The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity

Environmental Microbiology

Volumn 17, Issue 4, 2015, Pages 1166-1188

  Han, Qin ^a   Wu, Fengli ^a   Wang, Xiaonan ^a   Qi, Hong ^a   Shi, Liang ^a   Ren, Ang ^a   Liu, Qinghai ^a   Zhao, Mingwen ^a   Tang, Canming ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS AMYLOLIQUEFACIENS; BACTERIA (MICROORGANISMS); FUNGI; GOSSYPIUM HIRSUTUM; VERTICILLIUM DAHLIAE;

ANTIFUNGAL AGENT; CYCLOPEPTIDE; ITURIN A; ITURIN C; LIPOPEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; RNA 16S;

BACILLUS; CELL WALL; DRUG EFFECTS; ENZYME ACTIVATION; GENETICS; GOSSYPIUM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PLANT DISEASE; SIGNAL TRANSDUCTION; VERTICILLIUM;

ANTIFUNGAL AGENTS; BACILLUS; CELL WALL; ENZYME ACTIVATION; GOSSYPIUM; LIPOPEPTIDES; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATIVE STRESS; PEPTIDES, CYCLIC; PLANT DISEASES; REACTIVE OXYGEN SPECIES; RNA, RIBOSOMAL, 16S; SIGNAL TRANSDUCTION; VERTICILLIUM;

EID: 84926421587     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12538     Document Type: Article

References (146)

1. Al-Ajlani, M.M., Sheikh, M.A., Ahmad, Z., and Hasnain, S. (2007) Production of surfactin from Bacillus subtilis MZ-7 grown on pharmamedia commercial medium. Microb Cell Fact 6: 17.
2. Albertyn, J., Hohmann, S., Thevelein, J.M., and Prior, B.A. (1994) GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14: 4135-4144.
3. Alic, N., Higgins, V.J., Pichova, A., Breitenbach, M., and Dawes, I.W. (2003) Lipid hydroperoxides activate the mitogen-activated protein kinase Mpk1p in Saccharomyces cerevisiae. J Biol Chem 278: 41849-41855.
4. Alonso-Monge, R., Real, E., Wojda, I., Bebelman, J.P., Mager, W.H., and Siderius, M. (2001) Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects. Mol Microbiol 41: 717-730.
5. Alvarez, F., Castro, M., Príncipe, A., Borioli, G., Fischer, S., Mori, G., and Jofré, E. (2012) The plant-associated Bacillus amyloliquefaciens strains MEP2 18 and ARP2 3 capable of producing the cyclic lipopeptides iturin or surfactin and fengycin are effective in biocontrol of sclerotinia stem rot disease. J Appl Microbiol 112: 159-174.
6. Amey, R.C., Mills, P.R., Bailey, A., and Foster, G.D. (2003) Investigating the role of a Verticillium fungicola beta-1, 6-glucanase during infection of Agaricus bisporus using targeted gene disruption. Fungal Genet Biol 39: 264-275.
7. Antonopoulos, D.F., Tjamos, S.E., Antoniou, P.P., Rafeletos, P., and Tjamos, E.C. (2008) Effect of Paenibacillus alvei, strain K165, on the germination of Verticillium dahliae microsclerotia in planta. Biol Control 46: 166-170.
8. Aranda, F.J., Teruel, J.A., and Ortiz, A. (2005) Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochim Biophys Acta 1713: 51-56.
9. Arrebola, E., Jacobs, R., and Korsten, L. (2010) Iturin A is the principal inhibitor in the biocontrol activity of Bacillus amyloliquefaciens PPCB004 against postharvest fungal pathogens. J Appl Microbiol 108: 386-395.
10. Arroyo, J., Bermejo, C., García, R., and Rodríguez-Peña, J.M. (2009) Genomics in the detection of damage in microbial systems: cell wall stress in yeast. Clin Microbiol Infect 1: 44-46.
11. Bahn, Y.S., Kojima, K., Cox, G.M., and Heitman, J. (2005) Specialization of the HOG pathway and its impact on differentiation and virulence of Cryptococcus neoformans. Mol Biol Cell 16: 2285-2300.
12. Besson, F., and Michel, G. (1987) Isolation and characterization of new iturins: iturin D and iturin E. J Antibiot (Tokyo) 40: 437-442.
13. Besson, F., Peypoux, F., Michel, G., and Delcambe, L. (1976) Characterization of iturin A in antibiotics from various strains of Bacillus subtilis. J Antibiot (Tokyo) 29: 1043-1049.
14. Besson, F., Peypoux, F., Quentin, M.J., and Michel, G. (1984) Action of antifungal peptidolipids from Bacillus subtilis on the cell membrane of Saccharomyces cerevisiae. J Antibiotics (Tokyo) 37: 172-177.
15. Block, A., Li, G., Fu, Z.Q., and Alfano, J.R. (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11: 396-403.
16. Bonmatin, J.M., Laprevote, O., and Peypoux, F. (2003) Diversity among microbial cyclic lipopeptides: iturins and surfactins. Activity-structure relationships to design new bioactive agents. Comb Chem High T Scr 6: 541-556.
17. Borriss, R., Chen, X.H., Rueckert, C., Blom, J., Becker, A., Baumgarth, B., etal. (2011) Relationship of Bacillus amyloliquefaciens clades associated with strains DSM7T and FZB42: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on their discriminating complete genome sequences comparisons. Int J Syst Evol Microbiol 61: 1786-1801.
18. Brotman, Y., Makovitzki, A., Shai, Y., Chet, I., and Viterbo, A. (2009) Synthetic ultrashort cationic lipopeptides induce systemic plant defense responses against bacterial and fungal pathogens. Appl Environ Microbiol 75: 5373-5379.
19. Cadenas, E., and Davies, K.J. (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29: 222-230.
20. Cai, Y.F., He, X.H., Mo, J.C., Sun, Q., Yang, J.P., and Liu, J.G. (2009) Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: a review. Afr J Biotechnol 8: 7363-7372.
21. Cao, X.H., Wang, A.H., Wang, C.L., Mao, D.Z., Lu, M.F., Cui, Y.Q., and Jiao, R.Z. (2010) Surfactin induces apoptosis in human breast cancer MCF-7 cells through a ROS/JNK-mediated mitochondrial/caspase pathway. Chem Biol Interact 12: 357-362.
22. 2+ is associated with mitochondria permeability transition pore involved in surfactin-induced MCF-7 cells apoptosis. Chem Biol Interact 190: 16-27.
23. Chen, Y., Yan, F., Chai, Y., Liu, H., Kolter, R., Losick, R., and Guo, J.H. (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15: 848-864.
24. Dagley, M.J., Gentle, I.E., Beilharz, T.H., Pettolino, F.A., Djordjevic, J.T., Lo, T.L., etal. (2011) Cell wall integrity is linked to mitochondria and phospholipid homeostasis in Candida albicans through the activity of the post-transcriptional regulator Ccr4-Pop2. Mol Microbiol 79: 968-989.
25. Debode, J., De Maeyer, K., Perneel, M., Pannecoucque, J., De Backer, G., and Höfte, M. (2007) Biosurfactants are involved in the biological control of Verticillium microsclerotia by Pseudomonas spp. J Appl Microbiol 103: 1184-1196.
26. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19: 5157-5166.
27. Duran, R., Cary, J.W., and Calvo, A.M. (2010) Role of the osmotic stress regulatory pathway in morphogenesis and secondary metabolism in filamentous fungi. Toxins (Basel) 2: 367-381.
28. Erdogan, O., and Benlioglu, K. (2010) Biological control of Verticillium wilt on cotton by the use of fluorescent Pseudomonas spp. under field conditions. Biol Control 153: 39-45.
29. Fliegmann, J., Mithofer, A., Wanner, G., and Ebel, J. (2004) An ancient enzyme domain hidden in the putative beta-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J Biol Chem 279: 1132-1140.
30. Fradin, E.F., and Thomma, B. (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V-dahliae and V-alboatrum. Mol Plant Pathol 7: 71-86.
31. Fravel, D.R. (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43: 337-359.
32. Fuchs, B.B., and Mylonakis, E. (2009) Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot Cell 8: 1616-1625.
33. Gao, G., Yin, D., Chen, S., Xia, F., Yang, J., Li, Q., and Wang, W. (2012) Effect of biocontrol agent Pseudomonas fluorescens 2P24 on soil fungal community in cucumber rhizosphere using T-RFLP and DGGE. PLoS ONE 7: e31806.
34. García-Gutiérrez, L., Zeriouh, H., Romero, D., Cubero, J., de Vicente, A., and Pérez-García, A. (2013) The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate- and salicylic acid-dependent defence responses. Microb Biotechnol 6: 264-274.
35. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198: 190-202.
36. Gerik, K.J., Donlin, M.J., Soto, C.E., Banks, A.M., Banks, I.R., Maligie, M.A., etal. (2005) Cell wall integrity is dependent on the PKC1 signal transduction pathway in Cryptococcus neoformans. Mol Microbiol 58: 393-408.
37. Goicoechea, N. (2009) To what extent are soils amendments useful to control Verticillium wilt? Pest Manag Sci 65: 831-839.
38. Grant, C.M., Collinson, L.P., Roe, J.H., and Dawes, I.W. (1996) Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol Microbiol 21: 171-179.
39. Grau, A., Ortiz, A., de Godos, A., and Gómez-Fernández, J.C. (2000) A biophysical study of the interaction of the lipopeptide antibiotic iturin A with aqueous phospholipid bilayers. Arch Biochem Biophys 377: 315-323.
40. Gueldner, R.C., Reilly, C.C., Pusey, P.L., Costello, C.E., Arrendale, R.F., Cox, R.H., etal. (1988) Isolation and identification of iturins as antifungal peptides in biological control of peach brown rot with Bacillus subtilis. J Agric Food Chem 36: 366-370.
41. Guo, M., Chen, Y., Du, Y., Dong, Y., Guo, W., Zhai, S., etal. (2011) The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7: e1001302.
42. Hanson, L.E. (2000) Reduction of Verticillium wilt symptoms in cotton following seed treatment with Trichoderma virens. J Cotton Sci 4: 224-231.
43. Harrison, J.C., Zyla, T.R., Bardes, E.S., and Lew, D.J. (2004) Stress-specific activation mechanisms for the'cell integrity' MAPK pathway. J Biol Chem 279: 2616-2622.
44. Hartl, L., Zach, S., and Seidl-Seiboth, V. (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93: 533-543.
45. Hauck, P., Thilmony, R., and He, S.Y. (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA 100: 8577-8582.
46. Hawle, P., Horst, D., Bebelman, J.P., Yang, X.X., Siderius, M., and van der Vies, S.M. (2007) Cdc37p is required for stress-induced high-osmolarity glycerol and protein kinase C mitogen-activated protein kinase pathway functionality by interaction with Hog1p and Slt2p (Mpk1p). Eukaryot Cell 6: 521-532.
47. Heerklotz, H., and Seelig, J. (2007) Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur Biophys J 36: 305-314.
48. Henry, G., Deleu, M., Jourdan, E., Thonart, P., and Ongena, M. (2011) The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell Microbiol 13: 1824-1837.
49. Herdeiro, R.S., Pereira, M.D., Panek, A.D., and Eleutherio, E.C. (2006) Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim Biophys Acta 1760: 340-346.
50. Hernández-Lauzardo, A.N., Bautista-Baños, S., Velázquez-del Valle, M.G., Méndez-Montealvo, M.G., Sánchez-Rivera, M.M., and Bello-Pérez, L.A. (2008) Antifungal effects of chitosan with different molecular weights on in vitro development of Rhizopus stolonifer (Ehrenb.: Fr.) Vuill. Carbohydr Polym 73: 541-547.
51. Hernandez-Lopez, M.J., Randez-Gil, F., and Prieto, J.A. (2006) Hog1 mitogen-activated protein kinase plays conserved and distinct roles in the osmotolerant yeast Torulaspora delbrueckii. Eukaryot Cell 5: 1410-1419.
52. Hohmann, S. (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
53. Hu, H.L. (2012) Resarch the progression of cotton infection and colonization by Verticillium dahliae. Master Thesis. Nanjing, China: Nanjing Agricultural University.
54. Huang, J.L., Li, H.L., and Yuan, H.X. (2006) Effect of organic amendments on Verticillium wilt of cotton. Crop Protect 25: 1167-1173.
55. Huang, K., Czymmek, K.J., Caplan, J.L., Sweigard, J.A., and Donofrio, N.M. (2011) HYR1-mediated detoxification of reactive oxygen species is required for full virulence in the rice blast fungus. PLoS Pathog 7: e1001335.
56. Johansson, A., Staal, J., and Dixelius, C. (2006) Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA- and ET-associated signals via cytosolic NPR-1 and RFO1. Mol Plant Microbe Interact 19: 958-969.
57. Jones, J.D., and Dangl, J.L. (2006) The plant immune system. Nature 444: 323-329.
58. Joubert, A., Bataille-Simoneau, N., Campion, C., Guillemette, T., Hudhomme, P., Iacomi-Vasilescu, B., etal. (2011) Cell wall integrity and high osmolarity glycerol pathways are required for adaptation of Alternaria brassicicola to cell wall stress caused by brassicaceous indolic phytoalexins. Cell Microbiol 13: 62-80.
59. Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthelemy, J.P., Thonart, P., and Ongena, M. (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant Microbe Interact 22: 456-468.
60. Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., etal. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103: 11086-11091.
61. Khong, N.G., Randoux, B., Tayeh, C.H., Coutte, F., Bourdon, N., Tisserant, B., etal. (2012) Induction of resistance in wheat against powdery mildew by bacterial cyclic lipopeptides. Commun Agric Appl Biol Sci 77: 39-51.
62. Kim, J.H., Chan, K.L., Faria, N.C., Martins Mde, L., and Campbell, B.C. (2012) Targeting the oxidative stress response system of fungi with redox-potent chemosensitizing agents. Front Microbiol 3: 88.
63. Kim, K.K., Fravel, D.R., and Papavizas, G.C. (1988) Identification of a metabolite produced by Talaromyces flavus as glucose oxidase and its role in the biocontrol of Verticillium dahliae. Phytopathology 78: 488-492.
64. Kim, K.Y., Truman, A.W., and Levin, D.E. (2008) Yeast Mpk1 mitogen-activated protein kinase activates transcription through Swi4/Swi6 by a noncatalytic mechanism that requires upstream signal. Mol Cell Biol 28: 2579-2589.
65. Kim, P.I., Bai, H., Bai, D., Chae, H., Chung, S., Kim, Y., etal. (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97: 942-949.
66. Kim, P.I., Ryu, J., Kim, Y.H., and Chi, Y.T. (2010) Production of biosurfactant lipopeptides Iturin A, fengycin and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 20: 138-145.
67. Kim, S.Y., Ko, Y.J., Jung, K.W., Strain, A., Nielsen, K., and Bahn, Y.S. (2011) Hrk1 plays both Hog1-dependent and -independent roles in controlling stress response and antifungal drug resistance in Cryptococcus neoformans. PLoS ONE 6: e18769.
68. Klosterman, S.J., Atallah, Z.K., Vallad, G.E., and Subbarao, K.V. (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47: 39-62.
69. Ko, Y.J., Yu, Y.M., Kim, G.B., Lee, G.W., Maeng, P.J., Kim, S., etal. (2009) Remodeling of global transcription patterns of Cryptococcus neoformans genes mediated by the stress-activated HOG signaling pathways. Eukaryot Cell 8: 1197-1217.
70. Kojima, K., Takano, Y., Yoshimi, A., Tanaka, C., Kikuchi, T., and Okuno, T. (2004) Fungicide activity through activation of a fungal signaling pathway. Mol Microbiol 53: 1785-1796.
71. Kojima, K., Bahn, Y.S., and Heitman, J. (2006) Calcineurin, Mpk1 and Hog1 MAPK pathways independently control fludioxonil antifungal sensitivity in Cryptococcus neoformans. Microbiology 152: 591-604.
72. Kovács, Z., Szarka, M., Kovács, S., Boczonádi, I., Emri, T., Abe, K., etal. (2013) Effect of cell wall integrity stress and RlmA transcription factor on asexual development and autolysis in Aspergillus nidulans. Fungal Genet Biol 54: 1-14.
73. Kumar, V., Parkhi, V., Kenerley, C.M., and Rathore, K.S. (2009) Defense-related gene expression and enzyme activities in transgenic cotton plants expressing an endochitinase gene from Trichoderma virens in response to interaction with Rhizoctonia solani. Planta 230: 277-291.
74. Leclere, V., Bechet, M., Adam, A., Guez, J.S., Wathelet, B., Ongena, M., etal. (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism's antagonistic and biocontrol activities. Appl Environ Microbiol 71: 4577-4584.
75. Lee, S.C., Kim, S.H., Park, I.H., Chung, S.Y., and Choi, Y.L. (2007) Isolation and structural analysis of bamylocin A, novel lipopeptide from Bacillus amyloliquefaciens LP03 having antagonistic and crude oil-emulsifying activity. Arch Microbiol 188: 307-312.
76. Levin, D.E. (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69: 262-291.
77. Levin, D.E. (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189: 1145-1175.
78. Li, C.H., Shi, L., Han, Q., Hu, H.L., Zhao, M.W., Tang, C.M., and Li, S.P. (2012) Biocontrol of Verticillium wilt and colonization of cotton plants by an endophytic bacterial isolate. J Appl Microbiol 113: 641-651.
79. Li, C.H., Zhao, M.W., Tang, C.M., and Li, S.P. (2010) Population dynamics and identification of endophytic bacteria antagonistic toward plant-pathogenic fungi in cotton root. Microb Ecol 59: 344-356.
80. Li, Q., Harvey, L.M., and McNeil, B. (2009) Oxidative stress in industrial fungi. Crit Rev Biotechnol 29: 199-213.
81. Lin, C.H., Yang, S.L., and Chung, K.R. (2009) The YAP1 homolog-mediated oxidative stress tolerance is crucial for pathogenicity of the necrotrophic fungus Alternaria alternata in citrus. Mol Plant Microbe Interact 22: 942-952.
82. Liu, P., Luo, L., Guo, J., Liu, H., Wang, B., Deng, B., etal. (2010) Farnesol induces apoptosis and oxidative stress in the fungal pathogen Penicillium expansum. Mycologia 102: 311-318.
83. Liu, W.W., Leroux, P., and Fillinger, S. (2008) The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide- and phenylpyrrole-resistance. Fungal Genet Biol 45: 1062-1074.
84. Luo, X., Keyhani, N.O., Yu, X., He, Z., Luo, Z., Pei, Y., and Zhang, Y. (2012) The MAP kinase Bbslt2 controls growth, conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genet Biol 49: 544-555.
85. Ma, D., and Li, R. (2013) Current understanding of HOG-MAPK pathway in Aspergillus fumigatus. Mycopathologia 175: 13-23.
86. Maget-Dana, R., and Ptak, M. (1990) Iturin lipopeptides: interactions of mycosubtilin with lipids in planar membranes and mixed monolayers. Biochim Biophys Acta 1023: 34-40.
87. Maget-Dana, R., Ptak, M., Peypoux, F., and Michel, G. (1985) Pore-forming properties of iturin A, a lipopeptide antibiotic. Biochim Biophys Acta 815: 405-409.
88. Maget-Dana, R., Harnois, I., and Ptak, M. (1989) Interactions of the lipopeptides antifungal iturin A with lipids in mixed monolayers. Biochim Biophys Acta 981: 309-314.
89. Makkar, R.S., and Cameotra, S.S. (1999) Structural characterization of a biosurfactant produced by Bacillus subtilis at 45°C. J Surfactants Deterg 2: 367-372.
90. Meschke, H., Walter, S., and Schrempf, H. (2011) Characterization and localization of prodiginines from Streptomyces lividans suppressing Verticillium dahliae in the absence or presence of Arabidopsis thaliana. Environ Microbiol 14: 940-952.
91. Millet, Y.A., Danna, C.H., Clay, N.K., Songnuan, W., Simon, M.D., Werck-Reichhart, D., and Ausubel, F.M. (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973-990.
92. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., etal. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613-19618.
93. Mizumoto, S., Hirai, M., and Shoda, M. (2007) Enhanced iturin A production by Bacillus subtilis and its effect on suppression of the plant pathogen Rhizoctonia solani. Appl Microbiol Biotechnol 75: 1267-1274.
94. Mootz, H.D., Schwarzer, D., and Marahiel, M.A. (2002) Ways of assembling complex natural products on modular nonribosomal peptide synthetases. Chem Bio Chem 3: 490-504.
95. Moree, W.J., Yang, J.Y., Zhao, X., Liu, W.T., Aparicio, M., Atencio, L., etal. (2013) Imaging mass spectrometry of a coral microbe interaction with fungi. J Chem Ecol 39: 1045-1054.
96. Moyne, A.L., Shelby, R., Cleveland, T.E., and Tuzun, S. (2001) Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J Appl Microbiol 90: 622-629.
97. Munkres, K.D. (1990) Histochemical detection of superoxide radicals and hydrogen peroxide by Age-1 mutants of Neurospora. Fung Genet Newslett 37: 24-25.
98. Nagorska, K., Bikowski, M., and Obuchowskji, M. (2007) Multicellular behaviour and production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent. Acta Biochim Pol 54: 495-508.
99. Nasir, M.N., and Besson, F. (2011) Specific interactions of mycosubtilin with cholesterol-containing artificial membranes. Langmuir 27: 10785-10792.
100. Nasir, M.N., and Besson, F. (2012a) Conformational analyses of bacillomycin D, a natural antimicrobial lipopeptide, alone or in interaction with lipid monolayers at the air-water interface. J Colloid Interface Sci 387: 187-193.
101. Nasir, M.N., and Besson, F. (2012b) Interactions of the antifungal mycosubtilin with ergosterol-containing interfacial monolayers. Biochim Biophys Acta 1818: 1302-1308.
102. Nasir, M.N., Thawani, A., Kouzayha, A., and Besson, F. (2010) Interactions of the natural antimicrobial mycosubtilin with phospholipid membrane models. Colloids Surf B Biointerfaces 78: 17-23.
103. Nimchuk, Z., Eulgem, T., Holt, I.B., and Dangl, J.L. (2003) Recognition and response in the plant immune system. Annu Rev Genet 37: 579-609.
104. Ongena, M., and Jacques, P. (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16: 115-125.
105. Ongena, M., Jacques, P., Toure, Y., Destain, J., Jabrane, A., and Thonart, P. (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96: 1151-1160.
106. Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., etal. (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9: 1084-1090.
107. Pantelides, I.S., Tjamos, S.E., and Paplomatas, E.J. (2010) Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Mol Plant Pathol 11: 191-202.
108. Pardhasaradhi, B.V., Ali, A.M., Kumari, A.L., Reddanna, P., and Khar, A. (2003) Phycocyanin-mediated apoptosis in AK-5 tumor cells involves down-regulation of Bcl-2 and generation of ROS. Mol Cancer Ther 2: 1165-1170.
109. Pathak, K.V., and Keharia, H. (2013) Characterization of fungal antagonistic bacilli isolated from aerial roots of banyan (Ficus benghalensis) using intact-cell MALDI-TOF mass spectrometry (ICMS). J Appl Microbiol l114: 1300-1310.
110. Petkova, M.I., Pujol-Carrion, N., Arroyo, J., García-Cantalejo, J., and de la Torre-Ruiz, M.A. (2010) Mtl1 is required to activate general stress response through Tor1 and Ras2 inhibition under conditions of glucose starvation and oxidative stress. J Biol Chem 285: 19521-19531.
111. Phae, C.G., Shoda, M., and Kubota, H. (1990) Suppressive effect of Bacillus subtilis and its products on phytopathogenic microorganisms. J Ferment Bioeng 69: 1-7.
112. Puhalla, J.E. (1973) Differences in sensitivity of Verticillium species to ultraviolet irradiation. Phytopathology 63: 1488-1492.
113. Qi, G., Zhu, F., Du, P., Yang, X., Qiu, D., Yu, Z., etal. (2010) Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway. Peptides 31: 1978-1986.
114. Qiao, J., Liu, W., and Li, R. (2010) Truncated Afyap1 attenuates antifungal susceptibility of Aspergillus fumigatus to voriconazole and confers adaptation of the fungus to oxidative stress. Mycopathologia 170: 155-160.
115. Quentin, M.J., Besson, F., Peypoux, F., and Michel, G. (1982) Action of peptidolipidic antibiotics of iturin group on erythrocytes. Effects of some lipids on hemolysis. Biochim Biophys Acta 684: 207-211.
116. Ren, A., Li, M.J., Shi, L., Mu, D.S., Jiang, A.L., Han, Q., and Zhao, M.W. (2013) Profiling and quantifying differential gene transcription provide insights into ganoderic acid biosynthesis in Ganoderma lucidum in response to methyl jasmonate. PLoS ONE 8: e65027.
117. Rodrigues-Pousada, C., Menezes, R.A., and Pimentel, C. (2010) The Yap family and its role in stress response. Yeast 27: 245-258.
118. Roelfsema, M.R., Hedrich, R., and Geiger, D. (2012) Anion channels: master switches of stress responses. Trends Plant Sci 17: 221-229.
119. Romero, D., de Vicente, A., Olmos, J.L., Dávila, J.C., and Pérez-García, A. (2007a) Effect of lipopeptides of antagonistic strains of Bacillus subtilis on the morphology and ultrastructure of the cucurbit fungal pathogen Podosphaera fusca. J Appl Microbiol 103: 969-976.
120. Romero, D., de Vicente, A., Rakotoaly, R.H., Dufour, S.E., Veening, J.W., Arrebola, E., etal. (2007b) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact 20: 430-440.
121. Rui, O., and Hahn, M. (2007) The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol Plant Pathol 8: 173-184.
122. Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., etal. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214.
123. Staleva, L., Hall, A., and Orlow, S.J. (2004) Oxidative stress activates FUS1 and RLM1 transcription in the yeast Saccharomyces cerevisiae in an oxidant-dependent manner. Mol Biol Cell 15: 5574-5582.
124. Stosz, S.K., Fravel, D.R., and Roberts, D.P. (1996) In vitro analysis of the role of glucose oxidase from Talaromyces flavus in biocontrol of the plant pathogen Verticillium dahliae. Appl Environ Microbiol 62: 3183-3186.
125. Tao, Y., Bie, X.M., Lv, F.X., Zhao, H.Z., and Lu, Z.X. (2011) Antifungal activity and mechanism of fengycin in the presence and absence of commercial surfactin against Rhizopus stolonifer. J Microbiol 49: 146-150.
126. Thimon, L., Peypoux, F., Wallach, J., and Michel, G. (1995) Effect of the lipopeptide antibiotic, iturin A, on morphology and membrane ultrastructure of yeast cells. FEMS Microbiol Lett 128: 101-106.
127. Tjamos, E.C. (2000) Strategies in developing methods and applying techniques for the biological control of Verticillium dahliae-short review. In Advances in Verticillium Research and Disease Management. Tjamos, E.C., Rowe, R.C., Heale, J.B., and Fravel, D.R. (eds). St Paul, MN, USA: APS Press, pp. 227-231.
128. Tjamos, S.E., Flemetakis, E., Paplomatas, E.J., and Katinakis, P. (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18: 555-561.
129. Torres, M.A., Dangl, J.L., and Jones, J.D. (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517-522.
130. Touré, Y., Ongena, M., Jacques, P., Guiro, A., and Thonart, P. (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96: 1151-1160.
131. Tran, H., Ficke, A., Asiimwe, T., Höfte, M., and Raaijmakers, J.M. (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175: 731-742.
132. Velho, R.V., Medina, L.F., Segalin, J., and Brandelli, A. (2011) Production of lipopeptides among Bacillus strains showing growth inhibition of phytopathogenic fungi. Folia Microbiol (Praha) 56: 297-303.
133. Völksch, B., Ullrich, M., and Fritsch, W. (1993) Occurrence of anti-microbial activities of bacteria from soybean leaf pots. J Basic Microbiol 33: 349-355.
134. Wilhelm, S. (1955) Longevity of the Verticillium wilt fungus in the laboratory and field. Phytopathology 45: 180-181.
135. Williams, S.M., and Brodbelt, J.S. (2004) MS(n) characterization of protonated cyclic peptides and metal complexes. J Am Soc Mass Spectrom 15: 1039-1054.
136. Wojda, I., Alonso-Monge, R., Bebelman, J.P., Mager, W.H., and Siderius, M. (2003) Response to high osmotic conditions and elevated temperature in Saccharomyces cerevisiae is controlled by intracellular glycerol and involves coordinate activity of MAP kinase pathways. Microbiology 49: 1193-1204.
137. Woo, J.H., Kim, Y.H., Choi, Y.J., Kim, D.G., Lee, K.S., Bae, J.H., etal. (2003) Molecular mechanisms of curcumin-induced cytotoxicity: induction of apoptosis through generation of reactive oxygen species, down-regulation of Bcl-XL and IAP, the release of cytochromec and inhibition of Akt. Carcinogenesis 24: 1199-1208.
138. Wubben, M.J., Callahan, F.E., Hayes, R.W., and Jenkins, J.N. (2008) Molecular characterization and temporal expression analyses indicate that the MIC (Meloidogyne Induced Cotton) gene family represents a novel group of root-specific defense-related genes in upland cotton (Gossypium hirsutum L.). Planta 228: 111-123.
139. Yu, G.Y., Sinclair, J.B., Hartman, G.L., and Bertagnolli, B.L. (2002) Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34: 955-963.
140. Yuan, B., Wanga, Z., Qina, S., Zhao, G.H., Fenga, Y., Weia, J.H., and Jiang, J.H. (2012) Study of the anti-sapstain fungus activity of Bacillus amyloliquefaciens CGMCC 5569 associated with Ginkgo biloba and identification of its active components. Bioresour Technol 114: 536-541.
141. Zeriouh, H., Romero, D., Garcia-Gutierrez, L., Cazorla, F.M., de Vicente, A., and Perez-Garcia, A. (2011) The iturin-like lipopeptides are essential components in the biological control arsenal of Bacillus subtilis against bacterial diseases of cucurbits. Mol Plant Microbe Interact 24: 1540-1552.
142. Zhang, B., Dong, C., Shang, Q., Han, Y., and Li, P. (2013) New insights into membrane-active action in plasma membrane of fungal hyphae by the lipopeptide antibiotic bacillomycin L. Biochim Biophys Acta 1828: 2230-2237.
143. Zhang, Y., Lamm, R., Pillonel, C., Lam, S., and Xu, J.R. (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68: 532-538.
144. Zhang, Y., Wang, X., Yang, S., Chi, J., Zhang, G., and Ma, Z. (2011) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30: 2085-2096.
145. Zhao, Z.Z., Wang, Q.S., Wang, K.M., Brain, K., Liu, C.H., and Gu, Y.C. (2010) Study of the antifungal activity of Bacillus vallismortis ZZ185 in vitro and identification of its antifungal components. Bioresour Technol 101: 292-297.
146. Zhou, B.J., Jia, P.S., Gao, F., and Guo, H.S. (2012) Molecular characterization and functional analysis of a necrosis- and ethylene-inducing, protein-encoding gene family from Verticillium dahliae. Mol Plant Microbe Interact 25: 964-975.