Seed plants and general trends in secondary metabolite occurrence and evolution

2.3.7 Seed plants and general trends in secondary metabolite occurrence and evolution

Some, but by no means all, secondary metabolites appear to have become increasingly sophisticated throughout evolutionary time, and may be particularly advanced and variable among the seed plants. However, our knowledge is so incomplete that it is dubious whether or not tracing the evolution of certain classes of secondary metabolite provides an accurate picture. For instance, alkaloids are traditionally seen as advanced secondary metabolites produced by flowering plants (Harborne, 1993), but we have already seen that green algae, hornworts, and clubmosses may produce alkaloids (Trennhäuser, 1992; Trennhäuser et al., 1994; Liu et al., 2004; Leflaive and TenHage, 2007). Similarly, the fact that rosmarinic acid is produced by a number of hornworts and ferns (Häusler et al., 1992; Vogelsang et al., 2006) is at odds with the traditional view that this compound is exclusive to flowering plants of the families Lamiaceae and Boraginaceae. Our view of the distribution of secondary metabolites among the plant kingdom may be heavily skewed in favor of the relatively widespread flowering plants that have been more commonly studied.

Even within the flowering plants, it is currently extremely difficult to comment on the trends in the evolution of specific secondary metabolites within or between families. For example, cucurbitacins are a group of active compounds that are usually isolated from species of one particular family, in this case the Cucurbitaceae (cucumbers, melons, squashes, etc.). This has erroneously given the impression that cucur- bitacins are unique to this family. There is a growing recent literature centered around the description of new cucurbitacins from novel source species and the fact that these compounds may have antibacterial and anticancer activities (e.g., Sun et al., 2010). Most of these new sources are indeed Cucurbitaceae, but a wider search is now revealing that cucurbitacins also occur in members of the Scrophulariaceae (e.g., Smit et al., 2000; Wang et al., 2004; Zou et al., 2004; Allen et al., 2006; Kim et al., 2006; Bhandari et al., 2007; Kaya and Melzig, 2008), Rosaceae (Sarker et al., 1999; Munoz et al., 2000, 2002; Maloney et al., 2008), Sterculiaceae (Chen et al., 2006), Rubiaceae (Litaudon et al., 2003) and Elaeocarpaceae (Ito et al., 2002; Rodriguez et al., 2003), and thus appear to have evolved either a number of times in different groups or once in a common ancestor without being expressed in many species.

These studies have one thing in common: they have been conducted recently in (mainly) tropical floras for which the occurrence of secondary metabolites is little known, and where research into secondary metabolites and medicinal plants is a growing field for local science. In other words, attempts to describe the general occurrence of particular secondary metabolites among the plant kingdom may be premature because studies have historically been biased toward temperate, particularly European, flowering plants.

We do have a clear view of the evolution and occurrence of certain secondary metabolites. Mustard oils, for instance, are known to be restricted to 14 families that are closely allied to Brassicaceae (together these families form the order Capparales), based on molecular and morphological data (Rodman et al., 1996). As far as is known, only once has convergent evolution resulted in the appearance of mustard oils in a family not closely related to the Capparales—in the tree species Drypetes natalensis (Putranjivaceae; Johnson et al., 2009). Jensen et al. (2007) also advocate an approach similar to that of Rodman et al. (1996): that is, that combined use of DNA sequence data, plant morphology, and secondary metabolites can form a pow- erful tool for precisely discerning the relationships between closely related taxa. However, while these techniques allow investigation of the fine details of secondary metabolite evolution in particular cases, it is the broader view that we currently lack.

Comprehensive investigations of an entire class of secondary metabolites, such as that of Rodman et al. (1996), are rare. Even within the most common flowering plant families, our ignorance of plant secondary metabolites is profound. Only 0.5% (136 out of ~25,000 species) of one of the largest families, the Asteraceae, are included in the most recent edition of the authoritative Codex Vegetabilis (Proserpio, 1997; originally published as Steinmetz 1947). Within this subgroup, a range of compounds is evident: 67 species are valued as a source of essential oils, 9 species produce alkaloids, 8 glucosides, 28 tannins, 15 terpenes, 29 flavonoids, and a small number of species contain combinations of these compounds. Proserpio (1997) includes 109 Fabaceae (legumes), 19 of which contain alkaloids, 32 tannins, 27 essential oils, and a smaller number contain flavones, resins, or glucosides. In contrast, of the 73 species of Lamiaceae recorded as medicinal species, most (84%) are employed for their essential oils. Thus, different families tend to contain different numbers of species valued for particular classes of compound, but nonetheless a great range of com- pounds is present within each family. Furthermore, the above examples are based on extremely small sample sizes, insufficient to provide a comprehensive overview of the trends in the evolution of secondary metabolites within these families, and yet they are among the largest and, for medicinal plants, most widely utilized of flowering plant families.

In conclusion, these examples illustrate that while we may be able to discern the details of secondary metabolite evolution between particular taxa, attempts to broadly trace the evolution of active compounds are, in our opinion, currently inadequate. Ongoing investigation, particularly of ancient plant lineages and tropical floras, is revealing that supposedly advanced secondary metabolites, or metabolites that were once thought to be highly restricted to particular flowering plant lineages, may actually be found in a much greater range of taxa. For example, “the Anthocerotae [hornworts], like the large group of the Musci (mosses) . . . are considered to be poor in terpenoid metabolites. However, after the presence of many terpenoid compounds was reported in Musci, it appeared worthwhile to have a closer look at the volatile constituents of the Anthocerotae as well” (Mekem Sonwa and König, 2003), which, indeed, they went on to find. We suspect that there are many such instances in which an apparent lack of particular secondary metabolites in certain plant groups is simply an artifact of our lack of enquiry, rather than any deficiency on the part of the plant. This provides a message of hope for those wishing to exploit plant secondary metabolites for therapeutic purposes: the implication is that medicinal botany currently relies on a minuscule proportion of the biologically active compounds that exist in nature.

Soure: Giacinto Bagetta, Marco Cosentino, Marie Tiziana Corasaniti, Shinobu Sakurada (2012); Herbal Medicines: Development and Validation of Plant-derived Medicines for Human Health; CRC Press