R.; Givskov, M. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 2008, 10, 56-63.
47. Hunt, L.R.; Smith, S.M.; Downum, K.R.; Mydlarz, L.D. Microbial regulation in gorgonian corals. Mar. Drugs 2012, 10, 1225-1243.
48. Thenmozhi, R.; Nithyanand, P.; Rathna, J.; Pandian, S.K. Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol. Med. Microbiol. 2009, 57, 284-294.
49. Bakkiyaraj, D.; Sivasankar, C.; Pandian, S.K. Inhibition of quorum sensing regulated biofilm formation in Serratia marcescens causing nosocomial infections. Bioorg. Med. Chem. Lett. 2012, 22, 3089-3094.
50. Golberg, K.; Pavlov, V.; Marks, R.S.; Kushmaro, A. Coral-associated bacteria, quorum sensing disrupters, and the regulation of biofouling. Biofouling 2013, 29, 669-682.
51. Alagely, A.; Krediet, C.J.; Ritchie, K.B.; Teplitski, M. Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. ISME J. 2011, 5, 1609-1620.
52. Aggarwal, R.; Kharbikar, L.L.; Sharma, S.; Gupta, S.; Yadav, A. Phylogenetic relationships of Chaetomium isolates based on the internal transcribed spacer region of the rRNA gene cluster. Afr. J. Biotechnol. 2013, 12, 914-920.
53. Schoch, C.L.; Seifert, K.A.; Huhndorf, S.; Robert, V.; Spouge, J.L.; Levesque, C.A.; Chen, W. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. USA 2012, 109, 6241-6246.
54. Summerbell, R.C.; Gueidan, C.; Schroers, H.-J.; de Hoog, G.S.; Starink, M.; Rosete, Y.A.; Guarro, J.; Scott, J.A. Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud. Mycol. 2011, 68, 139-162.
55. Gazis, R.; Chaverri, P. Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol. 2010, 3, 240-254.
56. Geiser, D.M.; Klich, M.A.; Frisvad, J.C.; Peterson, S.W.; Varga, J.; Samson, R.A. The current status of species recognition and identification in Aspergillus. Stud. Mycol. 2007, 59, 1-10.
57. Steifert, K.A. Integrating DNA barcoding into the mycological sciences. Inoculum 2008, 59, 2-6.
58. De Carvalho, M.P.; Abraham, W.-R. Antimicrobial and biofilm inhibiting diketopiperazines. Curr. Med. Chem. 2012, 19, 3564-3577.
59. Holden, M.T.; Ram Chhabra, S.; de Nys, R.; Stead, P.; Bainton, N.J.; Hill, P.J.; Manefield, M.; Kumar, N.; Labatte, M.; England, D.; et al. Quorum-sensing cross talk: Isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol. 1999, 33, 1254-1266.
60. Widmer, K.W.; Soni, K.A.; Hume, M.E.; Beier, R.C.; Jesudhasan, P.; Pillai, S.D. Identification of poultry meat-derived fatty acids functioning as quorum sensing signal inhibitors to autoinducer-2 (AI-2). J. Food Sci. 2007, 72, M363-M368.
61. Soni, K.A.; Jesudhasan, P.; Cepeda, M.; Widmer, K.; Jayaprakasha, G.K.; Patil, B.S.; Hume, M.E.; Pillai, S.D. Identification of ground beef-derived fatty acid inhibitors of autoinducer-2-based cell signaling. J. Food Protect. 2008, 71, 134-138.
62. Hamill, R.L.; Higgens, C.E.; Boaz, H.E.; Gorman, M. The structure op beauvericin, a new depsipeptide antibiotic toxic to Artemia salina. Tetrahedron Lett. 1969, 10, 4255-4258.
63. Logrieco, A.; Moretti, A.; Castella, G.; Kostecki, M.; Golinski, P.; Ritieni, A.; Chelkowski, J. Beauvericin production by Fusarium species. Appl. Environ. Microbiol. 1998, 64, 3084-3088.
64. Deng, C.-M.; Liu, S.-X.; Huang, C.-H.; Pang, J.-Y.; Lin, Y.-C. Secondary metabolites of a mangrove endophytic fungus Aspergillus terreus (No. GX7-3B) from the South China Sea. Mar. Drugs 2013, 11, 2616-2624.
65. Oh, D.; Kauffman, C.A.; Jensen, P.R.; Fenical, W.; Diego, S.; Jolla, L. Induced production of emericellamides A and B from the marine-derived fungus Emericella sp. in competing co-culture. J. Nat. Prod. 2007, 70, 515-520.
66. Chiang, Y.; Szewczyk, E.; Nayak, T.; Davidson, A.D.; James, F.; Lo, H.; Wen-yueh, H.; Simityan, H.; Kuo, E.; Praseuth, A.; et al. Molecular genetic mining of the Aspergillus secondary metabolome: Discovery of the emericellamide biosynthetic pathway. Chem. Biol. 2008, 15, 527-532.
67. Liu, X.-H.; Miao, F.-P.; Qiao, M.-F.; Cichewicz, R.H.; Ji, N.-Y. Terretonin, ophiobolin, and drimane terpenes with absolute configurations from an algicolous Aspergillus ustus. RSC Adv. 2013, 3, 58-95.
68. Cohen, E.; Koch, L.; Thu, K.M.; Rahamim, Y.; Aluma, Y.; Ilan, M.; Yarden, O.; Carmeli, S. Novel terpenoids of the fungus Aspergillus insuetus isolated from the Mediterranean sponge Psammocinia sp. collected along the coast of Israel. Bioorg. Med. Chem. 2011, 19, 6587-6593.
69. Liu, H.; Edrada-Ebel, R.; Ebel, R.; Wang, Y.; Schulz, B.; Draeger, S.; Mu, W.E.G.; Wray, V.; Lin, W.; Proksch, P. Drimane sesquiterpenoids from the fungus Aspergillus ustus isolated from the marine sponge Suberites domuncula. J. Nat. Prod. 2009, 72, 1585-1588.
70. Zhou, L.-N.; Zhu, T.-J.; Cai, S.-X.; Gu, Q.-Q.; Li, D.-H. Three new indole-containing diketopiperazine alkaloids from a deep-ocean sediment derived fungus Penicillium griseofulvum. Helv. Chim. Acta 2010, 93, 1758-1763.
71. Gao, S.-S.; Li, X.-M.; Du, F.-Y.; Li, C.-S.; Proksch, P.; Wang, B.-G. Secondary metabolites from a marine-derived endophytic fungus Penicillium chrysogenum QEN-24S. Mar. Drugs 2011, 9, 59-70.
72. Bacon, C.; Porter, J.; Norred, W.; Leslie, J. Production of fusaric acid by Fusarium species. Appl. Envir. Microbiol. 1996, 62, 4039-4043.
73. Inokoshi, J.; Shigeta, N.; Fukuda, T.; Uchida, R.; Nonaka, K.; Masuma, R.; Tomoda, H. Epi-trichosetin, a new undecaprenyl pyrophosphate synthase inhibitor, produced by Fusarium oxysporum FKI-4553. J. Antibiot. 2013, 66, 549-554.
74. Tatong, M.D.K.; Talontsi, F.M.; Abdel Rahim, H.M.D.; Islam, M.T.; Oswald, R.B.; Laatsch, H. Banchromene and other secondary metabolites from the endophytic fungus Fusarium sp. obtained from Piper guineense inhibit the motility of phytopathogenic Plasmopara viticola zoospores. Tetrahedron Lett. 2014, 55, 4057-4061.
75. van Rij, E.T.; Wesselink, M.; Chin-A-Woeng, T.F.C.; Bloemberg, G.V.; Lugtenberg, B.J.J. Influence of environmental conditions on the production of phenazine-1-carboxamide by Pseudomonas chlororaphis PCL1391. Mol. Plant. Microbe. Interact. 2004, 17, 557-566.
76. van Rij, E.T.; Girard, G.; Lugtenberg, B.J.J.; Bloemberg, G.V. Influence of fusaric acid on phenazine-1-carboxamide synthesis and gene expression of Pseudomonas chlororaphis strain PCL1391. Microbiology 2005, 151, 2805-2814.
77. Kjer, J.; Debbab, A.; Aly, A.H.; Proksch, P. Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat. Protoc. 2010, 5, 479-490.
78. Lugo, A.; Alcocer, J.; Sanchez, M. del R.; Escobar, E. Littoral protozoan assemblages from two Mexican hyposaline lakes. Hydrobiologia 1998, 381, 9-13.
79. Barnett, H.L.; Hunter, B.B. Ilustrated Genera of Imperfect Fungi, 4th ed.; Macmillan Publishing Company: New York, NY, USA, 1998; p. 240.
80. Watanabe, T. Pictorial Atlas of Soil and Seed Fungi Morphologies of Cultured Fungi and Key to Specie, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2002; p. 504.
81. Vandeputte, O.M.; Kiendrebeogo, M.; Rajaonson, S.; Diallo, B.; Mol, A.; El Jaziri, M.; Baucher, M. Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 2010, 76, 243-253.
82. Martinelli, D.; Grossmann, G.; Séquin, U.; Brandl, H.; Bachofen, R. Effects of natural and chemically synthesized furanones on quorum sensing in Chromobacterium violaceum. BMC Microbiol. 2004, 4, 25.
83. Müller, F.M.; Werner, K.E.; Kasai, M.; Francesconi, A.; Chanock, S.J.; Walsh, T.J. Rapid extraction of genomic DNA from medically important yeasts and filamentous fungi by high-speed cell disruption. J. Clin. Microbiol. 1998, 36, 1625-1629.
84. Chung, W.-H.; Ishii, H.; Nishimura, K.; Ohshima, M.; Iwama, T.; Yoshimatsu, H. Genetic analysis and PCR-based identification of major Fusarium species causing head blight on wheat in Japan. J. Gen. Plant Pathol. 2008, 74, 364-374.
85. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731-2739.
86. Posada, D.; Crandall, K.A. Bioinformatics applications note modeltest: Testing the model of DNA substitution. Bioinformatics 1998, 14, 817-818.
87. Guindon, S.; Dufayard, J.-F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59, 307-321.