Lysobacter capsici AZ78 produces cyclo(l-Pro-l-Tyr), a 2,5-diketopiperazine with toxic activity against sporangia of Phytophthora infestans and Plasmopara viticola

Journal of Applied Microbiology

Volumn 117, Issue 4, 2014, Pages 1168-1180

  Puopolo, G ^a   Cimmino, A ^b   Palmieri, M C ^a   Giovannini, O ^a   Evidente, A ^b   Pertot, I ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Anti oomycete activity; Cyclo(l Pro l Tyr); Lysobacter capsici; Phytophthora infestans; Plasmopara viticola

Indexed keywords

FRUITS; KETONES; PLANTS (BOTANY); SPECTROSCOPIC ANALYSIS;

ANTI-OOMYCETE ACTIVITY; CULTURE FILTRATE; CYCLO(L-PRO-L-TYR); IN-VITRO; LYSOBACTER; LYSOBACTER CAPSICI; OOMYCETES; PATHOGENICS; PHYTOPHTHORA INFESTANS; PLASMOPARA VITICOLA;

MOLECULAR WEIGHT;

BACTERIAL DNA; BACTERIAL ENZYME; CYCLO(PROLYLTYROSINE); FUNGICIDE; GENOMIC DNA; NONRIBOSOMAL PEPTIDE SYNTHETASE; PIPERAZINEDIONE; POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG; CYCLOPEPTIDE; MACULOSIN; PIPERAZINE DERIVATIVE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; FUNGICIDAL ACTIVITY; GROWTH INHIBITION; IN VITRO STUDY; LATE BLIGHT; LYSOBACTER; LYSOBACTER CAPSICI; MYCELIAL GROWTH; NONHUMAN; PHYTOPHTHORA CACTORUM; PHYTOPHTHORA CAPSICI; PHYTOPHTHORA CINNAMOMI; PHYTOPHTHORA INFESTANS; PLASMOPARA VITICOLA; PYTHIUM ULTIMUM; SPORANGIUM; TOMATO; CHEMISTRY; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OOMYCETES; PLANT DISEASE;

LYSOBACTER; PHYTOPHTHORA INFESTANS; PLASMOPARA VITICOLA;

FUNGICIDES, INDUSTRIAL; LYCOPERSICON ESCULENTUM; LYSOBACTER; OOMYCETES; PEPTIDES, CYCLIC; PHYTOPHTHORA INFESTANS; PIPERAZINES; PLANT DISEASES; POLYKETIDE SYNTHASES; SPORANGIA;

EID: 84908215975     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12611     Document Type: Article

References (61)

1. Berger, S. and Braun, S. (2004) 200 and More Basic NMR Experiments: A Practical Course, 1st edn. Weinheim: Wiley-VCH.
2. Bernhard, F., Demel, G., Soltani, K., Döhren, H.V. and Blinov, V. (1996) Identification of genes encoding for peptide synthetases in the gram-negative bacterium Lysobacter sp. ATCC 53042 and the fungus Cylindrotrichum oligospermum. DNA Seq 6, 319-330.
3. Bobylev, M.M., Bobyleva, L.I. and Strobel, G.A. (1996) Synthesis and bioactivity of analogs of maculosin, a host-specific phytotoxin produced by Alternaria alternata on spotted knapweed (Centaurea maculosa). J Agric Food Chem 44, 3960-3964.
4. Borthwick, A.D. (2012) 2, 5-Diketopiperazines: synthesis, reactions, medicinal chemistry, and bioactive natural products. Chem Rev 112, 3641-3716.
5. Cain, C.C., Lee, D., Waldo, R.H. III, Henry, A.T., Casida, E.J. Jr, Wani, M.C., Wall, M.E., Oberlies, N.H. et al. (2003) Synergistic antimicrobial activity of metabolites produced by a nonobligate bacterial predator. Antimicrob Agents Chemother 47, 2113-2117.
6. Christensen, P. and Cook, F.D. (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. Int J Syst Bacteriol 28, 367-393.
7. De Rosa, S., Mitova, M. and Tommonaro, G. (2003) Marine bacteria associated with sponge as source of cyclic dipeptides. Biomol Eng 20, 311-316.
8. Degrassi, G., Aguilar, C., Bosco, M., Zahariev, S., Pongor, S. and Venturi, V. (2002) Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing bacterial sensors. Curr Microbiol 45, 250-254.
9. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39, 783-791.
10. Folman, L.B., Postma, J. and van Veen, J.A. (2001) Ecophysiological characterization of rhizosphere bacterial communities at different root locations and plant developmental stages of cucumber grown on rockwool. Microb Ecol 42, 586-597.
11. Folman, L.B., Postma, J. and van Veen, J.A. (2003) Characterization of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal diseases of cucumber. Microbiol Res 158, 107-115.
12. Folman, L.B., De Klein, M.J.E.M., Postma, J. and van Veen, J.A. (2004) Production of antifungal compounds by Lysobacter enzymogenes strain 3.1T8 under different conditions in relation to its efficacy as a biocontrol agent of Pythium aphanidermatum in cucumber. Biol Control 31, 145-154.
13. Fry, W. (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9, 385-402.
14. Fry, W. and Goodwin, S. (1997) Re-emergence of potato and tomato late blight in the United States. Plant Dis 81, 1349-1357.
15. Gessler, C., Pertot, I. and Perazzolli, M. (2011) Plasmopara viticola: a review of knowledge on downy mildew of grapevine and effective disease management. Phytopathol Mediterr 50, 3-44.
16. Guo, Q., Guo, D., Zhao, B., Xu, J. and Li, R. (2007) Two cyclic dipeptides from Pseudomonas fluorescens GcM5-1A carried by the pine wood nematode and their toxicities to Japanese black pine suspension cells and seedling in vitro. J Nematol 39, 243-247.
17. Halfeld-Vieira, B.A., Romeiro, R.S., Mounteer, A. and Mizubuti, E.S.G. (2008) Efficiency of phylloplane bacteria in controlling aerial tomato diseases under field conditions. Summa Phytopathol 34, 64-87.
18. Hayward, A.C., Fegan, N., Fegan, M. and Stirling, G.R. (2010) Stenotrophomonas and Lysobacter: ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. J Appl Microbiol 108, 756-770.
19. Holden, M.T.G., Chhabra, S.R., de Nys, R., Stead, P., Bainton, N.J., Hill, P.J., Manefield, M., Kumar, N. et al. (1999) Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol Microbiol 33, 1254-1266.
20. Homma, Y., Uchino, H., Kanzawa, K., Nakayama, T. and Sayama, M. (1993) Suppression of sugar beet damping-off and production of antagonistic substances by strains of rhizobacteria. Ann Phytopathol Soc Jpn 59, 282.
21. Hou, J., Robbel, L. and Marahiel, M.A. (2011) Identification and characterization of the lysobactin biosynthetic gene cluster reveals mechanistic insights into an unusual termination module architecture. Chem Biol 18, 655-664.
22. Islam, M.T., Hashidoko, Y., Deora, A., Itoi, T. and Tahara, S. (2005) Suppression of damping-off disease in host plants by rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soilborne peronosporomycetes. Appl Environ Microbiol 71, 3786-3796.
23. Jayatilake, G.S., Thornton, M.P., Leonard, A.C., Grimwade, J.E. and Baker, B.J. (1996) Metabolites from an Antarctic sponge-associated bacterium, Pseudomonas aeruginosa. J Nat Prod 59, 293-296.
24. Kato, M., Mizubuti, E.S., Goodwin, S.B. and Fry, W.E. (1997a) Sensitivity to protectant fungicides and pathogenic fitness of clonal lineages of Phytophthora infestans in the United States. Phytopathology 87, 973-978.
25. Kato, A., Nakaya, S., Ohashi, Y. and Hirata, H. (1997b) WAP-8294A(2), a novel anti-MRSA antibiotic produced by Lysobacter sp. J Am Chem Soc 119, 6680-6681.
26. Kimura, M. (1983) The Neutral Theory of Molecular Evolution. Cambridge, UK: Cambridge University Press.
27. Kimura, H., Suzuki, M. and Sumino, Y. (1995) Cloning and expression of the isopenicillin N synthase gene from Lysobacter lactamgenus YK90. J Ferment Bioeng 80, 118-123.
28. Kimura, H., Miyashita, H. and Sumino, Y. (1996) Organization and expression in Pseudomonas putida of the gene cluster involved in cephalosporin biosynthesis from Lysobacter lactamgenus YK90. Appl Microbiol Biotechnol 45, 490-501.
29. Kloepper, J.W., Ryu, C.M. and Zhang, S.A. (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 1259-1266.
30. Ko, H.-S., Jin, R.-D., Krishnan, H.B., Lee, S.-B. and Kim, K.-Y. (2009) Biocontrol ability of Lysobacter antibioticus HS124 against Phytophthora blight is mediated by the production of 4-hydroxyphenylacetic acid and several lytic enzymes. Curr Microbiol 59, 608-615.
31. Kumar, S., Tamura, K. and Nei, M. (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5, 150-163.
32. Lamsal, K., Kim, S.W., Kim, Y.S. and Lee, Y.S. (2013) Biocontrol of late blight and plant growth promotion in tomato using rhizobacterial isolates. J Microbiol Biotechnol 23, 897-904.
33. Li, X.-J., Gao, J.-M., Chen, H., Zhang, A.-L. and Tang, M. (2012) Toxins from a symbiotic fungus, Leptographium qinlingensis associated with Dendroctonus armandi and their in vitro toxicities to Pinus armandi seedlings. Eur J Plant Pathol 134, 239-247.
34. Lourenço Júnior, V., Maffia, L.A., Romeiro, R.S. and Mizubuti, E.S.G. (2006) Biocontrol of tomato late blight with the combination of epiphytic antagonists and rhizobacteria. Biol Control 38, 331-340.
35. Mizubuti, E.S.G., Júnior, V.L. and Forbes, G.A. (2007) Management of late blight with alternative products. Pest Technol 1, 106-116.
36. Musetti, R., Vecchione, A., Stringher, L., Borselli, S., Zulini, L., Marzani, C., D'Ambrosio, M., di Toppi, L.S. et al. (2006) Inhibition of sporulation and ultrastructural alterations of grapevine downy mildew by the endophytic fungus Alternaria alternata. Phytopathology 96, 689-698.
37. Musetti, R., Polizzotto, R., Vecchione, A., Borselli, S., Zulini, L., D'Ambrosio, M., di Toppi, L.S. and Pertot, I. (2007) Antifungal activity of diketopiperazines extracted from Alternaria alternata against Plasmopara viticola: an ultrastructural study. Micron 38, 643-650.
38. Nakayama, T., Homma, Y., Hashidoko, Y., Mizutani, J. and Tahara, S. (1999) Possible role of xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl Environ Microbiol 65, 4334-4339.
39. Nishanth Kumar, S., Mohandas, C., Siji, J.V., Rajasekharan, K.N. and Nambisan, B. (2012) Identification of antimicrobial compound, diketopiperazines, from a Bacillus sp. N strain associated with a rhabditid entomopathogenic nematode against major plant pathogenic fungi. J Appl Microbiol 113, 914-924.
40. Ono, H., Nozaki, Y., Katayama, N. and Okazaki, H. (1984) Cephabacins, new cephem antibiotics of bacterial origin. I. Discovery and taxonomy of the producing organisms and fermentation. J Antibiot 37, 1528-1535.
41. Ortiz-Castro, R., Díaz-Pérez, C., Martínez-Trujillo, M., del Río, R.E., Campos-García, J. and López-Bucio, J. (2011) Transkingdom signalling based on bacterial cyclopeptides with auxin activity in plants. Proc Natl Acad Sci USA 108, 7253-7258.
42. O'Sullivan, J., McCullough, J.E., Tymiak, A.A., Kirsch, D.R., Trejo, W.H. and Principe, P.A. (1988) Lysobactin, a novel antibacterial agent produced by Lysobacter sp. I. Taxonomy, isolation and partial characterization. J Antibiot 41, 1740-1744.
43. Palumbo, J.D., Sullivan, R.F. and Kobayashi, D.Y. (2003) Molecular characterization and expression in Escherichia coli of three beta-1, 3-glucanase genes from Lysobacter enzymogenes strain N4-7. J Bacteriol 185, 4362-4370.
44. Palumbo, J.D., Yuen, G.Y., Jochum, C.C., Tatum, K. and Kobayashi, D.Y. (2005) Mutagenesis of beta-1, 3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95, 701-707.
45. Park, J.H., Kim, R., Aslam, Z., Jeon, C.O. and Chung, Y.R. (2008) Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. Int J Syst Bacteriol 58, 387-392.
46. Puopolo, G., Giovannini, O. and Pertot, I. (2014) Lysobacter capsici AZ78 can be combined with copper to effectively control Plasmopara viticola on grapevine. Microbiol Res 169, 633-642.
47. Raaijmakers, J.M. and Mazzola, M. (2012) Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu Rev Phytopathol 50, 403-424.
48. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
49. Sergeeva, V., Nair, N., Legendre, L., Darley, E. and Spooner-Hart, R. (2002) The use of fluorochromes to determine the effect of chlorine dioxide on survival of Plasmopara viticola on grapevine. Australas Plant Pathol 31, 295-297.
50. Sharma, K., Butz, A.F. and Finckh, M.R. (2010) Effects of host and pathogen genotypes on inducibility of resistance in tomato (Solanum lycopersicum) to Phytophthora infestans. Plant Pathol 59, 1062-1071.
51. Stierle, A., Cardellina, J.H. and Strobel, G.A. (1988) Maculosin, a host-specific phytotoxin for spotted knapweed from Alternaria alternata. Proc Natl Acad Sci USA 85, 8008-8013.
52. Tatsuno, T., Sato, M., Kubota, Y., Kubota, Y. and Tsunoda, H. (1971) Toxicological investigations of metabolic substances of Fusarium nivale. Chem Pharm Bull 19, 1498-1500.
53. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgin, D.G. (1997) The CLUSTAL X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25, 4876-4882.
54. Tilcher, R., Wolf, G.A. and Brendel, G. (1994) Effects of microbial antagonists on leaf infestation, sporangia germination and zoospore behaviour of Plasmopara viticola (Berk. & Curtis) Berl. & de Toni. Mededelingen - Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Universiteit Gent 59, 919-929.
55. Tilcher, R., Schmidt, C., Lorenz, D. and Wolf, G.A. (2002) About the use of antagonistic bacteria and fungi. In 10th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture. Proceedings to the Conference from 4th to 7th February ed. Markus, B., pp. 142-145. Weinsberg/Germany.
56. 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.
57. Trouvelot, S., Varnier, A.L., Allègre, M., Mercier, L., Baillieul, F., Arnould, C., Gianinazzi-Pearson, V., Klarzynski, O. et al. (2008) A β-1, 3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Mol Plant Microbe Interact 21, 232-243.
58. Xie, Y., Wright, S., Shen, Y. and Du, L. (2012) Bioactive natural products from Lysobacter. Nat Prod Rep 29, 1277-1287.
59. Yan, Z., Reddy, M.S., Ryu, C.-M., McInroy, J.A., Wilson, M. and Kloepper, J.W. (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92, 1329-1333.
60. Yu, F., Zaleta-Rivera, K., Zhu, X., Huffman, J., Millet, J.C., Harris, S.D., Yuen, G., Li, X.-C. et al. (2007) Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action. Antimicrob Agents Chemother 51, 64-72.
61. Zhang, W., Li, Y., Qian, G., Wang, Y., Chen, H., Li, Y.Z., Liu, F., Shen, Y. et al. (2011) Identification and characterization of the anti-methicillin-resistant Staphylococcus aureus WAP-8294A2 biosynthetic gene cluster from Lysobacter enzymogenes OH11. Antimicrob Agents Chemother 55, 5581-5589.