Abstract
Extracellular alkalinization and H2O2 production are important early events during induced systemic resistance (ISR) establishment in plants. In a screen for metabolites as potential ISR activators from 98 fungal isolates associated with marine sponge Hymeniacidon perleve, the crude metabolites of fungus Eupenicillium brefeldianum HMP-F96 induced significant extracellular alkalinization coupled with H2O2 production in tobacco cell suspensions. A combined bioactivity and 1H NMR-guided fractionation approach was used to disclose the chemical determinants responsible for the activities. Eight cyclic dipeptides were purified from the fermentation broth of the strain and were structurally characterized by NMR and MS experiments. This study represents the first report of the occurrence of cyclic dipeptides in E. brefeldianum and of their activities of inducing extracellular alkalinization and H2O2 production in tobacco cell suspensions.
References
Bittel P, Robatzek S (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr Opin Plant Biol 10:335–341. doi:10.1016/j.pbi.2007.04.021
Camejo D, Martí MC, Jiménez A, Cabrera JC, Olmos E, Sevilla F (2011) Effect of oligogalacturonides on root length, extracellular alkalinization and O2 −-accumulation in alfalfa. J Plant Physiol 168:566–575. doi:10.1016/j.jplph.2010.09.012
Campbell J, Lin Q, Geske GD, Blackwell HE (2009) New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem Biol 4:1051–1059. doi:10.1021/cb900165y
Coursindel T, Restouin A, Dewynter G, Martinez J, Collette Y, Parrot I (2010) Stereoselective ring contraction of 2,5-diketopiperazines: an innovative approach to the synthesis of promising bioactive 5-membered scaffolds. Bioorg Chem 38:210–217. doi:10.1016/j.bioorg.2010.05.002
Cronan JM, Davidson TR, Singleton FL, Colwell RR, Cardellina JH (1998) Plant growth promoters isolated from a marine bacterium associated with Palythoa sp. Nat Prod Lett 11:271–278. doi:10.1080/10575639808044959
De Rosa S, Mitova M, Tommonaro G (2003) Marine bacteria associated with sponge as source of cyclic peptides. Biomol Eng 20:311–316. doi:10.1016/S1389-0344(03)00038-8
Dhlamini Z, Spillane C, Moss J, Ruane J, Urquia N, Sonnino A (2005) Status of research and application of crop biotechnologies in developing countries: preliminary assessment. Food and Agriculture Organization of the United Nations(FAO), Rome (Italy)
Erbs G, Newman M-A (2003) The role of lipopolysaccharides in induction of plant defence responses. Mol Plant Pathol 4:421–425. doi:10.1046/j.1364-3703.2003.00179.x
Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 4:307–316. doi:10.1046/j.1365-313X.1993.04020307.x
Folkes A, Roe MB, Sohal S, Golec J, Faint R, Brooks T, Charlton P (2001) Synthesis and in vitro evaluation of a series of diketopiperazine inhibitors of plasminogen activator inhibitor-1. Bioorg Med Chem Lett 11:2589–2592. doi:10.1016/S0960-894X(01)00508-X
Furtado NAJC, Pupo MT, Carvalho I, Campo VL, Duarte MCT, Bastos JK (2005) Diketopiperazines produced by an Aspergillus fumigatus Brazilian strain. J Braz Chem Soc 16:1448–1453. doi:10.1590/S0103-50532005000800026
Garbay-Jaureguiberry C, Arnoux B, Prange T, Wehri-Altenburger S, Pascard C, Roques BP (1980) X-ray and NMR studies of l-4-hydroxyproline conformation in oligopeptides related to collagen. J Am Chem Soc 102:1827–1837. doi:10.1021/ja00526a012
Gerber I, Dubery I (2004) Fluorescence microplate assay for the detection of oxidative burst products in tobacco cell suspensions using 2′,7′-dichlorofluorescein. Methods Cell Sci 25:115–122. doi:10.1007/s11022-004-3851-6
Guo Q, Guo D, Zhao B, Xu J, 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 seedlings in vitro. J Nematol 39:243–247
Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103. doi:10.1038/35074106
Holden MTG, Chhabra SR, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg S, Williams P (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. doi:10.1046/j.1365-2958.1999.01577.x
Ienaga K, Nakamura K, Goto T (1987) Bioactive compounds produced in animal tissues (I); two diketopiperadine plant growth regulators containing hydroxyproline isolated from rabbit skin tissue extract. Tetrahedron Lett 28:1285–1286. doi:10.1016/S0040-4039(00)95347-4
Ienaga K, Kurohashi M, Nakamura K, Nakanishi T, Ichii T, Konishi J (1988) Naturally occurring heterocycles inducing drought resistance in plants. Experientia 44:356–357. doi:10.1007/bf01961283
Ienaga K, Nakamura K, Kurohashi M, Nakanishi T, Ichii T (1990) Hydroxyproline-containing diketopiperazines inducing drought resistance in rice. Phytochemistry 29:35–39. doi:10.1016/0031-9422(90)89005-T
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:10.1038/nature05286
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275. doi:10.1146/annurev.arplant.48.1.251
Lenman MM, Lewis A, Gani D (1997) Synthesis of fused 1,2,5-triazepine-1,5-diones and some N2- and N3-substituted derivatives: potential conformational mimetics for cis-peptidyl prolinamides 1. J Chem Soc, Perkin Trans 1:2297–2312. doi:10.1039/a702107k
Mackey D, McFall AJ (2006) MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61:1365–1371. doi:10.1111/j.1365-2958.2006.05311.x
Martins MB, Carvalho I (2007) Diketopiperazines: biological activity and synthesis. Tetrahedron 63:9923–9932. doi:10.1016/j.tet.2007.04.105
McCleland K, Milne PJ, Lucieto FR, Frost C, Brauns SC, Van De Venter M, Du Plessis J, Dyason K (2004) An investigation into the biological activity of the selected histidine-containing diketopiperazines cyclo(His-Phe) and cyclo(His-Tyr). J Pharm Pharmacol 56:1143–1153. doi:10.1211/0022357044139
Mikes V, Milat M-L, Ponchet M, Panabières F, Ricci P, Blein J-P (1998) Elicitins, proteinaceous elicitors of plant defense, are a new class of sterol carrier proteins. Biochem Biophys Res Commun 245:133–139. doi:10.1006/bbrc.1998.8341
O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779. doi:10.1007/s00425-012-1696-9
Ongena M, Jourdan E, Schäfer M, Kech C, Budzikiewicz H, Luxen A, Thonart P (2005) Isolation of an N-alkylated Benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Mol Plant Microbe Interact 18:562–569. doi:10.1094/mpmi-18-0562
Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny J-L, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. doi:10.1111/j.1462-2920.2006.01202.x
Park MR, Kim YC, Lee S, Kim IS (2009) Identification of an ISR-related metabolite produced by rhizobacterium Klebsiella oxytoca C1036 active against soft-rot disease pathogen in tobacco. Pest Manag Sci 65:1114–1117. doi:10.1002/ps.1800
Prasad C (1995) Bioactive cyclic dipeptides. Peptides 16:151–164. doi:http://dx.doi.org/10.1016/0196-9781(94)00017-Z
Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in arabidopsis. Plant Physiol 134:1017–1026. doi:10.1104/pp.103.026583
Saguez J, Dubois F, Vincent C, Laberche J-C, Sangwan-Norreel BS, Giordanengo P (2006) Differential aphicidal effects of chitinase inhibitors on the polyphagous homopteran Myzus persicae (Sulzer). Pest Manag Sci 62:1150–1154. doi:10.1002/ps.1289
Simone TM, Higgins PJ (2012) Low molecular weight antagonists of plasminogen activator inhibitor-1: therapeutic potential in cardiovascular disease. Mol Med Ther 1:101. doi:10.4172/2324-8769.1000102
Stark T, Hofmann T (2005) Structures, sensory activity, and dose/response functions of 2,5-diketopiperazines in roasted cocoa nibs (theobroma cacao). J Agric Food Chem 53:7222–7231. doi:10.1021/jf051313m
Stierle AC, Cardellina JH, Strobel GA (1988) Maculosin, a host-specific phytotoxin for spotted knapweed from Alternaria alternata. Proc Natl Acad Sci USA 85:8008–8011
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347. doi:10.1128/mmbr.00040-06
Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85–88. doi:10.1126/science.1621099
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR-protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Zhang Q, Wang S-Q, Tang H-Y, Li X-J, Zhang L, Xiao J, Gao Y-Q, Zhang A-L, Gao J-M (2013) Potential allelopathic indole diketopiperazines produced by the plant endophytic aspergillus fumigatus using the one strain-many compounds method. J Agric Food Chem 61:11447–11452. doi:10.1021/jf403200g
Acknowledgments
This study was financially supported by National Natural Science Foundation of China (31471814), National High Technology Research and Development Program of China (863 Program, 2011AA09070404) and the National Science and Technology Pillar Program (2011BAE06B04).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, X., Mou, Y., Ling, J. et al. Cyclic dipeptides produced by fungus Eupenicillium brefeldianum HMP-F96 induced extracellular alkalinization and H2O2 production in tobacco cell suspensions. World J Microbiol Biotechnol 31, 247–253 (2015). https://doi.org/10.1007/s11274-014-1759-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-014-1759-0