Paraconiothyrium variabile, one of the specific endophytic fungi isolated from the host plant Cephalotaxus harringtonia, possesses the faculty to inhibit the growth of common phytopathogens, thus suggesting a role in its host protection. A strong antagonism between the endophyte P. variabile and Fusarium oxysporum was observed and studied using optic and electronic microscopies. A disorganization of the mycelium of F. oxysporum was thus noticed. Interestingly, the biological effect of the main secondary metabolites isolated from P. variabile against F. oxysporum did not account for this strong antagonism. However, a metabolomic approach of pure fungal strains and confrontation zones using the data analysis tool XCMS were analyzed and pointed out a competition-induced metabolite production by the endophyte in the presence of the phytopathogen. Subsequent MS/MS fragmentations permitted to identify one of the induced metabolites as 13-oxo-9,11-octadecadienoic acid and highlighted a negative modulation of the biosynthesis of beauvericin, one of the most potent mycotoxin of F. oxysporum, during the competition with the endophyte.
References
[1]
Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, et al. (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100: 15649–15654.
[2]
Schulz B, Rommert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103: 1275–1283.
[3]
Gimenez C, Cabrera R, Reina M, Gonzalez-Coloma A (2007) Fungal endophytes and their role in plant protection. Curr Org Chem 11: 707–720.
[4]
Prado S, Li Y, Nay B (2011) Diversity and Ecological Significance of Fungal Endophyte Natural Products. In: Atta-Ur-Rahman, editor. Studies in Natural Products Chemistry: Elsevier Science Publishers-Amsterdam.
[5]
Wicklow DT, Roth S, Deyrup ST, Gloer JB (2005) A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides. Mycol Res 109: 610–618.
[6]
Heilmann-Clausen J, Boddy L (2005) Inhibition and stimulation effects in communities of wood decay fungi: Exudates from colonized wood influence growth by other species. Microb Ecol 49: 399–406.
[7]
Evanno L, Jossang A, Nguyen-Pouplin J, Delaroche D, Herson P, et al. (2008) Further studies of the norditerpene (+)-harringtonolide isolated from Cephalotaxus harringtonia var. drupacea: absolute configuration, cytotoxic and antifungal activities. Planta Med 74: 870–872.
[8]
Bocar M, Jossang A, Bodo B (2003) New alkaloids from Cephalotaxus fortunei. J Nat Prod 66: 152–154.
[9]
Powell RG, Rohwedder WK, Smith JCR, Weisleder D (1970) Structures of harringtonine, isoharringtonine, and homoharringtonine. Tetrahedron Lett 11: 815–818.
[10]
Langenfeld A, Prado S, Nay B, Porcher E, Cruaud C, et al.. (2012) Geographic locality greatly influences fungal endophyte communities in Cephalotaxus harringtonia. Fungal Biol Accepted.
[11]
Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G (2006) XCMS: Processing mass spectrometry data for metabolite profiling using Nonlinear peak alignment, matching, and identification. Anal Chem 78: 779–787.
[12]
Smith CA, O’Maille G, Want EJ, Qin C, Trauger SA, et al. (2005) METLIN - A metabolite mass spectral database. Ther Drug Monit 27: 747–751.
[13]
Evidente A, Superchi S, Cimmino A, Mazzeo G, Mugnai L, et al. (2011) Regiolone and Isosclerone, two enantiomeric phytotoxic naphthalenone pentaketides: computational assignment of absolute configuration and its relationship with phytotoxic activity. Eur J Org Chem 28: 5564–5570.
[14]
Dufour C, Loonis M (2005) Regio- and stereoselective oxidation of linoleic acid bound to serum albumin: identification by ESI-mass spectrometry and NMR of the oxidation products. Chemistry and Physics of Lipids 138: 60–68.
[15]
Feng SB, Saw CL, Lee YK, Huang DJ (2007) Fungal-stressed germination of black soybeans leads to generation of oxooctadecadienoic acids in addition to glyceollins. J Agric Food Chem 55: 8589–8595.
[16]
Christensen SA, Kolomiets MV (2011) The lipid language of plant-fungal interactions. Fungal Genet Biol 48: 4–14.
[17]
Song HH, Lee HS, Lee GP, Ha SD, Lee C (2009) Structural analysis of enniatin H, I, and MK1688 and beauvericin by liquid chromatography-tandem mass spectrometry (LC-MS/MS) and their production by Fusarium oxysporum KFCC 11363P. Food Addit Contam A 26: 518–526.
[18]
Liu L, Gao H, Chen XL, Cai XY, Yang LL, et al.. (2010) Brasilamides A-D: Sesquiterpenoids from the Plant Endophytic Fungus Paraconiothyrium brasiliense. Eur J Org Chem: 3302–3306.
[19]
Shiono Y, Kikuchi M, Koseki T, Murayama T, Kwon E, et al. (2011) Isopimarane diterpene glycosides, isolated from endophytic fungus Paraconiothyrium sp MY-42. Phytochemistry 72: 1400–1405.
[20]
Soliman SSM, Tsao R, Raizada MN (2011) Chemical Inhibitors Suggest Endophytic Fungal Paclitaxel Is Derived from Both Mevalonate and Non-mevalonate-like Pathways. J Nat Prod 74: 2497–2504.
[21]
Fujimoto H, Nagano J, Yamaguchi K, Yamazaki M (1998) Immunosuppressive components from an ascomycete, Diplogelasinospora grovesii. Chem Pharm Bull 46: 423–429.
[22]
Laurent D, Guella G, Mancini I, Roquebert MF, Farinole F, et al. (2002) A new cytotoxic tetralone derivative from Humicola grisea, a filamentous fungus from wood in the southeastern lagoon of New Caledonia. Tetrahedron 58: 9163–9167.
[23]
Morita M, Nakanishi H, Morita H, Mihashi S, Itokawa H (1996) Structures and spasmolytic activities of derivatives from sesquiterpenes of Alpinia speciosa and Alpinia japonica. Chem Pharm Bull 44: 1603–1606.
[24]
Dong JY, Song HC, Li JH, Tang YS, Sun R, et al. (2008) Ymf 1029A–E, preussomerin analogues from the fresh-water-derived fungus YMF 1.01029. J Nat Prod 71: 952–956.
[25]
Iwasaki S, Muro H, Sasaki K, Nozoe S, Okuda S, et al. (1973) Isolations of phytotoxic substances produces by Pyricularia-oryzae cavara. Tetrahedron Lett 37: 3537–3542.
[26]
Knight DW, Portas CD (1977) Total synthesis of +/？ Iso-ochracinic acid, hydroxy phtalide from Alternaria kikuchiana Tetrahedron Lett. 18: 4543–4544.
[27]
Ballio A, Barcello S, Santurba B (1966) 5-Methylmellein a new natural dihydroisocoumarin. Tetrahedron Lett 7: 3723–3725.
[28]
Kokubun T, Veitch NC, Bridge PD, Simmonds MSJ (2003) Dihydroisocoumarins and a tetralone from Cytospora eucalypticola. Phytochemistry 62: 779–782.
[29]
Leao PN, Pereira AR, Liu WT, Ng J, Pevzner PA, et al. (2010) Synergistic allelochemicals from a freshwater cyanobacterium. Proc Natl Acad Sci U S A 107: 11183–11188.
[30]
Singh SK, Strobel GA, Knighton B, Geary B, Sears J, et al. (2011) An endophytic Phomopsis sp possessing bioactivity and fuel potential with its volatile organic compounds. Microb Ecol 61: 729–739.
[31]
Macias-Rubalcava ML, Hernandez-Bautista BE, Oropeza F, Duarte G, Gonzalez MC, et al. (2010) Allelochemical Effects of Volatile Compounds and Organic Extracts from Muscodor yucatanensis, a Tropical Endophytic Fungus from Bursera simaruba. J Chem Ecol 36: 1122–1131.
[32]
Oh DC, Jensen PR, Kauffman CA, Fenical W (2005) Libertellenones A-D: induction of cytotoxic diterpenoid biosynthesis by marine microbial competition. Bioorg Med Chem 13: 5267–5273.
[33]
Oh DC, Kauffman CA, Jensen PR, Fenical W (2007) Induced production of emericellamides A and B from the marine-derived fungus Emericella sp. in competing co-culture. J Nat Prod 70: 515–520.
[34]
Park HB, Kwon HC, Lee CH, Yang HO (2009) Glionitrin A, an antibiotic-antitumor metabolite derived from competitive interaction between abandoned mine microbes. J Nat Prod 72: 248–252.
[35]
Zhang CL, Zheng BQ, Lao JP, Mao LJ, Chen SY, et al. (2008) Clavatol and patulin formation as the antagonistic principle of Aspergillus clavatonanicus, an endophytic fungus of Taxus mairei. Appl Microbiol Biotechnol 78: 833–840.
[36]
Schroeckh V, Scherlach K, Nutzmann HW, Shelest E, Schmidt-Heck W, et al. (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106: 14558–14563.
[37]
Young CA, Bryant MK, Christensen MJ, Tapper BA, Bryan GT, et al. (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol Genet Genom 274: 13–29.
[38]
Estrada AER, Hegeman A, Kistler HC, May G (2011) In vitro interactions between Fusarium verticillioides and Ustilago maydis through real-time PCR and metabolic profiling. Fungal Genet Biol 48: 874–885.
[39]
Glauser G, Gindro K, Fringeli J, De Joffrey JP, Rudaz S, et al. (2009) Differential analysis of mycoalexins in confrontation zones of grapevine fungal pathogens by ultrahigh pressure liquid chromatography/time-of-flight mass spectrometry and capillary nuclear magnetic resonance. J Agric Food Chem 57: 1127–1134.
[40]
Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15: 109–118.
[41]
Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez MJ, et al. (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol 139: 1902–1913.
[42]
Tsitsigiannis DI, Keller NP (2006) Oxylipins act as determinants of natural product biosynthesis and seed colonization in Aspergillus nidulans. Mol Microbiol 59: 882–892.
[43]
Fox EM, Howlett BJ (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11: 481–487.
[44]
Reverberi M, Ricelli A, Zjalic S, Fabbri AA, Fanelli C (2010) Natural functions of mycotoxins and control of their biosynthesis in fungi. Appl Microbiol Biotechnol 87: 899–911.
