The role of secondary compounds in plants

The first secondary compounds to be characterised were those accumulating in relatively high concentration and this led to the view that they were probably 'excretory products' or 'end products of metabolism'. They were thus described by Czapek in the second edition of his 1921 textbook Plant Biochemistry and this view persisted into the 1970s. An alternative to the 'waste product' hypothesis was that the synthesis of secondary metabolites provides a way of 'using up' primary metabolites to keep open primary production lines which might be shut down altogether when external conditions were unfavourable for growth or development. It was proposed that the nature of the secondary metabolite was unimportant, which explained their conspicuous and unexplained structural variation (Swain, 1974).

Neither of these hypotheses was adequate to explain the findings of metabolic tracer studies from the 1960s onward that biosynthetic pathways leading to the elaboration of secondary products are complex and that both their synthesis and degradation are under strict regulatory control (Luckner, 1980, 1990). As pointed out by Swain (1974), if the role of secondary products were merely to detoxify excess primary metabolites or keep the wheels of primary energy production ticking over there would be no need to synthesise more than one or two types of product from any given primary precursor, which would involve as few enzyme-catalysed reactions as possible. It was also shown that secondary compounds are turned over, sometimes quite rapidly, to produce primary metabolites and that they are also found in many different types of actively dividing tissue. This suggested that they are not linked to the utilisation of primary substances or to the resting stages of cell division.

Despite the dominance of the waste product hypothesis in the earlier years of the century, both Czapek and Pfeffer had suggested that secondary compounds might serve an ecological role. In 1959 Fraenkel drew attention to the possible link between the diversity and distribution of secondary compounds and the specificity of the interaction between insects and their host plants. Ehrlich and Raven (1964), examining the close structural and chemical links evident in the relation between insects and plants, proposed the term 'coevolution', suggesting reciprocal genetic changes maintaining a close relation between insects and host plants as both evolved. By the 1970s there was overwhelming evidence that many secondary compounds can and do serve as attractants, poisons and repellents of other organisms. (Swain, 1974; McKey, 1979; Rhoades, 1979; Bell, 1980a; Harborne, 1988). The heterogeneity of plant secondary compounds, far from being fortuitous, was seen as a measure of the diversity of strategies which have evolved to allow different organisms to adapt to, and co-exist in, a particular ecological niche. Adaptation is assumed to be the consequence of the selection of the expression of new genetic traits which have been brought about by evolutionary change over long periods of time within a group of organisms. Genetic mutations leading to changes in primary metabolism are likely to be lethal. In contrast, those leading to changes in secondary metabolism could be expected to provide a range of viable organisms with differing secondary chemistry enabling them to adapt to differing ecological niches. This might explain the enormous variety of secondary metabolites - over 20000 have been isolated from higher plants alone (Waterman, 1992).

Most early experiments designed to show that plant chemicals could exert effects on other organisms were carried out with isolated, purified compounds. They also revealed that many predators of plants containing toxic chemicals have evolved mechanisms to avoid their detrimental effects (the 'coevolution' of Ehrlich and Raven). Recently, attempts have been made to understand better the ecological effects of the total mixture of chemicals present in plants, the composition of which is known to change seasonally and diurnally, and sometimes to vary intraspecifically. Such changes may have functional significance. For example, Harborne (1990) points out that where a species is polymorphic for a particular defensive compound, that is, individual plants contain different amounts, then those individuals containing little or none of the deterrent compound would be attacked preferentially. Individuals containing higher levels would be avoided. By this means the defensive compound could confer protection on the group without being itself totally toxic or deterrent to the predator, and adaptation to it would be slower than if it were present at a uniform level in all members of the group.

Many current assumptions about the role of secondary compounds as defensive agents have been questioned by Jones and Firn (1991) who suggest that the relation between the specific chemical composition of a plant and its overall level of defence may actually be weak. They consider that well-defended plants might be expected to have a moderate diversity of secondary compounds with high biological activity whereas in practice it is found that most plants have a wide array of compounds, most of which have no demonstrable biological activity, and of the few that do it is rare to find 100% inhibition or deterrence of putative target organisms. According to the traditional view of survival of the fittest, plants accumulating compounds with no biological activity would incur costs without benefits in the short term and would be expected to lose out in the struggle for survival. Those plants however, producing a few active compounds would be well protected in the short term but would be less well fitted to respond to consumer adaptation or to new colonists in the long term.

Jones and Firn believe that many plant compounds may not serve any specific defensive role other than their contribution to the diversity necessary to increase the possibility of having a few defensive compounds available at any one time. In other words, mechanisms have evolved to ensure the generation and retention of biological diversity above all, and that a particular compound, or the class to which it belongs, may not have evolved as a result of selection by a particular organism. Those metabolic traits which confer diversity may have been selected very early in evolution, probably before the emergence of terrestrial plants, because microorganisms and algae show similar traits. The natural screening process of diversification and elimination may then have proceeded in a manner which was largely independent of specific biotic interactions, provided that there was always selection for well-defended plants. The pressures for selection against these biochemical pathways may have been minimal in comparison with selection for other survival and adaptive mechanisms. Random genetic drift may have ensured their survival and modification in the absence of any specific selection pressure.

It is worth noting here that Swain (1974) referred to reports that putatively advanced species of families and genera of plants have less DNA than more primitive members, and that this might indicate a trading of a loss of future evolutionary potential for short-term success. A corollary of this is that major evolutionary changes may arise from apparently primitive members of a group which had retained the option of greater flexibility of response to changing conditions, and that the loss of primitive members might therefore herald the end of the taxon. Bennett (1987) concludes, however, that more work needs to be done to understand the ecological significance of varying DNA amounts.

The development of all theories as to the origin and role of secondary compounds is hampered by a lack of knowledge of the cost-benefit relation of the accumulation of a particular spectrum of secondary compounds, or of a complete understanding of their biological activity. Herms and Mattson (1992) have extensively reviewed the literature on costs and benefits of plant defences and integrated the various evolutionary models into a 'growth-differentiation balance' framework to form an integrated system of those explaining and predicting patterns of plant defence and competitive interactions. The authors point out that plants have a dilemma: they must grow fast enough to compete, yet maintain the defences necessary to survive in the presence of pathogens and herbivores. Secondary compounds can divert resources from growth, hence the delicate cost-benefit balance. A full analysis of the trade-off between growth and secondary metabolism has yet to be established for any species.

Nevertheless, several strategies can be discerned whereby plants reduce the metabolic cost of a range of secondary compounds that they produce (Jones and Firn, 1991). These include the use of branched pathways permitting a wide range of compounds to be made through just a few biosynthetic routes, combining pathways, and also regulating pathways in such a way that only trace amounts of compounds need normally be produced, but facilitating the increased production when needed, for example when the plant is under attack (Tallamy and Raupp, 1991).

Jones and Firn (1991) also suggest that enzymes used in secondary metabolism may possess low substrate specificity and be able to utilise a range of substrates avoiding the need to always provide specific pathways for the generation of specific compounds. Costs might also be limited by producing very potent compounds in small quantities, increasing potency through synergistic interactions, restricting the production of defensive compounds to vulnerable parts of the plant, using them for other purposes, for example for attraction of pollinators, structural support, temporary nutrient storage, phytohormone regulation, drought resistance, protection from ultraviolet light, protection of roots from acidic and reducing environments, facilitation of nutrient uptake and mediation of relations with nitrogen-fixing bacteria and by recycling them into primary metabolism after their defensive role has past (Harborne, 1990; Herms and Mattson, 1992).

Swain (1974) contrasted the intricacies of secondary metabolism of plants as an aid to survival with the intricacies of behavioural patterns in mammals which serve a similar purpose: 'animals act, plants produce'.

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