Cyanogenesis in the Australian tropical rainforest endemic Brombya platynema (Rutaceae): chemical characterisation and polymorphism

Rebecca E. Miller; Judy Simon; Ian E. Woodrow

doi:10.1071/FP05305

RESEARCH ARTICLE

Previous Next Contents Vol 33(5)

Cyanogenesis in the Australian tropical rainforest endemic Brombya platynema (Rutaceae): chemical characterisation and polymorphism

Rebecca E. Miller ^A ^B , Judy Simon ^A and Ian E. Woodrow ^A

+ Author Affiliations

- Author Affiliations

^A School of Botany, The University of Melbourne, Parkville, Vic. 3010, Australia.

^B Corresponding author. Email: rem@unimelb.edu.au

^C This paper originates from a presentation at ECOFIZZ 2005, North Stradbroke Island, Queensland, Australia, November 2005.

Functional Plant Biology 33(5) 477-486 https://doi.org/10.1071/FP05305
Submitted: 14 December 2005 Accepted: 23 February 2006 Published: 2 May 2006

Abstract

This study examined two aspects of cyanogenesis in Brombya platynema F. Muell. (Rutaceae), a subcanopy tree endemic to tropical rainforest in far north Queensland, Australia. First, cyanogenic glycosides in foliage were fractionated and identified. The rare meta-hydroxylated cyanogenic glycoside, holocalin, was identified as the principal cyanogen, and traces of prunasin and amygdalin were detected. This is the first characterisation of cyanogenic constituents within the genus, and to the authors’ knowledge, only the third within the Rutaceae, and the order Rutales. Second, variation in cyanogenic glycoside content within a population of B. platynema in lowland tropical rainforest was quantified. Both qualitative and quantitative polymorphism for cyanogenesis was identified. Interestingly, ~57% of individuals were considered acyanogenic, with concentrations of cyanogenic glycosides less than 8 μg CN g^–1 DW. Among cyanogenic individuals there was substantial quantitative variation in cyanogenic glycoside concentration, which varied from 10.5 to 1285.9 μg CN g^–1 DW. This high frequency of acyanogenic individuals is contrasted with the apparent absence of the acyanogenesis among populations of other tropical rainforest tree species. In the high herbivory environment of the tropical rainforest, this frequency of acyanogenesis among cyanogenic tropical tree taxa is unique.

Keywords: amygdalin, Australia, β-glucosidase, Brombya platynema, cyanogenesis, cyanogenic glycoside, defence, holocalin, polymorphism, prunasin, Rutaceae, tropical rainforest.

Acknowledgments

We thank Dr Michael Stewart and Prof. Robert Capon, The Institute of Molecular Biosciences, University of Queensland for conducting ¹H NMR analysis. We are grateful to Rigel Jensen for identification of the species in the field, and Alan Curtis, for collecting extra foliage samples for chemical analysis. We also thank Kyatt Dixon and Pascal Stroh for assistance in the field. We also acknowledge the Rainforest Canopy Crane Facility, Cape Tribulation for allowing access to rainforest on the site. We thank Damian Callahan, School of Chemistry, The University of Melbourne, for preliminary LC-ESI / MS analysis of the crude methanol extract. Fieldwork was conducted under Queensland Parks and Wildlife Service Scientific Purposes Permits F1 / 000270 / 99 / SAA and WITK01167103, and was in part supported by an Individual Award from the Queen’s Trust for Young Australians to RE Miller.

References

Adsersen A, Adsersen H, Brimer L (1988) Cyanogenic constituents in plants from the Galapagos Islands. Biochemical Systematics and Ecology 16, 65–77.
| Crossref | GoogleScholarGoogle Scholar |

Aikman K, Bergman D, Ebinger J, Seigler D (1996) Variation of cyanogenesis in some plant species of the Midwestern United States. Biochemical Systematics and Ecology 24, 637–645.
| Crossref | GoogleScholarGoogle Scholar |

Briggs MA (1991) Influence of herbivory and nutrient availability on biomass, reproduction and chemical defences of Lotus corniculatus L. Functional Ecology 5, 780–786.

Briggs MA, Schultz JC (1990) Chemical defense production in Lotus corniculatus L. II. Trade-offs among growth, reproduction and defense. Oecologia 83, 32–37.
| Crossref | GoogleScholarGoogle Scholar |

Brimer L, Cicalini AR, Federici F, Petruccioli M (1995) Beta-glycosidase as a side activity in commercial pectinase preparations of fungal origin. The hydrolysis of cyanogenic glycosides. Italian Journal of Food Sciences 4, 387–394.

Brinker AM, Seigler DS (1989) Methods for the detection and quantitative determination of cyanide in plant materials. Phytochemical Bulletin 21, 24–31.

Brophy JJ, Goldsack RJ, Forster PI (2004) Leaf oils of the genus Brombya (Rutaceae). Journal of Essential Oil Research 16, 402–404.

Buhrmester RA, Ebinger JE, Seigler DS (2000) Sambunigrin and cyanogenic variability in populations of Sambucus canadensis L. (Caprifoliaceae). Biochemical Systematics and Ecology 28, 689–695.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical rainforest. Ecological Monographs 53, 209–233.
| Crossref |

Coley PD , Aide TM (1991) A comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In ‘Plant–animal interactions: evolutionary ecology in tropical and temperate regions’. (Eds PW Price, TM Lewinsohn, GW Fernandes, WW Benson) pp. 25–49. (Wiley and Sons: New York)

Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27, 305–335.
| Crossref | GoogleScholarGoogle Scholar |

Conn EE, Maslin BR, Curry S, Conn ME (1985) Cyanogenesis in Australian species of Acacia. Survey of herbarium specimens and living plants. Western Australian Herbarium Research Notes 10, 1–13.

Cooper-Driver GA, Swain T (1976) Cyanogenic polymorphism in bracken in relation to herbivore predation. Nature 260, 604.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Cooper-Driver GA, Finch S, Swain T (1977) Seasonal variation in secondary plant compounds in relation to the palatability of Pteridium aquilinum. Biochemical Systematics and Ecology 5, 177–183.
| Crossref | GoogleScholarGoogle Scholar |

Cork SJ, Krockenberger AK (1991) Methods and pitfalls of extracting condensed tannins and other phenolics from plants: insights from investigations into Eucalyptus. Journal of Chemical Ecology 17, 123–134.
| Crossref | GoogleScholarGoogle Scholar |

DellaGreca M, Fiorentino A, Monaco P, Previtera L, Simonet AM (2000) Cyanogenic glycosides from Sambucus nigra. Natural Product Letters 14, 175–182.

Dicenta F, Martinez-Gomez P, Grane N, Martin ML, Leon A, Canovas JA, Berenguer V (2002) Relationship between cyanogenic compounds in kernels, leaves, and roots of sweet and bitter kernelled almonds. Journal of Agricultural and Food Chemistry 50, 2149–2152.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ellis WM, Keymer RJ, Jones DA (1977) The defensive function of cyanogenesis in natural populations. Experimentia 33, 309–311.
| Crossref | GoogleScholarGoogle Scholar |

Everist SL (1981) ‘Poisonous plants of Australia.’ (Angus and Robertson: Sydney)

Feeny P (1976) Plant apparency and chemical defense. In ‘Biochemical interaction between plants and insects’. (Eds JW Wallace, RL Mansell) pp. 1–40. (Plenum Press: New York)

Feigl F, Anger V (1966) Replacement of benzidine by copper ethylacetoacetate and tetra base as spot-test reagent for hydrogen cyanide and cyanogen. The Analyst 91, 282–284.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Fikenscher LH, Hegnauer R (1977) Cyanogenese bei den Cormophyten. 12. Mitteilung. Chaptalia nutans, eine stark cyanogene Planze Brasiliens. Planta Medica 31, 266–269.
| PubMed |

Finnemore H, Cooper JM (1936) Cyanogenetic glucosides in Australian plants. Part 4. Zieria laevigata. Journal of the Royal Society of New South Wales 70, 175–182.

Foulds W, Grime JP (1972) The influence of soil moisture on the frequency of cyanogenic plants in populations of Trifolium repens and Lotus corniculatus. Heredity 28, 143–146.

Gibbs RD (1974) ‘Chemotaxonomy of flowering plants.’ (McGill–Queen’s University Press: Montreal)

Gleadow RM, Woodrow IE (2002a) Constraints on effectiveness of cyanogenic glycosides in herbivore defence. Journal of Chemical Ecology 28, 1301–1313.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Gleadow RM, Woodrow IE (2002b) Defense chemistry of cyanogenic Eucalyptus cladocalyx seedlings is affected by water supply. Tree Physiology 22, 939–945.
| PubMed |

Gleadow RM, Foley WJ, Woodrow IE (1998) Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell. Plant, Cell & Environment 21, 12–22.
| Crossref | GoogleScholarGoogle Scholar |

Gleadow RM, Vecchies AC, Woodrow IE (2003) Cyanogenic Eucalyptus nobilis is polymorphic for both prunasin and specific β-glucosidases. Phytochemistry 63, 699–704.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Gmelin R, Schüler M, Bordas E (1973) Holocalin: ein neues cyanogenes glykosid aus Holocalyx balansae. Phytochemistry 12, 457–461.
| Crossref | GoogleScholarGoogle Scholar |

Gomez E, Burgos L, Soriano C, Marin J (1998) Amygdalin content in the seeds of several apricot cultivars. Journal of the Science of Food and Agriculture 77, 184–186.
| Crossref | GoogleScholarGoogle Scholar |

Goodger JQD, Woodrow IE (2002) Cyanogenic polymorphism as an indicator of genetic diversity in the rare species Eucalyptus yarraensis (Myrtaceae). Functional Plant Biology 29, 1445–1452.
| Crossref | GoogleScholarGoogle Scholar |

Goodger JQD, Capon RJ, Woodrow IE (2002) Cyanogenic polymorphism in Eucalyptus polyanthemos Schauer subsp. vestita L. Johnson and K. Hill (Myrtaceae). Biochemical Systematics and Ecology 30, 617–630.
| Crossref | GoogleScholarGoogle Scholar |

Gorz HJ, Gaskins FA, Vögel KP (1986) Inheritance of dhurrin content in mature sorghum leaves. Crop Science 26, 65–67.

Hruska AJ (1988) Cyanogenic glucosides as defense compounds. A review of the evidence. Journal of Chemical Ecology 14, 2213–2217.
| Crossref | GoogleScholarGoogle Scholar |

Hübel W, Nahrstedt A, Fikenscher LH, Hegnauer R (1982) Zierinxyloside, a new cyanogenic glycoside from Xeranthemum cylindraceum. Planta Medica 44, 178–180.

Hughes MA (1991) The cyanogenic polymorphism in Trifolium repens L. (white clover). Heredity 66, 105–115.

Hughes MA , Sharif AL , Alison-Dunn M , Oxtoby E (1988) The molecular biology of cyanogenesis. In ‘Cyanide compounds in biology’. (Eds D Evered, S Harnett) pp. 111–130. (John Wiley & Sons: Chichester)

Hurst E (1942) ‘The poison plants of New South Wales.’ (Poison Plants Committee NSW: Sydney)

Hyland BPM , Whiffin T , Christophel DC , Gray B , Elick RW (2003) Australian rainforest plants: trees, shrubs, vines. [CD-ROM] (CSIRO Publishing: Collingwood)

Janzen DH (1973) Comments on host-specificity of tropical herbivores and its relevance to species richness. In ‘Taxonomy and ecology’. (Ed. VH Heywood) pp. 201–211. (Academic Press: New York)

Jensen SR, Nielsen BJ (1973) Cyanogenic glucosides in Sambucus nigra L. Acta Chemica Scandanavia 27, 2661–2662.

Jones DA (1988) Cyanogenesis in animal–plant interactions. In ‘Cyanide compounds in biology’. (Eds D Evered, S Harnett) pp. 151–165. (John Wiley and Sons: Chichester)

Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. Journal of Agricultural and Food Chemistry 33, 213–217.
| Crossref | GoogleScholarGoogle Scholar |

Kakes P (1989) An analysis of the costs and benefits of the cyanogenic system in Trifolium repens L. Theoretical and Applied Genetics 77, 111–118.
| Crossref | GoogleScholarGoogle Scholar |

Kakes P, Chardonnens AN (2000) Cyanotypic frequencies in adjacent and mixed populations of Trifolium occidentale Coombe and Trifolium repens L. are regulated by different mechanisms. Biochemical Systematics and Ecology 28, 633–649.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Kaplan MAC, Figueiredo MR, Gottlieb OR (1983) Variation in cyanogenesis in plants with season and insect pressure. Biochemical Systematics and Ecology 11, 367–370.
| Crossref | GoogleScholarGoogle Scholar |

Kofod H, Eyjólfsson R (1969) Cyanogenesis in species of the fern genera Cystopteris and Davallia. Phytochemistry 8, 1509–1511.
| Crossref | GoogleScholarGoogle Scholar |

Langenheim JH (1983) The roles of plant secondary chemicals in wet tropical ecosystems. In ‘Physiological ecology of plants of the wet tropics’. (Eds E Medina, HA Mooney, C Vazques-Yanes) pp. 189–208. (The Hague: Boston)

Lechtenberg M , Nahrstedt A (1999) Cyanogenic glycosides. In ‘Naturally occurring glycosides’. (Ed R Ikan) pp. 147–191. (John Wiley & Sons: Chichester)

Levin DA (1976) Alkaloid-bearing plants: an ecogeographic perspective. American Naturalist 110, 261–284.
| Crossref | GoogleScholarGoogle Scholar |

Levin DA, York BM (1978) The toxicity of plant alkaloids: an ecogeographic perspective. Biochemical Systematics and Ecology 6, 61–76.
| Crossref | GoogleScholarGoogle Scholar |

Mabberley DJ (1990) ‘The plant book.’ (Cambridge University Press: Cambridge)

Mali S, Borges RM (2003) Phenolics, fibre, alkaloids, saponins, and cyanogenic glycosides in a seasonal cloud forest in India. Biochemical Systematics and Ecology 31, 1221–1246.
| Crossref | GoogleScholarGoogle Scholar |

Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226, 537–539.

Maslin BR, Dunn JE, Conn EE (1988) Cyanogenesis in Australian species of Acacia. Phytochemistry 27, 421–428.
| Crossref | GoogleScholarGoogle Scholar |

McMahon JM, White WLB, Sayre RT (1995) Cyanogenesis in cassava (Manihot esculenta Crantz). Journal of Experimental Botany 46, 731–741.

Miller RE (2004) Cyanogenesis in Australian tropical rainforests: resource allocation to a nitrogen-based defence. PhD Thesis, The University of Melbourne.

Miller RE, Gleadow RM, Woodrow IE (2004) Cyanogenesis in tropical Prunus turneriana: characterisation, variation and response to low light. Functional Plant Biology 31, 491–503.
| Crossref | GoogleScholarGoogle Scholar |

Miller RE, Jensen R, Woodrow IE (2006a) Frequency of cyanogenesis in tropical rainforests of far north Queensland, Australia. Annals of Botany In press ,
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Miller RE, McConville MJ, Woodrow IE (2006b) Cyanogenic glycosides from the rare Australian endemic rainforest tree Clerodendrum grayi (Lamiaceae). Phytochemistry 67, 43–51.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Møller BL , Seigler DS (1999) Biosynthesis of cyanogenic glycosides, cyanolipids, and related compounds. In ‘Plant amino acids: biochemistry and biotechnology’. pp. 563–609. (Ed. KK Singh). (Marcel Dekker: New York)

Morley BD , Toelken HRE (1983) ‘Flowering plants in Australia.’ (Rigby Publishers: Adelaide)

Nahrstedt A (1976) Prunasin in Holocalyx balansae. Phytochemistry 15, 1983–1984.
| Crossref | GoogleScholarGoogle Scholar |

Nahrstedt A (1981) Isolation and structure elucidation of cyanogenic glycosides. In ‘Cyanide in biology’. (Eds B Vennesland, EE Conn, CJ Knowles, J Westley, F Wissing) pp. 145–181. (Academic Press: London)

Nahrstedt A, Schwind P (1992) Phenylalanine is the biogenetic precursor of meta-hydroxylated zierin, the aromatic cyanogenic glucoside of unripe akenes of Xeranthemum cylindraceum. Phytochemistry 31, 1997–2001.
| Crossref | GoogleScholarGoogle Scholar |

Neilson EH, Goodger JQD, Woodrow IE (2006) Novel aspects of cyanogenesis in Eucalyptus camphora subsp. humeana. Functional Plant Biology 33, 487–496.
| Crossref | GoogleScholarGoogle Scholar |

Noitsakis B, Jacquard P (1992) Competition between cyanogenic and acyanogenic morphs of Trifolium repens. Theoretical and Applied Genetics 83, 443–450.
| Crossref | GoogleScholarGoogle Scholar |

Olafsdottir ES, Andersen JV, Jaroszewski JW (1989) Cyanohydrin glycosides of Passifloraceae. Phytochemistry 28, 127–132.
| Crossref | GoogleScholarGoogle Scholar |

Pederson GA, Fairbrother TE, Greene SL (1996) Cyanogenesis and climatic relationships in US white clover germplasm collection and core subset. Crop Science 36, 427–433.

Price JR (1963) The distribution of alkaloids in the Rutaceae. In ‘Chemical plant taxonomy’. (Ed. T Swain) pp. 429–452. (Academic Press: London)

Rockenbach J, Nahrstedt A (1990) New and known cyanogenic glycosides from the Rubiaceae. Planta Medica 56, 591–592.

Rockenbach J, Nahrstedt A, Wray V (1992) Cyanogenic glycosides from Psydrax and Oxyanthus species. Phytochemistry 31, 567–570.
| Crossref | GoogleScholarGoogle Scholar |

Rosenthaler L (1919) Die Verbreitung der Blausäure im Pflanzenreich. Journal Suisse de Pharmacie 57, 279–346.

Santamour FS (1998) Amygdalin in Prunus leaves. Phytochemistry 47, 1537–1538.
| Crossref | GoogleScholarGoogle Scholar |

Schappert PJ, Shore JS (1995) Cyanogenesis in Turnera ulmifolia L. (Turneraceae). I. Phenotypic distribution and genetic variation for cyanogenesis on Jamaica. Heredity 74, 392–404.

Schappert PJ, Shore JS (2000) Cyanogenesis in Turnera ulmifolia L. (Turneraceae). II. developmental expression, heritability and cost of cyanogenesis. Evolutionary Ecology Research 2, 337–352.

Schwind P, Wray V, Nahrstedt A (1990) Structure elucidation of an acylated cyanogenic triglycoside, and further cyanogenic constituents from Xeranthemum cylindraceum. Phytochemistry 29, 1903–1911.
| Crossref | GoogleScholarGoogle Scholar |

Seigler DS (1991) Cyanide and cyanogenic glycosides. In ‘Herbivores: their interactions with secondary plant metabolites’. (Eds GA Rosenthal, MR Berenbaum) pp. 35–77. (Academic Press: San Diego)

Seigler DS (2003) Phytochemistry of Acacia — sensu lato. Biochemical Systematics and Ecology 31, 845–873.
| Crossref | GoogleScholarGoogle Scholar |

Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16, 144–158.

Spencer KC, Seigler DS (1983) Cyanogenesis of Passiflora edulis. Journal of Agricultural and Food Chemistry 31, 794–796.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Spencer KC, Seigler DS (1985) Cyanogenic glycosides and the systematics of the Flacourtiaceae. Biochemical Systematics and Ecology 13, 421–431.
| Crossref | GoogleScholarGoogle Scholar |

Thomsen K, Brimer L (1997) Cyanogenic constituents in woody plants in natural lowland rain forest in Costa Rica. Biological Journal of the Linnean Society 121, 273–291.

Tracey JC (1982) ‘The vegetation of the humid tropical region of north Queensland.’ (CSIRO)

Urbanska K (1982) Polymorphism of cyanogenesis in Lotus alpinus in Switzerland. I. Small-scale variability in phenotypic frequencies upon acidic silicate and carbonate. Bericht des Geobotanischen Institutes ETH. 49, 35–55.

van Valen F (1978) Contribution to the knowledge of cyanogenesis in angiosperms. 3. Communication. Cyanogenesis in Liliaceae. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen. Series C. 81, 132–140.

Viette M, Tettamanti C, Saucy F (2000) Preference for acyanogenic white clover (Trifolium repens) in the vole Arvicola terrestris. II. Generalization and further investigations. Journal of Chemical Ecology 26, 101–122.
| Crossref | GoogleScholarGoogle Scholar |

Wajant H, Riedel D, Benz S, Mundry K-W (1994) Immunocytological localization of hydroxynitrile lyases from Sorghum bicolor L. and Linum usitatissimum L. Plant Science 103, 145–154.
| Crossref | GoogleScholarGoogle Scholar |

Webb LJ, Tracey JG, Williams WT (1972) Regeneration and pattern in the sub-tropical rainforest. Journal of Ecology 60, 675–695.

Webber BL (2005) Plant–animal interactions and plant defence in the rainforest tree, Ryparosa. PhD Thesis, The University of Melbourne.

Woodrow IE, Slocum DJ, Gleadow RM (2002) Influence of water stress on cyanogenic capacity in Eucalyptus cladocalyx. Functional Plant Biology 29, 103–110.
| Crossref | GoogleScholarGoogle Scholar |