Polyphyletic Origin of Pyrrolizidine Alkaloids within the Asteraceae. Evidence from Differential Tissue Expression of Homospermidine Synthase

Abstract

The evolution of pathways within plant secondary metabolism has been studied by using the pyrrolizidine alkaloids (PAs) as a model system. PAs are constitutively produced by plants as a defense against herbivores. The occurrence of PAs is restricted to certain unrelated families within the angiosperms. Homospermidine synthase (HSS), the first specific enzyme in the biosynthesis of the necine base moiety of PAs, was originally recruited from deoxyhypusine synthase, an enzyme involved in the posttranslational activation of the eukaryotic initiation factor 5A. Recently, this gene recruitment has been shown to have occurred several times independently within the angiosperms and even twice within the Asteraceae. Here, we demonstrate that, within these two PA-producing tribes of the Asteraceae, namely Senecioneae and Eupatorieae, HSS is expressed differently despite catalyzing the same step in PA biosynthesis. Within Eupatorium cannabinum, HSS is expressed uniformly in all cells of the root cortex parenchyma, but not within the endodermis and exodermis. Within Senecio vernalis, HSS expression has been previously identified in groups of specialized cells of the endodermis and the adjacent root cortex parenchyma. This expression pattern was confirmed for Senecio jacobaea as well. Furthermore, the expression of HSS in E. cannabinum is dependent on the development of the plant, suggesting a close linkage to plant growth.

Pyrrolizidine Alkaloid Biosynthesis in Phalaenopsis Orchids: Developmental Expression of Alkaloid-Specific Homospermidine Synthase in Root Tips and Young Flower Buds

“…Thus, the expression pattern of PA biosynthesis within Phalaenopsis is completely different from that found in other PA-producing species (i.e. S. vernalis and E. cannabinum of the Senecioneae and Eupatorieae tribe within the Asteraceae, respectively (Moll et al, 2002;Anke et al, 2004). These results add a further facet to the diversity of plant secondary metabolism and indicate the complexity of processes that were necessary in evolution to integrate new pathways within plant metabolism.…”

“…catalysis of the first specific step within PA biosynthesis). In contrast to Senecio, HSS within E. cannabinum is expressed in all cells of the cortex parenchyma, excluding the endodermis (Moll et al, 2002;Anke et al, 2004). We have interpreted this observation as providing further support for the independent origin of PA biosynthesis in these two lineages of the Asteraceae (Anke et al, 2004;Reimann et al, 2004).…”

Cell Type–Specific Localization of Transcripts Encoding Nine Consecutive Enzymes Involved in Protoberberine Alkaloid Biosynthesis

“…Two scenarios have emerged concerning the relationship between the cell type-specific localization and evolutionary origin of plant alkaloids. In the case of pyrrolizidine alkaloids, the differential localization of a key pathway enzyme has been interpreted to support the independent origin of the biosynthetic pathway in various lineages (Anke et al, 2004). By contrast, the differential cell type-specific localization of benzylisoquinoline alkaloid gene transcripts in T. flavum and P. somniferum implicates the migration of established pathways between cell types as a key feature of phytochemical evolution.…”

“…Biosynthetic enzymes or gene transcripts involved in the initial and final steps of tropane alkaloid biosynthesis were colocalized to the pericycle (Hashimoto et al, 1991;Suzuki et al, 1999), whereas an intermediate enzyme was found in the adjacent endodermis and nearby cortical cells in Atropa belladonna and Hyoscyamus muticus (Nakajima and Hashimoto, 1999). Pyrrolizidine alkaloids also accumulate in aerial organs but are synthesized in endodermal and cortical cells immediately adjacent to the phloem in roots of Senecio vernalis (Moll et al, 2002) or throughout the cortex in roots of Eupatorium cannabinum (Anke et al, 2004). In Papaver somniferum, benzylisoquinoline alkaloids accumulate in specialized laticifers, but biosynthetic gene transcripts and enzymes are restricted to companion cells and sieve elements, respectively (Facchini and De Luca, 1995;Bird et al, 2003).…”

New aspect of plant–rhizobia interaction: Alkaloid biosynthesis in Crotalaria depends on nodulation

“…dhs expression has been described as being correlated with cell proliferation (28) and was shown, in contrast to hss, to be transcribed uniformly in most plant tissues (26,29,30). Moreover, for Crotalaria, we found transcript levels of dhs to be constant in all analyzed tissues, but at an extremely low level (on average, 800-fold lower than that of hss, using actin as a reference) (Fig.…”