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Penicillium Digitatum Metabolites on Synthetic Media and Citrus Fruits

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Penicillium Digitatum Metabolites on Synthetic Media and Citrus Fruits J. Agric. Food Chem. 2002, 50, 6361−6365 6361 Penicillium digitatum Metabolites on Synthetic Media and Citrus Fruits MARTA R. ARIZA,† THOMAS O. LARSEN,‡ BENT O. PETERSEN,§ JENS Ø. DUUS,§ AND ALEJANDRO F. BARRERO*,† Department of Organic Chemistry, University of Granada, Avdn. Fuentenueva 18071, Spain; Mycology Group, BioCentrum-DTU, Søltofts Plads, Technical University of Denmark, 2800 Lyngby, Denmark; and Carlsberg Research Laboratory, Gamle Carlsberg Vej 10, DK-2500 Valby, Denmark Penicillium digitatum has been cultured on citrus fruits and yeast extract sucrose agar media (YES). Cultivation of fungal cultures on solid medium allowed the isolation of two novel tryptoquivaline-like metabolites, tryptoquialanine A (1) and tryptoquialanine B (2), also biosynthesized on citrus fruits. Their structural elucidation is described on the basis of their spectroscopic data, including those from 2D NMR experiments. The analysis of the biomass sterols led to the identification of 8-12. Fungal infection on the natural substrates induced the release of citrus monoterpenes together with fungal volatiles. The host-pathogen interaction in nature and the possible biological role of citrus volatiles are also discussed. KEYWORDS: Citrus fruits; Penicillium digitatum; quivaline metabolites; tryptoquivaline; P. digitatum sterols; phenylacetic acid derivatives; volatile metabolites INTRODUCTION obtained from a Hewlett-Packard 5972A mass spectrometer using an ionizing voltage of 70 eV, coupled to a Hewlett-Packard 5890A gas P. digitatum grows on the surface of postharvested citrus fruits chromatograph. producing a characteristic powdery olive-colored conidia and Preparation of TMS Derivatives and Analysis by GC-MS. TMS is commonly known as green-mold. This pathogen is of main derivatives were obtained according to the procedure previously concern as it is responsible for 90% of citrus losses due to described (7). The samples (1 µL) were injected onto a 25 m × 0.32 diseases occurring during the storage period, and it causes mm i.d. HP-1 methylsilicone capillary column with a He flow rate of serious damages in commerce (1). Most of the research works 0.6 mL min-1. The temperature program for the study of sterols and on P. digitatum focus on treatments against the infection oxygenated triterpenes went from 120 °Cto220°Cat5°C min-1, symptoms, and literature about fungal metabolites is scarce (2, from 220 °Cto280°Cat3°C min-1, and 10-min hold at 280 °C. 3). To extend the study of P. digitatum metabolites and their Identification of the sterols and oxygenated triterpenes from P. digitatum possible role in the toxigenesis, as well as to know more about biomass has been made by interpretation of the characteristic mode of medium-pathogen relation, the microorganism has been cul- fragmentation of their TMS-ethers when subjected to GC-MS (7-9), tured on natural and synthetic media. Several metabolites have and by comparison of RI and mass spectra with those from standards. been isolated and studied by NMR. Fungal Material and Fermentation. P. digitatum IBT 10051 and IBT 21830 isolates, (ex Mandarin), were obtained from the fungal MATERIALS AND METHODS culture collection (IBT) at BioCentrum-DTU, at The Technical University of Denmark. General Experimental Procedures. NMR spectra were recorded P. digitatum Cultured on YES Liquid Medium. IBT 10051 was in DMSO on a Bruker DRX 600, at 600.13 MHz for 1H and 150.92 cultured on YES liquid medium, (20 g of yeast extract and 150 g of MHz for 13C according to Larsen et al. (4). The chemical shifts are sucrose in 1000 mL of distilled water). The fungus was inoculated into given relative to DMSO, 2.50 ppm for H1 and 39.5 ppm for C13 (Table 1). The circular dichroism (CD) spectra were measured on a JASCO 50 500-mL Erlenmeyer flasks (100 mL of YES medium per flask) and ° J-710 spectropolarimeter and the UV spectra were measured on a grown in the dark with shaking at 24 C for 15 days. Hewlett-Packard 8452A diode array spectrophotometer. Analytical P. digitatum Cultured on YES Solid Medium. IBT 21830 was cultured HPLC conditions were similar to those given by Smedsgaard (5), and for 14 days at 25 °C in the dark, as three-point mass inoculation on retention indices (RI) of fungal metabolites were calculated according 200 YES agar plates (2). to Frisvad and Thrane (6). EIMS for the study of citrus volatiles were P. digitatum Cultured on Citrus Fruits. IBT 21830 was cultured on citrus fruits (Valencia oranges) for production of both volatile and * To whom correspondence should be addressed. Phone: 958 24 33 20. nonvolatile metabolites. The citrus fruits were inoculated at several Fax: 958 24 33 20. E-mail: [email protected]. points and cultivated at 25 °C. † University of Granada. ‡ University of Denmark. Collection of Volatile Metabolites. Volatile metabolites were § Carlsberg Research Laboratory. collected by diffusive sampling onto Tenax TA and analyzed by GC- 10.1021/jf020398d CCC: $22.00 © 2002 American Chemical Society Published on Web 09/20/2002 6362 J. Agric. Food Chem., Vol. 50, No. 22, 2002 Ariza et al. Table 1. NMR Data of Tryptoquialanine A (1) in DMSO-d6 no 13C 1H (mult., J ) Hz) HMBC NOESY 2 84.0 5.23 (sa) H-13, 16-NOH H-13b 3 85.6 H-2, H-5, H-13 4 134.4 H-6, H-8 5 125.5 7.91 (dd, 8.5, 1.1) H-7 H-6, H-12, H-13a 6 125.2 7.31 (ddd, 8.5, 6.8, 1.8) H-8 H-5, H-7 7 131.5 7.52 (ddd, 7.9, 6.8, 1.1) H-5 H-6, H-8 8 114.8 7.52 (dd, 7.9, 1.8) H-6 H-7 9 137.2 H-5, H-7 11 170.0 H-12, H-13 12 54.5 5.92 H-13 H-5, H-13a, H-27 13 34.3 3.13 (dd, 13.4, 10.0) H-2, H-12 3.08 (dd, 13.4, 10.0) 14 170.8 H-2, H-29, H-30 15 70.7 16-NOH, H-29, H-30 -NOH 7.95 (sa) 18 160.5 H-12, H-20 19 119.9 H-21, H-23 20 126.3 8.18 (ddd, 8.1, 1.5, 0.5) H-22 H-21 21 128.1 7.64 (td, 8.1, 1.1) H-23 H-20, H-22 22 135.6 7.94 (td, 8.1, 1.5) H-20 H-21, H-23 23 127.5 7.77 (ddd, 8.1, 1.1, 0.5) H-21 H-22 24 146.0 H-20, H-22 26 154.9 H-12, H-27, H-28 27 68.5 6.31 (q, 6.3) H-28 H-12 CH3COO- 170.1 CH3COO, H-27 CH3COO- 20.7 2.08 (s) 28 18.7 1.70 (d, 6.3) 29 22.9 1.32 (s) H-30 30 16.8 1.35 (s) H-29 MS according to Larsen and Frisvad (10) except that citrus fruits were 0:100 in 40 min) with a mobile phase at 20 mL/min flow rate, to give placed in glass exicators fitted with cotton stoppers, instead of in Petri 37.7 mg of 2-hydroxyphenylacetic acid methyl ester (5), 88.2 mg of 6, dishes. and 22.5 mg of phenylacetic acid (7). Extraction and Separation. P. digitatum Cultured on YES Liquid P. digitatum Cultured on Citrus Fruits. Fungal spores and mycelium Medium. After the incubation period of IBT 10051 the fungal mycelium were scraped off the highly molded citrus fruits with a knife and was removed by vacuum filtration, lyophilized, and weighed, giving transferred into a glass vial in which they were extracted with 2 mL of 14.207 g of dried biomass per L of culture. Dried mycelium (71 g) MeOH. This extract was filtered through a 0.45-µm filter and then was ground and extracted first with CHCl3 (4 × 1.5 L) to give 7.814 analyzed by HPLC-DAD according to Smedsgaard (5). g of chloroform extract, and then extracted with MeOH (4 × 1.5 L), Tryptoquialanine A (1). HREIMS m/z (rel intensity) found 518.1801 + 22 yielding 60.380 g. The chloroform fraction (6 g) was chromatographed (100) [calcd for C27H26O7N4, 518.1801 (M )]. [R] D ) 0° (c 0.09, over an Al2O3 column, using hexane/MTBE mixtures of increasing EtOH). UV λmax (EtOH) nm (log ∈) 222 (4.48), 225 (4.49), 273 (sh polarity. Sterol esters (270 mg) were eluted with hexane/MTBE (80: 3.90), 289 (sh 3.69), 298 (sh 3.54), 310 (sh 3.39). CD (EtOH, c 0.02), 20), whereas free sterols (75 mg), were eluted with mixtures of hexane/ ∆∈ (λ nm) 215 (+13.15), 228 (-4.24), 240 (-2.12), 252 (-4.45), MTBE (50:50 to 30:70). Sterol esters were saponified, and the 290 (0.00). NMR, Table 1. nonsaponifiable fraction was derivatized and analyzed by GC-MS Tryptoquialanine B (2). HREIMS m/z (rel intensity) found 504.1645 + 22 together with the free sterols. Cholesterol (8), ergosta-7,22-dien-3â- (100) [calcd for C26H24O7N4, 504.1645 (M )]. [R] D )+57.1° (c 0.14, OH (9), ergosta-7,22,24(28)-trien-3â-OH (10), episterol (11), and EtOH). UV λmax (EtOH) nm (log ∈) 220 (4.48), 225 (4.49), 272 (sh eburicol (12) were identified in the sterol ester fraction, whereas 8 and 3.88), 286 (sh 3.67), 296 (sh 3.53), 311 (sh 3.43). CD (EtOH, c 0.03), 12 were found in the free sterol and oxygenated triterpene fraction. ∆∈ (λ nm) 216 (+11.13), 234 (-2.07), 236 (-1.13), 252 (-4.70), P.
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