1. Introduction. 2. Studies on Natural Cyanamide W3-11
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1 Cyanamide Contained in Several Fabaceae Plants Tsunashi Kamo National Institute for Agro-Environmental Sciences Kan-nondai, Tsukuba, Ibaraki , Japan Abstract: Cyanamide (NH 2 CN) has been synthesized for over a hundred years for agricultural and industrial uses. In 2001, this compound was isolated from the leaves and stems of Vicia villosa subsp. varia (Host) Corb., using plant growth inhibitory activity against lettuce Lactuca sativa L. seedlings as an isolation guide. A large proportion of the inhibitory activity in the crude extract of V. villosa subsp. varia was explained by the presence of cyanamide, suggesting that this compound could be a possible allelochemical in this species. This was the first isolation of cyanamide from natural sources. To demonstrate that the cyanamide was of natural origin, [ 15 N]nitrate was administered to V. villosa subsp. varia seedlings, from which cyanamide was purified and subjected to GCMS analysis. The isotopic ratio of 15 N in the cyanamide was significantly higher than that of the cyanamide extracted from the seedlings grown in the presence of a natural N source. This 15 N-enrichment established the presence of natural cyanamide. The distribution of natural cyanamide in the plant kingdom appears to be limited, as indicated by our investigation on 101 weed species. We investigated 553 species in total but have so far found only three species with the ability to biosynthesize cyanamide at detectable levels, V. villosa subsp. varia, V. cracca L., and Robinia pseudo-acacia L. Keywords: Cyanamide, Allelopathy, Vicia villosa subsp. varia, Robinia pseudo-acacia 1. Introduction Cyanamide (NH 2 CN) has been produced industrially in large quantities for more than a hundred years. In the form of its calcium salt, synthesized from calcium carbide and nitrogen gas under high temperature and at high pressure, it was first produced in Germany in 1898, as the first artificial fertilizer. It works as a pesticide, fungicide, nematocide, and herbicide if it is applied to soils, where it is biologically converted into inorganic nitrogen sources available to plants. This multi-functional agrochemical is also active in halting the dormancy of fruit buds [1]. The inducible enzyme in the soil fungus Myrothecium verrucaria, which specifically hydrates cyanamide, has been characterized in detail [2]. Its high specificity was surprising, since cyanamide had never been found in nature [3]. Vicia villosa subsp. varia (Host) Corb., a leguminous plant, is utilized for efficiently suppressing weed growth in winter in the United States [4] and as a cover crop in orchards and abandoned paddy fields in Japan [5]. In addition, it supplies a large amount of nitrogen to the soil and prevents evaporation of water and soil erosion [6]. Weed growth inhibition by chemical components in this plant has been regarded as an important factor in weed suppression, as well as competition for light, nutrients, and water [7,8]. Although the extract of the leaves showed stronger phytotoxicity than those of many other plants [5,7,9], none of the plant growth inhibitors was identified. To examine whether allelopathy is involved in weed growth suppression, the possible allelochemicals of this crop should be identified. During the course of investigating the plant growth inhibitors in V. villosa subsp. varia, we isolated cyanamide as a major inhibitory compound [10]. To exclude any possibility that the cyanamide isolated from this plant was an artifact, we demonstrated its natural occurrence by a feeding experiment using [ 15 N]nitrate [11]. Distribution of cyanamide in the plant kingdom was the subject investigated because knowledge of this could enable us to understand the physiological function of cyanamide in plants, obtain plant material suitable for biosynthetic study, and investigate the genetic code of cyanamide biosynthesis. To conduct a survey that would serve our purpose, we established a direct quantitative determination method to detect and measure cyanamide by stable isotope dilution gas chromatography-mass spectrometry [12]. Using this method, we conducted a preliminary study, analyzing 101 species of common weeds in Japan [13]. Then we conducted an extensive survey of 452 species of higher plants in order to clarify the distribution of cyanamide-biosynthesizing species [14]. In the present paper, we describe (1) the first isolation of cyanamide from plants, (2) demonstration of the natural occurrence of cyanamide, and (3) limited distribution of natural cyanamide in higher plants. 2. Studies on Natural Cyanamide 1) First Isolation of Cyanamide from Plants The crude extract of fresh leaves and stems of V. villosa subsp. varia showed inhibitory activity on the hypocotyl elongation of lettuce Lactuca sativa L. seedlings. This plant growth inhibitory activity was used as an isolation guide for all fractionation procedures. The amounts of samples used for the bioassay were calculated on the basis of the fresh weight of the extract. The fraction showing the strongest activity was further fractionated chromatographically, finally yielding a major plant growth inhibitory compound. This compound showed only one broad signal at δ 5.39 in the 1 H NMR spectrum (600 MHz, acetone-d 6 ), corresponding to a proton on the NH group based on the chemical 1
2 shift value and broadened peak shape. The UV spectrum consisted of end absorption only. The IR spectrum of this compound suggested the presence of NH (3384 and 1630 cm 1 ) and nitrile (2260 cm 1 ) groups from the absorbent bands. Only one signal at δ was observed in the 13 C NMR spectrum (150 MHz, MeOH-d 4 ) and assigned to a carbon on the nitrile group based on the chemical shift value (Figure 1). Comparison with the 13 C NMR spectra for dicyandiamide (Figure 1A) and cyanamide (Figure 1B) indicated that the isolated material (Figure 1C) was cyanamide containing a small portion of its dimer, dicyandiamide. A NH 2 C(=NH)NHCN B NH 2 CN C Figure 1. The 13 C NMR spectra (150 MHz, acetone-d 6 ) for (A) dicyandiamide, (B) cyanamide, and (C) the material isolated from Vicia villosa subsp. varia. Relative Intensity (%) 100 A [M] + (100.0) B [M+1] + (2.4) [M] + (100.0) 50 0 [M+1] + (20.7) [M+2] + (8.8) m/z Figure 2. The mass spectra on GCMS analysis corresponding to cyanamide isolated from 5-week-old seedlings of Vicia villosa subsp. varia treated with (A) non-labeled and (B) 15 N-labeled potassium nitrate (3.4 mm) for 3 weeks. The values in parentheses indicate the relative intensities of the positive ions. 2
3 Table 1. Cyanamide content in 553 species of higher plants. Family Genus Species Cyanamide content * (μg g 1 fresh wt) Fabaceae Robinia R. luxurians <1 R. pseudo-acacia 46 ± 7 Vicia V. amoena <1 V. amurensis <1 V. angustifolia <1 V. cracca 3526 ± 61 V. hirsuta <1 V. japonica <1 V. pseudo-orobus <1 V. unijuga <1 V. villosa subsp. varia 449 ± genera <1 141 families 373 genera <1 *Values are means ± standard deviations (n = 3). It was confirmed that the plants used for the isolation of the plant growth inhibitor contained 130 μg of cyanamide g 1 fresh wt. The crude extract and authentic cyanamide were compared with regard to their ability to inhibit the growth of lettuce hypocotyls on the basis of their cyanamide concentration. At all concentrations examined, the growth inhibition of the crude extract on the lettuce hypocotyls was explained by the presence of cyanamide contained in the extract. This result suggests that cyanamide could be a major allelochemical in V. villosa subsp. varia. 2) Demonstration of Natural Occurrence of Cyanamide Cyanamide has been produced industrially and utilized for drugs and agrochemicals, but is not considered to occur naturally. At the early stage of this study, it was not certain whether the cyanamide isolated was from a natural source, since unexpected contamination by artificial forms might be possible in the field. To exclude this possibility, two-week-old seedlings of V. villosa subsp. varia were grown for another 3 weeks in an illuminated growth chamber with the administration of a 3.4 mm potassium [ 15 N]nitrate aqueous solution. As a control, non-labeled potassium nitrate (3.4 mm) was administered to another group of 2-week-old seedlings for another 3 weeks. The acetone extract of the 5-week-old plants was successively passed through cartridge columns. The eluate was purified by preparative HPLC to give cyanamide, which was then analyzed by GCMS. A peak corresponding to cyanamide was detected at t R 8.1 min in the total ion chromatogram from GCMS. The mass spectrum of cyanamide isolated from plants treated with non-labeled potassium nitrate showed the [M] + ion at m/z 42 at 100% of the relative intensity (Figure 2A). The relative intensity of the [M+1] + ion at m/z 43 was 2.4% (theoretical relative intensity; 1.8%). The mass spectrum of cyanamide isolated from the plants treated with [ 15 N]nitrate was characterized by enhancements of the relative intensity of the ion at m/z 43 (20.7%; Figure 2B). The relative intensity of the ion at m/z 44, which was at a negligible level in the control mass spectrum (0.2%; Figure 2A), was distinctly strengthened to 8.8% in that of cyanamide isolated from the [ 15 N]nitrate-treated plants. The isotopic ratio of 15 N in total N of the cyanamide which was isolated from the [ 15 N]nitrate-treated plants was calculated to be 0.143, while that of the control was (theoretically; ), indicating that nitrogen atoms of cyanamide were labeled with 15 N by [ 15 N]nitrate administration. This observation proved the presence of natural cyanamide. 3) Limited Distribution of Natural Cyanamide in Higher Plants Of the 101 species tested, cyanamide was detected only in two Vicia species. Vicia villosa subsp. varia and V. cracca contained cyanamide at 449 ± 70 μg g 1 fresh wt and 3526 ± 61 μg g 1 fresh wt, respectively (Table 1). Other Vicia species tested, V. amoena, V. angustifolia, V. hirsuta, and V. unijuga, contained no detectable cyanamide (<1 μg g 1 fresh wt), showing that not all Vicia species were able to biosynthesize cyanamide. The same was true for plants of other genera that we tested. Thorough investigation might lead to the identification of other groups in the plant kingdom that biosynthesize cyanamide. We conducted an extensive survey of other higher plants to clarify the distribution of natural cyanamide. The leaves of 452 species, were extracted and analyzed by GCMS. In addition to the six Vicia species tested, we analyzed the cyanamide contents of V. amurensis, V. japonica, and V. pseudo-orobus, and found that these three Vicia species contained no detectable cyanamide (<1 μg g 1 fresh wt). The ability to biosynthesize cyanamide was limited to V. villosa subsp. varia and V. cracca in this genus as far as we have investigated. Although all the other 3
4 species of higher plants tested here also showed no detectable cyanamide, we found a remarkable exception: a leguminous tree, Robinia pseudo-acacia L., containing 46 ± 7 μg g 1 fresh wt of cyanamide in the leaves. The leaves of another Robinia species, R. luxurians, contained no detectable cyanamide. Among the 553 species we have investigated to date, only three species, V. villosa subsp. varia, V. cracca, and R. pseudo-acacia, are able to biosynthesize cyanamide. 3. Conclusions The first natural cyanamide was isolated from V. villosa subsp. varia, a possible allelopathic plant. However, to advocate a significant role of allelopathy in the weed suppression by V. villosa subsp. varia, it is necessary to demonstrate that a sufficient concentration of cyanamide is present in the soil to inhibit the growth of other plants [15]. It is still not known whether cyanamide is emitted into the environment from this plant. Cyanamide is biosynthesized in plants, but the distribution in the plant kingdom is very limited. It cannot be an essential component in the metabolic pathway of plants, because if it were, it would be contained in a variety of plants. According to a phylogenetic classification study on leguminous plants, the genera Vicia and Robinia are categorized in a group together with Lotus, Medicago, and others [16]. This suggests an identical origin of the ability to biosynthesize cyanamide in the evolution process: while the majority of the genera and species in the group may have lost the ability to biosynthesize cyanamide due to loss of a gene(s) or its expression, V. villosa subsp. varia, V. cracca, and R. pseudo-acacia may have continued to biosynthesize cyanamide. Another hypothesis is also possible: a large number of plant species biosynthesize and rapidly metabolize cyanamide, while the three species may have lost ability to metabolize cyanamide. This problem remains to be investigated. Acknowledgments This work was supported in part by a Grant-in-Aid for Young Scientists (B) from The Ministry of Education, Culture, Sports, Science, and Technology ( and ). References [1] Shulman, Y., Nir, G., Fanberstein, L., and Lavee, S The Effect of Cyanamide on the Release from Dormancy of Grapevine Buds. Scientia Horticulturae, 19: [2] Maier-Greiner, U. H., Obermaier-Skrobranek, B. M. M., Estermaier, L. M., Kammerloher, W., Freund, C., Wülfing, C., Burkert, U. I., Matern, D. H., Breuer, M., Eulitz, M., Küfrevioglu, Ö. I., and Hartmann, G. R Isolation and Properties of a Nitrile Hydratase from the Soil Fungus Myrothecium verrucaria That Is Highly Specific for the Fertilizer Cyanamide and Cloning of its Gene. Proceedings of the National Academy of Sciences of the United States of America, 88: [3] Estermaier, L. M., Sieber, A. H., Lottspeich, F. L., Matern, D. H. M., and Hartmann, G. R Biochemical Degradation of Cyanamide and Dicyandiamide. Angewandte Chemie International Edition in English, 31: [4] Hoffman, M. L., Regnier, E. E., and Cardina, J Weed and Corn (Zea mays) Responses to a Hairy Vetch (Vicia villosa) Cover Crop. Weed Technology, 7: [5] Fujii, Y Screening and Future Exploitation of Allelopathic Plants as Alternative Herbicides with Special Reference to Hairy Vetch. Journal of Crop Production, 4: [6] Teasdale, J. R Contribution of Cover Crops to Weed Management in Sustainable Agricultural Systems. Journal of Production Agriculture, 9: [7] White, R. H., Worsham, A. D., and Blum, U Allelopathic Potential of Legume Debris and Aqueous Extracts. Weed Science, 37: [8] Bradow, J. M. and Connick, W. J. Jr Volatile Seed Germination Inhibitors from Plant Residues. Journal of Chemical Ecology, 16: [9] Teasdale, J. R. and Daughtry, C. S. T Weed Suppression by Live and Desiccated Hairy Vetch (Vicia villosa). Weed Science, 41: [10] Kamo, T., Hiradate, S., and Fujii, Y First Isolation of Natural Cyanamide as a Possible Allelochemical from Hairy Vetch Vicia villosa. Journal of Chemical Ecology, 29: [11] Kamo, T., Kato, K., Hiradate, S., Nakajima, E., Fujii, Y., and Hirota, M Evidence of Cyanamide Production in Hairy Vetch Vicia villosa. Natural Product Research, 20: [12] Hiradate, S., Kamo, T., Nakajima, E., Kato, K., and Fujii, Y Direct Quantitative Determination of Cyanamide by Stable Isotope Dilution Gas Chromatography-Mass Spectrometry. Journal of Chromatography A, 1098: [13] Kamo, T., Sato, M., Kato, K., Hiradate, S., Nakajima, E., Fujii, Y., and Hirota, M Quantification of Cyanamide Contents in Herbaceous Plants. Bioscience, Biotechnology, and Biochemistry, 70: [14] Kamo, T., Endo, M., Sato, M., Kasahara, R., Yamaya, H., Hiradate, S., Fujii, Y., Hirai, N., and Hirota, M Limited Distribution of Natural Cyanamide in Higher Plants: Occurrence in Vicia villosa subsp. varia, V. cracca, and Robinia pseudo-acacia. Phytochemistry, 69: [15] Gershenzon, J Plant Defenses: Surface Protectants and Secondary Metabolites, pp , in L. Taiz and E. Zeiger (eds.) Plant Physiology. 2nd Ed. Sinauer Associates, Sunderland, MA. 4
5 [16] Doyle, J. J., Doyle, J. L., Ballenger, J. A., Dickson, E. E., Kajita, T., and Ohashi, H., A Phylogeny of the Chloroplast Gene rbcl in the Leguminosae: Taxonomic Correlations and Insights into the Evolution of Nudulation. American Journal of Botany, 84:
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