Metal Resistance in Trees: The Role of Mycorrhizae

Abstract

On metal contaminated soils, the colonization and survival of plants is known to occur primarily through the selection of genotypes with heritable resistance traits that occur naturally within some species and populations (Bradshaw and McNeilly 1982, Bradshaw 1984, Baker 1987, Shaw 1990, Ernst et al. 1992). Recent studies have pointed to the additional importance of phenotypic plasticity, itself under normal genetic control, which potentially allows the survival of individual plants in contaminated environments until favourable conditions are encountered either spatially or temporally (Bradshaw 1991, Dickinson et al. 1991); this may involve an alteration of gene expression within an individual plant (Dickinson et al. 1992, Turner and Dickinson 1993a, b). It has also been suggested, however, that the ability to withstand pollution stress may be due to mycorrhizal colonization of roots ameliorating the toxicity of heavy metals (Dickinson et al. 1991, Wilkins 1991). The evolutionary significance of this possibility has not really been considered, but there is considerably more opportunity for genetic change in the shorter lifecycle of a fungus than in even a short-lived higher plant. We argue that elucidation of genetic changes within mycorrhizal communities is crucial to a proper understanding of the survival of long-lived and non-tolerant plants in metal-contaminated soils. Mycorrhizae are found associated with most higher plants and the fossil record suggests that even the earliest land plants were heavily infected (Begon et al. 1990). Perennial species that are normally or occasionally arbuscular mycorrhizal occur in almost twice as many habitat types as those that are infrequently mycorrhizal, which suggests that mycorrhizae increase the niche width of plants (Peat and Fitter 1993). The widespread arbuscular mycorrhizae make up three quarters of the mycorrhizal associations recorded in the British flora; long-lived woody species are almost invariably mycorrhizal. Over 150 taxa of mycorrhizae have been found to be associated with Salix (willows) alone in Britain (Watling 1992). As obligate symbionts, mycorrhizal fungi receive carbon and perhaps other resources from the plant host but it is often difficult to demonstrate that infected plants receive any benefit from the association in the field (Dosskey et al. 1990, Stenstrom and Ek 1990, Colpaert et al. 1992, Colpaert and Van Assche 1993). However, benefits that have been identified include improved uptake of less mobile nutrients such as phosphate, improved water relations, protection from fungal pathogens and protection from soil toxins (Harley and Smith 1983, Fitter 1991, Abbott et al. 1992, Fitter and Merryweather 1992, Gadd 1993). It is thought that the detrimental effect of air pollution on mycorrhizae is a likely causal factor of forest decline in Europe and North America (Jakucs 1988, Fellner 1989), further indicating the likely importance of the symbiotic association. Communities of mycorrhizal fungi change with time after planting trees (Last et al. 1992), and the absence of sheathing (ecto-)mycorrhizae may account for poor establishment of planted trees on some soils, including metal-contaminated soils (Burton and Morgan 1984, Ernst et al. 1990, Kahle 1993). Other studies have shown that, despite an apparent protective role of mycorrhizae, tree roots in mineralized forest soils naturally enriched with metals have a reduced active mycorrhizal root tip count (Bell et al. 1988). Metal-tolerant fungi may be more abundant in soils with extremely high concentrations of metals, but metal-tolerant fungi can also be isolated from clean soil, which suggests that wide genetic variation for metal tolerance may exist in many normal mycorrhizal populations. Mycorrhizal isolates from nickel-, copperand zinc-contaminated soils that have been grown on axenic media containing elevated metals have been found not to grow any better than the same species isolated from clean soils; it appears to be the behaviour of the fungus in the presence of roots that is particularly critical (Brown and Wilkins 1985a,b, Jones and Hutchinson 1986a, b). Seedlings of birch, pine and spruce are less susceptible to toxic concentrations of zinc, copper, nickel and aluminium in the growth medium in the presence of sheath-