Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The accumulation of terpenoid oils does not incur a growth cost in Eucalyptus polybractea seedlings

Drew J. King A , Roslyn M. Gleadow B and Ian E. Woodrow A C
+ Author Affiliations
- Author Affiliations

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

B Faculty of Science, Monash University, Vic. 3800, Australia.

C Corresponding author. Email: iewood@unimelb.edu.au

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

Functional Plant Biology 33(5) 497-505 https://doi.org/10.1071/FP05304
Submitted: 14 December 2005  Accepted: 14 February 2006   Published: 2 May 2006

Abstract

The deployment of secondary metabolites, such as terpenes, as anti-herbivore defences is thought to be costly for plants in terms of primary metabolism. Moreover, it is assumed that the cost of this deployment is modified by resource availability. In this study we examined the impact of terpenoid oil accumulation on the growth of Eucalyptus polybractea R.T.Baker seedlings from four maternal half-sib families, under conditions of sufficient and limiting nitrogen. The foliar oil concentration measured was extremely variable, varying almost 20-fold to a maximum of 13% (w / DW). Oil concentration was higher in plants grown under high nitrogen than in low-nitrogen plants, and it was positively correlated with foliar nitrogen concentration. Oil concentration was related to maternal concentration, although this relationship was weak because of the variation encountered. The composition of oil, dominated by monoterpenes, was also extremely variable, although this variation could not be adequately explained by either nitrogen availability or the seedling parentage. Importantly, we detected no negative correlations between oil concentration and relative growth rate (RGR), net assimilation rate (NAR), or leaf nitrogen productivity (LNP). Rather, under nitrogen limiting conditions, positive correlations were detected between oil concentration and all three indices. We conclude that oil accumulation is associated with factors that promote growth and if there is a cost to oil deployment, it could not be detected using the experimental design employed here.


References


Barton AFM, Cotterill PP, Brooker MIH (1991) Heritability of cineole yield in Eucalyptus kochii.  Silvae Genetica 40, 37–38. open url image1

Bjorkman C, Larsson S, Gref R (1991) Effects of nitrogen fertilization on pine needle chemistry and sawfly performance. Oecologia 86, 202–209.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brophy JJ , House APN , Boland DJ , Lassak EV (1991) Digests of the essential oils of 111 species from northern and eastern Australia. In ‘Eucalyptus leaf oils, use, chemistry, distillation and marketing’. (Eds DJ Boland, JJ Brophy, APN House) pp. 29–115. (Inkarta Press: Melbourne)

Bryant JP, Chapin FS, Klein DR (1983) Carbon / nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368. open url image1

Burns AE, Gleadow RM, Woodrow IE (2002) Light alters the allocation of nitrogen to cyanogenic glycosides in Eucalyptus cladocalyx.  Oecologia 133, 288–294.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chen Z, Kolb TE, Clancy KM (2002) The role of monoterpenes in resistance of Douglas Fir to western spruce budworm defoliation. Journal of Chemical Ecology 28, 897–920.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chippendale GM (1988) ‘Eucalyptus, Angophora (Myrtaceae).’ (Australian Government Publishing Service: Canberra)

Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defence. Science 230, 895–899. open url image1

Cork SJ, Krockenberger 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.
Crossref |
open url image1

Doran JC (1991) Commercial sources, uses, formation, and biology. In ‘Eucalyptus leaf oils, use, chemistry, distillation and marketing’. (Eds DJ Boland, JJ Brophy, APN House) pp. 11–28. (Inkarta Press: Melbourne)

Doran JC, Matheson AC (1994) Genetic parameters and expected gains from selection for monoterpene yields in Petford Eucalyptus camaldulensis.  New Forests 8, 155–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fahn A (1979) ‘Secretory tissues in plants.’ (Academic Press: New York)

Field C , Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In ‘On the economy of plant form and function’. (Ed. T Givinish) pp. 22–55. (Cambridge University Press: London)

Gershenzon J , Croteau RB (1991) Terpenoids. In ‘Herbivores, their interactions with secondary metabolites. Vol. 1. The chemical participants’. (Eds GA Rosenthal, MR Berenbaum) pp. 165–219. (Academic Press: San Diego)

Gleadow RM, Woodrow IE (2000) Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx.  Tree Physiology 20, 591–598.
PubMed |
open url image1

Gleadow RM, Woodrow IE (2002) Defense chemistry of cyanogenic Eucalyptus cladocalyx seedlings is affected by water supply. Tree Physiology 22, 939–945.
PubMed |
open url image1

Goodger JQD, Ades PK, Woodrow IE (2004) Cyanogenesis in Eucalyptus polyanthemos seedlings: heritability, ontogeny and effect of soil nitrogen. Tree Physiology 24, 681–688.
PubMed |
open url image1

Guenther AB, Monson RK, Fall R (1991) Isoprene and monoterpene emission rate variability: observations with Eucalyptus and emission rate algorithm development. Journal of Geophysical Research 96, 10799–10808. open url image1

Gulmon SL , Mooney HA (1986) Costs of defense and their effects on plant productivity. In ‘On the economy of plant from and function’. (Ed. TA Givinish) pp. 681–698. (Cambridge University Press: Cambridge)

Hanover JW (1966) Genetics of terpenes. I. Gene control of monoterpene levels in Pinus monticola Dougl. Heredity 21, 73–84. open url image1

He C, Murray F, Lyons T (2000) Monoterpene and isoprene emissions from 15 Eucalyptus species in Australia. Atmospheric Environment 34, 645–655.
Crossref | GoogleScholarGoogle Scholar | open url image1

Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283–335.
Crossref | GoogleScholarGoogle Scholar | open url image1

Honkanen T, Haukioja E, Kitunen V (1999) Responses of Pinus sylvestris branches to simulated herbivory are modified by tree sink / source dynamics and by external resources. Functional Ecology 13, 126–140.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kainulainen P, Holopainen J, Palomaki V, Holopainen T (1996) Effects of nitrogen fertilization on secondary chemistry and ectomycorrhizal state of Scots pine seedlings and on growth of grey pine aphid. Journal of Chemical Ecology 22, 617–636.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kimball BA, Turnblom EC, Nolte DL, Griffin DL, Engeman RM (1998) Effects of thinning and nitrogen fertilization on sugars and terpenes in Douglas-fir vascular tissues: Implications for black bear foraging. Forest Science 44, 599–602. open url image1

King DJ, Gleadow RM, Woodrow IE (2004) Terpene deployment in Eucalyptus polybractea; relationships with leaf structure, environmental stresses, and growth. Functional Plant Biology 31, 451–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83, 176–190. open url image1

Koricheva J, Larsson S, Haukioja E, Keinanen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos 83, 212–226. open url image1

Lamontagne M, Bauce E, Margolis HA (2002) Testing the ecophysiological basis for the control of monoterpene concentrations in thinned and unthinned balsam fir stands across different drainage classes. Oecologia 130, 15–24. open url image1

Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. Journal of Chemical Ecology 20, 1223–1280.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lawler IR, Foley WJ, Woodrow IE, Cork SJ (1997) The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109, 59–68.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lerdau M , Gershenzon J (1997) Allocation theory and chemical defense. In ‘Plant resource allocation’. (Eds F Bazzaz, J Grace) pp. 265–277. (Academic Press: San Diego)

Lerdau M, Dilts SB, Westberg H, Lamb BK, Allwine EJ (1994) Monoterpene emission from ponderosa pine. Journal of Geophysical Research 99, 16609–16615.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lerdau M, Matson P, Fall R, Monson R (1995) Ecological controls over monoterpene emissions from Douglas Fir (Pseudotsuga menziezii). Ecology 76, 2640–2647. open url image1

Litvak ME, Constable JVH, Monson RK (2002) Supply and demand processes as controls over needle monoterpene synthesis and concentration in Douglas fir Pseudotsuga menziesii (Mirb.) Franco. Oecologia 132, 382–391.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loreto F, Forster A, Durr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant, Cell & Environment 21, 101–107.
Crossref | GoogleScholarGoogle Scholar | open url image1

McKinnon ML, Quiring DT, Bauce E (1998) Influence of resource availability on growth and foliar chemistry within and among young white spruce trees. Ecoscience 5, 295–305. open url image1

Muzika R-M (1993) Terpenes and phenolics in response to nitrogen fertilization: a test of the carbon / nutrient balance hypothesis. Chemoecology 4, 3–7.
Crossref | GoogleScholarGoogle Scholar | open url image1

Powell JS, Raffa KF (1999) Sources of variation in concentration and composition of foliar monoterpenes in tamarack (Larix laricina) seedlings: roles of nutrient availability, time of season, and plant architecture. Journal of Chemical Ecology 25, 1771–1797.
Crossref | GoogleScholarGoogle Scholar | open url image1

Russell M, Southwell I (2002) Monoterpenoid accumulation in Melaleuca alternifolia seedlings. Phytochemistry 59, 709–716.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Warren CR, Adams MA (2004) What determines rates of photosynthesis per unit nitrogen in Eucalyptus seedlings? Functional Plant Biology 31, 1169–1178.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warren CR, Adams MA (2005) What determines interspecific variation in relative growth rate of Eucalyptus seedlings? Oecologia 144, 373–381.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1