Handling dangerous molecules: Transport and compartmentation of plant natural products

Abstract

The plant cell faces a dilemma: secondary products provide a multitude of defence and signalling functions, but their biosynthesis poses a severe burden, as it competes for energy sources and building blocks and may generate toxic products. Thus, evolution of recent secondary metabolites is not only driven by their advantageous functions but also selects for strict control mechanisms including the integration of biosynthesis into the cellular ultrastructure. In order to minimize the risk of self-intoxication, secondary products are usually targeted into compartments of low metabolic activity, notably the vacuole and the extracellular space. This is most obvious for phenolic substances but also for alkaloids, the best studied plant toxins. Compartmentation on a cellular or subcellular level is also instrumental in plants synthesizing preformed defence substances such as cyanogenic glycosides in order to assure that the active toxins are only liberated in case of an attack. Biosynthetic pathways and regulatory elements are well-established at least for some natural compound classes such as the flavonoids. In contrast, our knowledge of transport steps behind the subcellular distribution of these substances is just scratching the surface. This chapter provides an overview on transport processes involved in secondary metabolite compartmentation that is concentrated at the best known areas of flavonoid and alkaloid production. Starting from 'classical' data of secondary metabolite transport we characterize the actually known transporters - which mainly belong to the ATP-Binding Cassette (ABC) or Multidrug and Toxic Extrusion (MATE) superfamilies - and their specific functioning in cells and tissues as analyzed by modern experimental techniques. The 'transporter' hypothesis is confronted with 'vesicle transport' models of subcellular trafficking. Although it appears premature to find common ground between these alternative models, the discovery of novel cellular functions of secondary metabolites facilitates our understanding of an intimate interplay between biosynthetic steps, transmembrane fluxes and metabolic channels, i.e. the plant's solution to the 'toxic dilemma'.