Isolation and Biological Activity of Cyl-2, a Metabolite of Cylindrocladium scoparium

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1 Agr. Biol. Chem., 37 (3), 643 `647, 1973 Isolation and Biological Activity of Cyl-2, a Metabolite of Cylindrocladium scoparium Akira HIROTA, Akinori SUZUKI, Hiroshi SUZUKI* and Saburo TAMURA Department of Agricultural Chemistry, The University of Tokyo, Bunkyo-ku, Tokyo *Department of Agricultural Chemistry, Kagawa University, Kagawa Received September 20, 1972 Three metabolites designated Cyl-1, -2 and -3 were isolated as plant growth regulators from culture filtrate of Cylindrocladium scoparium Morgan, a phytopathogenic fungus. Cyl-2 was obtained as pure crystals, and it revealed marked inhibitory activity on the root growth of lettuce seedlings. Cyl-1 showed inhibition on the same organ, while Cyl-3 showed promotion. Cyindrocladium scoparium Morgan is a pathogenic fungus to cause various kinds of diseases on higher plants; basal or crown canker in Rosa spp., sheath net-blotch in Oryza sativa L., damping off in Abies spp., Latrix leptolepis Gordon, Pinus densiflora Sieb. et Zucc., Pinus koraiensis Sieb. et Zucc., Cryptomeria japonica D. Don, Acacia dealbata Link and Eucalyptus spp., and so on. Being interested in the biological action of the pathogen, we investigated the probability that the fungus may produce some principles toxic for higher plants. After several trials, we noticed the occurrence of at least three biological active substances designated Cyl-1, -2 and -3 in culture filtrate of the fungus and recently succeeded in isolation of Cyl-2 in crystalline state. The compound completely inhibited the root growth of lettuce seedlings even at a concentration of 30 mg/liter. In this paper we wish to report the isolation and biological activity of these substances, parti cularly of Cyl-2 in detail. Cyl. scoparium was grown in Czapek-Dox medium in stationary culture for 4-6 weeks at 26.5 C. The culture broth (ph 6-7) thus obtained was filtered, and the filtrate was repeatedly extracted with ethyl acetate, which was concentrated in vacuo. As a preliminary experiment, a small amount of the residue was applied to preparative thin-layer chromatography (TLC) using silica gel G and acetonechloroform (2: 3, v/v). After development the chromatoplate was divided into ten equal sections, which were then extracted with acetone. Each extract was bioassayed by use of lettuce seedlings according to the method of Frankland and Wareing!, As shown in Fig. 1, inhibitory activities on root growth were observed at Rf0.1 `0.3 and 0.4 `0.6, and promotive activity at Rf 0.7 `1.0. The substances corresponding to these spots were designated as Cyl-1, -2 and -3, respectively. For large scale preparation of these materials, the residue from the ethyl acetate extract of culture filtrate was subjected to silicic acid adsorption column chromatography. Elu tion was made succesively with benzene and benzene-ethyl acetate increasing stepwise the content of the latter. Then, eluates were bioassayed using lettuce seedlings as mentioned above. Cyl-3 was eluted at first with benzene and then Cyl-2 with benzene containing 40 ethyl acetate. By increasing the ethyl acetate content to 60% (v/v), the fractions containing Cyl-1 were afforded. The isolation procedure is illustrated in Fig. 2. The eluates with benzene showing rootgrowth promotion were rechromatographed by use of a silicic acid column and a solvent system of n-hexane and ethyl acetate (97: 3, v/v) to give an active oil. The oil was further

2 644 A. HIROTA, A. SUZUKI, H. SUZUKI and S. TAMURA purified by TLC using n-hexane containing 2-3% ethyl acetate. Preliminary investiga tion on oily Cyl-3 by TLC using silica gel G and IR spectroscopy suggested that the substance was still a mixture. Biological activity of Cyl-3 was tested by use of lettuce seedlings. It doubled the root elongation at a concentra tion of 200 mg/liter. Further purification of Cyl-3 is in progress. The eluates with 40% ethyl acetate containing Cyl-2 were further purified by preparative TLC by use of silica gel G and acetonechloroform (2: 3, v/v). The dark-purple zone (Rf ca. 0.6) detected under a UV lamp (2537 A) was extracted with acetone, which gave crude Cyl-2 on evaporation. Recrystallization from methanol afforded pure Cyl-2 as colorless FIG. 1. Biological Activity of the Ethyl Acetate Extract from Culture Filtrate of Cylindrocladium scoparium on Lettuce Seedlings. The extract was subjected to TLC by use of acetonechloroform (2: 3, v/v) and bioassayed Control; * Necrosis needles, mp `180.5 Ž, in a yield of 1 mg from 1 liter of the culture broth. Based on high resolution mass spectrometry the molecular formula of Cyl-2 was established as C32H46N4O7. Peptidic nature of the compound was inferred from its IR spectrum (Fig. 3). Its UV absorption maxima at 276 nm (e 1790) and 283 nm (e 1530) suggested the presence of aromatic ring (Fig. 4). The details FIG. 2. Isolation and Purification of Cyl-1, -2 and -3 from Culture Filtrate of Cylindrocladium scoparium.

3 Isolation and Biological Activity of Cyl FIG. 3. Infrared Spectrum of Cyl-2 (Nujol). FIG. 5. Effect of Cyl-2 on the Growth of Lettuce Seedlings Control FIG. 4. UV Spectrum of Cyl-2 (chloroform). of the experiment leading to structure elucida tion of Cyl-2 will be disclosed in the forthcoming papers. Biological activities of Cyl-2 were examined using lettuce and rice seedlings and Avena coleoptiles. As illustrated in Fig. 5, Cyl-2 markedly inhibited the growth of lettuce seedl ings, particularly the root growth. Suppres sion of the root growth was appreciable even at a concentration of 1 mg/liter. Above 30 mg/liter, it completely inhibited the root growth accompanying necrosis. On the other hand, inhibitory effect of Cyl-2 on the hypo cotyl growth was weaker than that observed with the root growth. For rice seedlings, Cyl-2 at a dose of 3.4 mg/liter reduced by 40 the total length (second leaf sheath+second leaf) (Fig. 6). Complete inhibition of the root growth was observed at 34 mg/liter. Besides, Cyl-2 reduced the straight growth FIG. 6. Effect of Cyl-2 on the Growth of Rice Seedlings Control of Avena coleoptile segments induced by simultaneous application of IAA as shown in Fig. 7. At 10 mg/liter the compound reduced the effect of IAA to 70 %. However, Cyl-2 itself, without IAA, did not inhibit the growth

4 646 A. HIROTA, A. SUZUKI, H. SUZUKI and S. TAMURA observed in the root growth rather than in the hypocotyl growth. At 12 mg/liter, Cyl-1 reduced the root elongation to half. Further purification and chemical charac terization of Cyl-1 is now in progress. Participation of Cyl-1, -2 and -3 in the pathogenicity of Cyl. scoparium has not been clarified yet. As described above, however, the marked biological activity of these substances, particularly that of Cyl-2, may sug gest that they play an important role on the host-parasite interaction of the disease, and this problem should be investigated in future from the view point of phytopathology. FIG. 7. Effect of Cyl-2 on the Growth of Avena Coleoptile Segments. IAA solution (1 mg/liter) containing 2% sucrose; œ ucrose solution (2%). EXPERIMENTAL The melting point was measured on a microscope hot plate and reported uncorrected. The UV spectrum was obtained with a Cary spectrophotometer Model 14. The IR spectra were recorded on a JASCO IR-S spectrometer. The mass spectrum was measured with a Hitachi RMH-2 mass spectrometer equipped with a Hitachi datalyzer ) Cultivation of Cyl. scoparium. Cyl. scoparium kept on a potato slant was transferred into 2-liter flasks each containing 1.2 liter of the Czapek-Dox medium composed of sucrose 3.0, NaNO2 0.2, K2HPO4 0.1, KCI 0.05, MgSO4 E7H2O 0.05 and FeSO4 FIG. 8. Infrared Spectrum of Cyl-1 (Film) % and stationarily cultured for 4--6 weeks at 26.5 Ž. of coleoptile segments even at a concentration of 100 mg/liter. The fractions eluted with benzene containing 60% ethyl acetate were rechromatographed on a silicic acid column. Biological activity corresponding to Cyl-1 was detected in an eluate with 60 % ethyl acetate, which was further subjected to preparative TLC using silica gel G and acetone-chloroform (2: 1, v/v). The zone at Rf was eluted with acetone to give crude Cyl-1 as an oil. Al coholic nature was suggested with Cyl-1 based on its IR spectrum (Fig. 8). However, the oil thus obtained still contained some impurities judged from its TLC. The biological activity of Cyl-1 was assayed on lettuce seedlings. Marked inhibition was 2) Isolation of Cyl-1, -2 and -3. The isolation procedure of Cyl-1, -2 and -3 is illustrated in Fig. 2. Forty liters of culture filtrate (ph 6-7) was extracted with two 20-liter portions of ethyl acetate. The combined extracts were concentrated to a small volume under reduced pressure and dried over anhydrous sodium sulfate. Evaporation of the solvent under reduced pressure yielded 2.0 g of a brown paste. The paste was mixed with 1.5 g of Celite 545 (Johns-Manville Co.) and applied onto a column (3.3 ~50cm) packed with 60 g of silicic acid (Mallinckrodt). The column was eluted at first with benzene and then benzeneethyl acetate increasing stepwise the content of the latter. On evaporation under reduced pressure, the eluates with benzene yielded 1.0 g of a brown oil, which showed promotive activity on lettuce seedlings. This oil was chromatographed by use of silicic acid and a solvent system of n-hexane and ethyl acetate (97: 3, v/v) to give an active oil (140 mg), Cyl-3, which was still a mixture judging from TLC and its IR spectrum.

5 Isolation and Biological Activity of Cyl The eluate with benzene-ethyl acetate (60: 40) showed inhibitory activity on lettuce seedlings. When a small portion of the eluate was subjected to TLC using Silica Gel GF254 (Merck) plate of 0.25 mm thickness and chloroform-acetone (3: 2, v/v), a dark-purple spot corresponding to Cyl-2 was detected at Rf 0.6 under a UV lamp (2537 A). Then, the eluate was evaporated under reduced pressure and subjected to preparative TLC using a plate of 0.5 mm thickness. The dark-purple zone detected under a UV lamp (2537 A) was extracted with acetone, which was evaporated to yield 50 mg of crude Cyl-2. Recrystallization from methanol gave about 40 mg of colorless crystals. mp `180.5 Ž. The eluate with benzene-ethyl acetate (40: 60) gave an oil (130 mg) showing inhibitory activity on lettuce seedlings, and the oil was rechromatographed on a silicic acid column. The fractions eluted with benzene containing 60%. ethyl acetate were evaporated to yield 57 mg of a brown oil, which was further subjected to preparative TLC using Silica Gel GF254 (Merck) and acetone-chloroform (2: 1, v/v). The zone at Rf was eluted with acetone to give crude Cyl-1 as an oil, 8.5 mg. 3) Physicochemical properties of Cyl-2. Cyl-2 thus obtained gave a single spot on TLC using various solvent systems as illustrated in Table I. UV_??_ nm(s): 276 (1790), 283 (1530). IR _??_ cm-1: 3250, 2910, 2850, 1710, 1650, 1635, 1515, 1460, 1380, 1310, MS (molecular ion peak), m/e: (Calcd. for C32H46N4O7, ). Cyl-2 was positive to 2,4- dinitrophenylhydrazine. It decolorized aqueous potassium permanganate solution and showed yellowgreen coloration with the chlorine-ƒí-tolidine-potassium iodide reagent. a sheet of filter paper placed in a 6cm-Petri dish. After spontaneous evaporation of the solvent to dryness, 3 ml of doubly diluted Hoagland's nutrient solution was poured into the dish. Then, twelve lettuce seedlings (Lactuca sativa L., cv. Great Lakes), which had been germinated in distilled water at 26 Ž for one day, were transferred onto the filter paper. After incubation at 25 Ž under continuous light (ca lux) for three days, the growth of hypocotyls and roots was measured. The results are shown in Fig. 5. b) For rice seedlings. A definite amount of the sample was dissolved in acetone and poured onto a sheet of absorbent cotton placed in a 6 cm-petri dish. The solvent was evaporated to dryness spontaneously, and 10 ml of doubly diluted Hoagland's nutrient solu tion was poured into the dish. Twelve rice seedlings (Ory=a sativa L., cv. Tonewase), which had been ger minated in distilled water at 30 Ž for two days, were put there. After incubation at 25 Ž for seven days under continuous light (ca lux), the growth of roots, second sheaths and leaves were observed. The results are shown in Fig. 6. c) For Avena coleoptile segments. A definite amount of the sample dissolved in acetone was poured onto a sheet of filter paper placed in a 4.5cm-Petri dish. After spontaneous evaporation of the solvent to dryness, 2.5ml of an aqueous solution containing 2.5ƒÊg of IAA and 2% sucrose was poured there. Seven coleoptile segments (5 mm), which were excised from oat seedlings (Avena sativa L., var. Russell) grown for 3 days under red light at 26.5 Ž, were floated in the dish. After incubation at 26.5 Ž for 20 hr in the dark, the growth of segments was measured. The results are illustrated in Fig. 7. TABLE L Rf VALUES OF Cyl-2 IN SILICA GEL THIN-LAYER CHROMATOGRAPHY Acknowledgements. We wish to express our thanks to Dr. K. Ito of the Government Forest Experiment Station for the gift of Cyl. scoparium strains. We are also grateful to Mr. K. Aizawa of this Department for the measurements of UV, IR and MS spectra. We are indebted to Mr. H. Sonobe for his technical assistance. 4) Assay of biological activities. a) For lettuce seedlings. A definite amount of the sample was dissolved in acetone and poured onto REFERENCE 1) B. Frankland and P. F. Wareing, Nature, 185, 255 (1960).

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