The function of secondary metabolites in plant carnivory

Abstract

Background: Carnivorous plants are an ideal model system for evaluating the role of secondary metabolites in plant ecology and evolution. Carnivory is a striking example of convergent evolution to attract, capture and digest prey for nutrients to enhance growth and reproduction and has evolved independently at least ten times. Though the roles of many traits in plant carnivory have been well studied, the role of secondary metabolites in the carnivorous habit is considerably less understood.

Scope: This review provides the first synthesis of research in which secondary plant metabolites have been demonstrated to have a functional role in plant carnivory. From these studies we identify key metabolites for plant carnivory and their functional role, and highlight biochemical similarities across taxa. From this synthesis we provide new research directions for integrating secondary metabolites into understanding of the ecology and evolution of plant carnivory.

Conclusions: Carnivorous plants use secondary metabolites to facilitate prey attraction, capture, digestion and assimilation. We found ~170 metabolites for which a functional role in carnivory has been demonstrated. Of these, 26 compounds are present across genera that independently evolved a carnivorous habit, suggesting convergent evolution. Some secondary metabolites have been co-opted from other processes, such as defence or pollinator attraction. Secondary metabolites in carnivorous plants provide a potentially powerful model system for exploring the role of metabolites in plant evolution. They also show promise for elucidating how the generation of novel compounds, as well as the co-option of pre-existing metabolites, provides a strategy for plants to occupy different environments.

Keywords: Carnivorous plants; ecology; evolution; function; plant-insect; secondary metabolites.

Fig. 1.

Phylogenetic tree of carnivorous plants and research and metabolites identified with known function in carnivory. Branches are to emphasize the location of carnivorous taxa and do not signify time since divergence or a metric of relatedness. Trap morphology is grouped into: (a) flypaper; (b) snap-trap; (c) pitfall; (d) lobster pot; and (e) suction bladder. Colour bands signify a common carnivorous ancestor. Tree generated using NCBI taxonomy browser, iTOL and APG (Chase et al., 2016; Letunic and Bork, 2016). Nepenthales is sensu stricto sister to Caryophyllales (Fleischmann et al., 2018). Twenty-six common compounds are found in the Nepenthales lineage and Sarraceniaceae lineage. Note that Aldrovanda and Utricularia are genera of aquatic carnivorous plants.

Fig. 2.

Function of secondary metabolites in trap coloration requires further investigation. (A) Drosera rotundifolia changes in colour from accumulation of anthocyanin (red pigmentation) in response to environmental stimuli, but this is not confirmed to be related to carnivory. (B) (Upper panel) Nepenthes species show redder locations, possibly to contrast the trap peristome against the background for prey attraction. (Lower panel) Nepenthes spp. also use UV florescence for prey attraction. (C) Sarracenia purpurea, with high diversity of red and green pigmentation from secondary compounds with high background contrast in situ. (Photographs of Nepenthes courtesy of Dr S. Baby in Kurup et al., 2013; Drosera rotundifolia and Sarracenia purpurea photographs are by C. R. Hatcher).

Fig. 3.

Evolution and production zones of metabolites for attraction of prey via use of extrafloral nectaries. Highlighted areas indicate the highest density of extrafloral nectaries for attraction of prey. Areas for secretion of secondary metabolites and nectar are important for prey attraction and capture. Length of phylogenetic branches does not signify relatedness or any other metric of evolution.