CASE STUDY 13.1  CO2, cyanide and plant defence

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Roslyn Gleadow and Ian Woodrow

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Figure 1 A healthy stand of Eucalyptus cladocalyx (sugar gums) near Ouyen (north-western Victoria). Sugar gums are indigenous to South Australia but they have been planted widely throughout the world. They are common on farms in western Victoria because this area was settled by farmers from South Australia who brought the seed with them. The tree was popular because it coppices easily, forming long straight branches that could be used for fence posts, but stock avoid eating the young shoots.

(Photograph courtesy P.E. Kriedemann)

Young tips of eucalypts are particularly attractive to mammalian herbivores such as koalas as well as to insects because they are higher in protein and nitrogen but lower in fibre (softer) than old leaves. Such herbivory impacts on plants because these shoots are future sources of photoassimilate. Lost foliage needs to be replaced, consuming valuable energy and nutrient stores. Vascular plants have evolved with a range of physical and chemical mechanisms that increase their resistance to herbivores and minimise such losses.

Nevertheless, these mechanisms are ‘expensive’ in terms of energy and of resources that could otherwise be used for photosynthesis. Cyanogenic glycosides are one such group of chemical defence compounds that are both nitrogen rich and take much energy to synthesise.

Cyanogenic glycosides consist of a cyanide group (NC-) bound to a sugar. When the sugar is cleaved by a ß-glycosidase enzyme, free hydrocyanic acid (HCN) is released. HCN interferes with cytochrome oxidase (Section 2.4) and is extremely toxic to herbivores. Such plants are termed cyanogenic. They avoid poisoning themselves by storing cyanogenic glycosides and the β-glucosidase in separate places: glycoside in vacuoles and enzyme in apoplasm. Enzyme and substrate are brought together when a leaf is crushed, as in chewing. About 4% of all plants are cyanogenic, including a number of species of Eucalyptus. Cyanogenesis discourages grazing by both mammalian and invertebrate herbivores.

Cyanide production represents a resource cost to a plant in terms of nitrogen. Given that nitrogen is in limited supply in most ecosystems, any diversion of nitrogen away from primary metabolism is likely to have a negative impact on plant growth. Any benefit takes the form of reduced herbivory. There is thus a trade-off between the benefit of reduced herbivory and the cost in terms of lower growth rates. Will this balance change in a high-CO2 world?

Plants at elevated CO2 grow faster and more efficiently (using less water and fewer nutrients per unit CO2 fixed) than those at ambient levels. If atmospheric concentration of CO2 is doubled from 350 to around 750 µmol mol–1, biomass and photosynthetic rates increase. Leaves from plants grown at elevated CO2 also contain lower concentrations of nitrogen and protein. Since most of a plant’s nitrogen is invested in photosynthetic enzymes, nitrogen use efficiency increases under elevated CO2 (Table 6.7).

If plants grown at elevated CO2 are able to achieve higher rates of photosynthesis with less nitrogen, then nitrogen in excess of those requirements could be used for other purposes such as the synthesis of herbivore defence compounds.

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Figure 2 This tone-coded diagram of a typical branch of a 6-month-old Eucalyptus cladocalyx seedling shows a gradient in concentration of cyanogenic glycosides (measured as cyanide) from younger to older parts. Tips are softer and are highly sought after by herbivores, but higher levels of cyanogenic glycosides may offer protection (Original diagram courtesy R.M. Gleadow)

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Figure 3   Leaf nitrogen invested in cyanogenic glycosides as a proportion of total leaf nitrogen was significantly greater in leaves of Eucalyptus cladocalyx seedlings grown at elevated CO2 concentration (about 350 µmol mol-1). As a result, leaves from plants grown at elevated CO2 are both less nutritious and more toxic to herivores. (Based on Gleadow et al. 1998)

Accordingly the hypothesis that increased efficiency of nitrogen use under elevated CO2 would lead to an increase in nitrogen allocation to cyanogenic glycosides was tested. Seedlings of Eucalyptus cladocalyx (sugar gum) were chosen for the study (Gleadow et al. 1998) because they invest up to 20% of leaf nitrogen in cyanogenic glycosides (Figure 2), and consequently any changes would be readily detected.

Seedlings of E. cladocalyx were grown in a pair of glasshouses that differed only in the amount of CO2 in the atmosphere — extra CO2 was added to one chamber to raise the atmos-pheric concentration of CO2 from 350 to 750 µmol mol–1.

The growth response of seedlings was typical of woody plants grown at elevated CO2 — biomass increased, leaves were thicker and the leaf area ratio (LAR, Section 6.1) was reduced. In addition, the concentration of nitrogen and protein in leaves decreased, implying gains in the efficiency of nitrogen use. More importantly, allocation of nitrogen to cyanogenic glycosides increased significantly in plants grown at elevated CO2 (Figure 3). As a result, plant protein content decreased and the amount of protein relative to the amount of cyanogenic glycosides decreased even more. Plants would not only be less nutritious to herbivores, but also more toxic.

If these controlled-environment experiments are good predictors of what will happen in more complex, natural ecosystems then the balance between plants and herbivores in the next century could be different. While this is good news for plants, it is bad news for herbivores. In a future high-CO2 world plants are likely to be less nutritious and also contain increased concentrations of toxins and defence compounds. Plants will be able to grow faster and be more resistant to herbivores. That outcome will have serious implications for herbivores such as leaf-eating mammals, who are already under threat from habitat destruction.

References

Gleadow, R.M., Foley, W.J. and Woodrow I.E. (1998). ‘Enhanced CO2 alters the photosynthesis–defence relationship in cyanogenic Eucalyptus cladocalyx F. Muell.’, Plant, Cell and Environment, 21, 12–22.

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