Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Novel aspects of cyanogenesis in Eucalyptus camphora subsp. humeana

Elizabeth H. Neilson A , Jason Q. D. Goodger A B and Ian E. Woodrow A

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

B Corresponding author. Email: jgoodger@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) 487-496 http://dx.doi.org/10.1071/FP05293
Submitted: 13 December 2005  Accepted: 10 February 2006   Published: 2 May 2006

Abstract

Cyanogenesis is the release of cyanide from certain organisms upon tissue disruption. Tissue disruption, such as that caused by folivory, brings cyanogenic glycosides into contact with catabolic enzymes and toxic HCN is subsequently released. The process provides a measure of defence against generalist herbivores. Within the genus Eucalyptus, several species have been identified as cyanogenic and all of these store cyanide exclusively in the form of the cyanogenic glycoside prunasin. Here we report for the first time cyanogenesis in Eucalyptus camphora subsp. humeana L.A.S. Johnson & K.D. Hill. We found that foliage contains at least five different cyanogenic glycosides, three of which were purified and identified (prunasin, sambunigrin and amygdalin). Two natural populations of E. camphora trees were screened for cyanogenesis, and quantitative polymorphism was measured at both sites. Trees varied in their capacity for cyanogenesis from 0.014 to 0.543 mg CN g–1 DW in one population and from 0.011 to 0.371 mg CN g–1 DW in the other. A progeny trial, testing both cyanogenesis and carbon-based defence (namely total phenolics and condensed tannins), was performed with seed sourced from two cyanogenic, open-pollinated maternal trees. Interestingly, the seedlings exhibited markedly lower levels of cyanogenesis and condensed tannins than the adult population, with some individuals completely lacking one or both of the chemical defences. Total phenolic concentrations, however, were significantly higher in the seedlings than in the parental population from which the seed was sourced. Eucalyptus camphora is relatively unique among cyanogenic trees having multiple foliar cyanogenic glycosides and an apparently marked ontogenetic regulation of cyanogenic capacity.

Keywords: cyanogenesis, cyanogenic glycoside, defence, eucalypt, phenolics, prunasin.


References

Basey MB Jenkins SH Busher PE 1988 Optimal central-place foraging by beavers: tree-size selection in relation to defensive chemicals of quaking aspen. Oecologia 76 278 282 doi:10.1007/BF00379963

Boege K Marquis RJ 2005 Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution 20 441 448 doi:10.1016/j.tree.2005.05.001

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

Burns A Gleadow RM Woodrow IE 2002 Light alters the allocation of nitrogen to cyanogenic glycosides in Eucalyptus cladocalyx. Oecologia 133 288 294
doi:10.1007/s00442-002-1055-9

Busk PK Møller BG 2002 Dhurrin synthesis in Sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiology 129 1222 1231 doi:10.1104/pp.000687

Chappill JA Ladiges PY 1996 Phylogenetic analysis of Eucalyptus informal subgenus Symphyomyrtus section Maidenaria. Australian Systematic Botany 9 71 93 doi:10.1071/SB9960071

Conn EE (1980) Cyanogenic glycosides. In ‘Encyclopedia of plant physiology. New Series’. (Eds EA Bell, BV Charlwood) pp. 461–492. (Springer: Berlin)

Conn EE (1981) Cyanogenic glycosides. In ‘The biochemistry of plants’. (Eds PK Stumpf, EE Conn) pp. 479–500. (Academic Press: New York)

Conn EE 1991 The metabolism of a natural product: lessons learned from cyanogenic glycosides. Planta Medica 57 1 9

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 60


Conn EE Seigler DS Maslin BR Dunn J 1989 Cyanogenesis in Acacia subgenus Aculeiferum. Phytochemistry 28 817 820
doi:10.1016/0031-9422(89)80121-9

Cork SJ Krokenburger AK 1991 Methods and pitfalls of extracting condensed tannins and other phenolics from plants: insights from investigations on Eucalyptus leaves. Journal of Chemical Ecology 17 123 134 doi:10.1007/BF00994426

Dahler JM McConchie CA Turnbull CGN 1995 Quantification of cyanogenic glycosides in seedlings of three Macadamia (Proteaceae) species. Australian Journal of Botany 43 619 628 doi:10.1071/BT9950619

Dominy NJ Lucas PW Wright SJ 2003 Mechanics and chemistry of rainforest leaves: canopy and understorey compared. Journal of Experimental Botany 54 2007 2014 doi:10.1093/jxb/erg224

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

Finnemore H Reichard SK Large DK 1935 Cyanogenetic glucosides in Australian plants. Part 3. Eucalyptus cladocalyx. Journal of the Proceedings of the Royal Society of NSW 69 209 214

Fritz RS Hochwender CG Lewkiewicz DA Bothwell S Orians CM 2001 Seedling herbivory by slugs in a willow hybrid system: developmental changes in damage, chemical defense, and plant performance. Oecologia 129 87 97
doi:10.1007/s004420100703

Gardner CA , Bennetts HW (1956) ‘The toxic plants of Western Australia.’ (West Australian Newspapers Ltd.: Perth)

Gleadow RM (1999) Resource allocation in cyanogenic Eucalyptus cladocalyx. PhD Thesis, University of Melbourne.

Gleadow RM Woodrow IE 2000 a Polymorphism in cyanogenic glycoside content and cyanogenic β-glucosidase activity in natural populations of Eucalyptus cladocalyx. Australian Journal of Plant Physiology 27 693 699

Gleadow RM Woodrow IE 2000 b Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx. Tree Physiology 20 591 598


Gleadow RM Woodrow IE 2002 a Defense chemistry of cyanogenic Eucalyptus cladocalyx seedlings is affected by water supply. Tree Physiology 22 939 945


Gleadow RM Woodrow IE 2002 b Mini-review: constraints on effectiveness of cyanogenic glycosides in herbivore defense. Journal of Chemical Ecology 28 1301 1313
doi:10.1023/A:1016298100201

Gleadow RM Foley W Woodrow IE 1998 Enhanced CO2 alters the relationship between photosynthesis and defence in Eucalyptus cladocalyx F. Muell. Plant, Cell & Environment 27 693 699

Gleadow RM Vecchies AC Woodrow IE 2003 Cyanogenic Eucalyptus nobilis is polymorphic for both prunasin and specific β-glucosidases. Phytochemistry 63 699 704
doi:10.1016/S0031-9422(03)00245-0

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 doi:10.1071/FP02027

Goodger JQD Ades PK Woodrow IE 2004 Cyanogenesis in Eucalyptus polyanthemos seedlings: heritability, ontogeny and effect of soil nitrogen. Tree Physiology 24 681 688

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
doi:10.1016/S0305-1978(01)00141-7

Hickel A Hasslacher M Griengl H 1996 Hydroxynitrile lyases: functions and properties. Physiologia Plantarum 98 891 898 doi:10.1034/j.1399-3054.1996.980430.x

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

Johnson LAS Hill KD 1990 New taxa and combinations in Eucalyptus and Angophora (Myrtaceae). Telopea 4 37 108

Jones DA 1998 Why are so many food plants cyanogenic? Phytochemistry 47 155 162
doi:10.1016/S0031-9422(97)00425-1

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

Laitinen M Julkunen-Tiitto R Tahvanainen J Heinonen J Rousi M 2005 Variation in birch (Betula pendula) shoot secondary chemistry due to genotype, environment, and ontogeny. Journal of Chemical Ecology 31 697 717
doi:10.1007/s10886-005-3539-7

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

Loyd RC Gray E 1970 Amount and distribution of hydrocyanic acid potential during the life cycle of plants of three sorghum cultivars. Agronomy Journal 45 159 162

Maslin BR Dunn JE Conn EE 1988 Cyanogenesis in Australian species of Acacia. Phytochemistry 27 421 428
doi:10.1016/0031-9422(88)83112-1

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 doi:10.1071/FP03218

Miller RE McConville MJ Woodrow IE 2006 a Cyanogenic glycosides from the rare Australian endemic rainforest tree Clerodendrum grayi (Lamiaceae). Phytochemistry 67 43 51 doi:10.1016/j.phytochem.2005.09.038

Miller RE Simon J Woodrow IE 2006 b Cyanogenesis in the Australian tropical rainforest endemic Brombya platynema (Rutaceae): chemical characterisation and polymorphism. Functional Plant Biology 33 477 486 doi:10.1071/FP05305

Møller BL , Seigler DS (1999) ‘Plant amino acids: biochemistry and biotechnology.’ (Marcel Dekker: New York)

Nahrstedt A 1985 Cyanogenic compounds as protecting agents for organisms. Plant Systematics and Evolution 150 35 47 doi:10.1007/BF00985566

Okolie PN Obasi BN 1993 Diurnal variation of cyanogenic glucosides, thiocyanate and rhodanese in cassava. Phytochemistry 33 775 778 doi:10.1016/0031-9422(93)85273-T

Poulton JE (1983) Cyanogenic compounds in plants and their toxic effects. In ‘The handbook of natural toxins’. (Eds RF Keeler and WT Tu) pp. 117–157. (Dekker: New York)

Poulton JE 1990 Cyanogenesis in plants. Plant Physiology 94 401 405

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


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

Simmons D Brown G 1986 The distribution of some Eucalyptus species (the swamp gums) in the Yarra Valley, Victoria. Victorian Naturalist 103 19 25


Tahvanainen J Helle E Julkunen-Tiitto R Lavola A 1985 Phenolic compounds of willow bark as deterrents against feeding by mountain hare. Oecologia 65 319 323
doi:10.1007/BF00378905

Webb LJ (1949) An Australian phytochemical survey. I. Alkaloids and cyanogenetic compounds in Queensland plants. Bulletin 214, CSIRO, Melbourne.

Wheeler JL Mulcahy C Walcott JJ Rapp GG 1990 Factors affecting the hydrogen cyanide potential of forage sorghum. Australian Journal of Agricultural Research 41 1093 1100 doi:10.1071/AR9901093

Woodrow IE Slocum D Gleadow RM 2002 Influence of water stress on cyanogenic capacity in Eucalyptus cladocalyx. Functional Plant Biology 29 103 110 doi:10.1071/PP01116

Zagrobelny M Bak S Rasmussen AV Jørgensen B Naumann CM Møller BL 2004 Cyanogenic glucosides and plant–insect interactions. Phytochemistry 65 293 306 doi:10.1016/j.phytochem.2003.10.016



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