Genetics and Biochemistry of Secondary Metabolites in Plants
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trends in plant science Perspectives maintains the original function and a second Genetics and biochemistry of copy that is not restricted by natural selection. This second copy can then accumulate mutations until, rarely, it has acquired a new secondary metabolites in function and might then become fixed in the population. Domain swapping, with or without prior gene duplications, can also create new, plants: an evolutionary composite genes19. How often do genes for secondary metab- olism arise by gene duplication and diver- perspective gence, and how often do they arise by simple allelic divergence? To resolve this issue, com- Eran Pichersky and David R. Gang parative analyses of orthologous loci from related species that also include the identifi- The evolution of new genes to make novel secondary compounds in plants is an cation of gene function must be carried out – ongoing process and might account for most of the differences in gene function but such data are not yet available. Obviously, among plant genomes. Although there are many substrates and products in if the original gene had an essential function, plant secondary metabolism, there are only a few types of reactions. Repeated as genes of primary metabolism would be evolution is a special form of convergent evolution in which new enzymes with expected to have, gene duplication is a the same function evolve independently in separate plant lineages from a shared necessary prerequisite. However, it is theo- pool of related enzymes with similar but not identical functions. This appears to retically possible, for example, for a new be common in secondary metabolism and might confound the assignment of allele in one of the plant’s genetic loci to be gene function based on sequence information alone. selected for if it encodes the ability to make a new defense compound, whereas the older lants produce an amazing diversity of chemicals produced by plants also seems to be alleles specify the synthesis of another defense low molecular weight compounds. vast, and individual plant lineages synthesize compound that is no longer effective at deter- Although the structures of close to only a small subset of such compounds11. ring the plant’s enemies. Thus, in secondary P 1 50 000 have already been elucidated , there metabolism, there is a potential for new genes are probably hundreds of thousands of such Each species contains only a subset of to evolve without a prior gene duplication compounds. Only a few of these are part of genes for secondary metabolism event. In such cases, orthologous genes in ‘primary’ metabolic pathways (those common Although the pathways that produce most sec- related species might encode proteins with dif- to all organisms). The rest are termed ‘sec- ondary compounds have not yet been eluci- ferent functions. ondary’ metabolites; this term is historical and dated, it is clear that there are possibly was initially associated with inessentiality but, hundreds of thousands of different enzymes Origin of new genes for secondary here, a ‘secondary’ metabolite is defined as a involved in secondary metabolism in plants. metabolism compound whose biosynthesis is restricted to There are many known instances in secondary A gene can be defined as new and distinct selected plant groups. metabolism in which the synthesis of multiple from its ancestral gene when: (1) it encodes an The ability to synthesize secondary products can be catalyzed by a single enzyme, enzyme that catalyzes a chemically similar compounds has been selected throughout the either from different substrates12,13 or, more reaction but on a different substrate than the course of evolution in different plant lineages rarely, even from the same substrate14. enzyme encoded by its progenitor gene; or (2) when such compounds addressed specific However, in most cases that have been investi- the encoded enzyme carries out a different needs (Fig. 1). For example, floral scent gated, the enzymes in plant secondary metab- chemical reaction on the same substrate. A volatiles and pigments have evolved to attract olism are specific for a given substrate and single-step change in both the substrate and insect pollinators and thus enhance fertiliz- produce a single product. the type of reaction is much less likely. How ation rates2,3. The ability to synthesize toxic Plant genomes are variously estimated to often do new genes of secondary metabolism chemicals has evolved to ward off pathogens contain 20 000–60 000 genes, and perhaps arise from other genes of secondary metab- and herbivores (from bacteria and fungi to 15–25% of these genes encode enzymes olism, and how often do they arise from genes insects and mammals) or to suppress the for secondary metabolism15,16. Clearly, the of primary metabolism? growth of neighboring plants4–7. Chemicals genome of a given plant species encodes only The recent advances in whole-genome found in fruits prevent spoilage and act as signals a small fraction of all the enzymes that would sequencing EST databases have provided (in the form of color, aroma and flavor) of be required to synthesize the entire set of important information for this question, but no the presence of potential rewards (sugars, secondary metabolites found throughout the definitive answers. In general, the order of ori- vitamins and amino acids) for animals who eat plant kingdom. This article focuses on the gin of different genes in primary metabolism the fruit and thereby help to disperse the seeds. molecular evolutionary mechanisms that are can be inferred from their level of relatedness Other chemicals serve cellular functions that responsible for generating the great diversity to each other (i.e. their level of sequence iden- are unique to the particular plant in which they of plant secondary metabolites. tity). Current sequencing projects are uncover- occur (e.g. resistance to salt or drought8,9). ing many gene ‘families’ whose existence and The chemical solutions to a common prob- Gene duplication is not the only extent was only suspected before (Table 1). lem are often different in different plant lin- mechanism of evolution of new genes These families are defined by their shared eages. For example, the compounds that make in secondary metabolism ‘motifs’ in the encoded proteins (which up floral scents vary widely from species to It is believed that, at least in primary metab- might constitute the active site and/or bind- species, even when the same class of pollina- olism, new genes almost always arise by gene ing domains of substrates and co-factors). tors (e.g. moths) are attracted to the differing duplication followed by divergence17,18. This However, because the true functions of most bouquets10. The variety of herbivore-deterring leaves the organism with one gene that members of plant gene families are not yet 1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(00)01741-6 October 2000, Vol. 5, No. 10 439 trends in plant science Perspectives possible. For example, some of the acylated anthocyanin derivatives that are synthesized (a) OH by enzymes belonging to the aforementioned acyltransferase family might be synthesized HO O (b) OH by all plants, at least under some specific but presently unknown conditions, but this has O not yet been ascertained. Even if they are not uniformly found in all plants, the ability OH O OH H O O O to make such compounds might be an O ancestral trait that has been lost in various HO O O OH plant lineages; this means that, at one point in time, these compounds were primary OH H O metabolites (produced by all plant groups). HO OH OMe Thus, although comparisons of available OH OMe sequence information indicate that many genes of secondary metabolism have evolved Rutin Rotenone directly from other genes known or presumed to be involved in secondary metabolism, it (c) (d) O is reasonable to assume that, in most cases, OH the ultimate (and sometimes the proximate) N ancestor was a gene involved in primary O metabolism. Indeed, genes of primary metab- OMe olism can serve as a pool from which similar genes of secondary metabolism could evolve OMe over and over again. Linalool Berberine Gain and loss of genes for specific secondary compounds are continuing processes (e)MeO O OH (f) N There are many examples of a specific sec- S ondary compound that is restricted to one N O plant lineage and is not found in related lin- N OH H eages, especially the ancestral one (such an observation should always be considered pro- DIMBOA Brassilexin visional because it is of course possible that other lineages will later be found to make such a compound). This represents prima facie evi- Fig. 1. Examples of plant secondary metabolites and their proposed function in the plant from dence that the ability to synthesize this com- which they were isolated. (a) Rutin, obtained from Forsythia intermedia, thought to act as a visual pound arose within this lineage. pollinator attractant. (b) Rotenone, obtained from Derris elliptica, thought to act as an Molecular evidence for the origin of a insect feeding deterrent. (c) Linalool, obtained from Clarkia breweri, thought to act as an olfactory pollinator attractant. (d) Berberine, obtained from Berberis wilsoniae, thought to act as a new gene encoding the enzyme that catalyzes defense toxin. (e) DIMBOA, obtained from Zea mays, thought to act as a defense toxin. the formation of this compound requires (f) Brassilexin, obtained from Brassica spp., thought to act as an antifungal toxin. analysis of the presence of the gene in this and related plant lineages, as well as a com- parison of its sequence similarity to other related genes. For example, the gene from known, it remains difficult to answer the metabolism glycosyl transferases that also Clarkia breweri (family Onagraceae) that questions posed above completely.