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Frequent Gain and Loss of Pyrrolizidine Alkaloids in the Evolution of Senecio Section Jacobaea (Asteraceae)

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Frequent Gain and Loss of Pyrrolizidine Alkaloids in the Evolution of Senecio Section Jacobaea (Asteraceae) PHYTOCHEMISTRY Phytochemistry 66 (2005) 1285–1295 www.elsevier.com/locate/phytochem Frequent gain and loss of pyrrolizidine alkaloids in the evolution of Senecio section Jacobaea (Asteraceae) Pieter B. Pelser a,b,*, Helene de Vos c, Claudine Theuring d, Till Beuerle d, Klaas Vrieling c, Thomas Hartmann d,* a Department of Botany, Miami University, Oxford, OH 45056, USA b Nationaal Herbarium Nederland, Universiteit Leiden Branch, P.O. Box 9514, 2300 RA Leiden, The Netherlands c Institute of Biology, Leiden University, P.O. Box 9516, 2300 RA Leiden, The Netherlands d Institut fu¨r Pharmazeutische Biologie, Technische Universita¨t Braunschweig, Mendelssohnstrasse 1, D-38106 Braunschweig, Germany Received 18 November 2004; received in revised form 12 January 2005 Available online 17 May 2005 Abstract Pyrrolizidine alkaloids (PAs) of the macrocyclic senecionine type are secondary metabolites characteristic for most species of the genus Senecio (Asteraceae). These PAs are deterrent and toxic to most vertebrates and insects and provide plants with a chemical defense against herbivores. We studied the PA composition of 24 out of 26 species of Senecio section Jacobaea using GC-MS. The PA profiles of eight of these species have not been studied before and additional PAs were identified for most other species that were included in previous studies. With one exception (senecivernine) all 26 PAs identified in sect. Jacobaea can be regarded as derivatives of the biosynthetic backbone structure senecionine. Based on the PA profiles of the species of sect. Jacobaea and the results of pre- vious tracer studies, we constructed two hypothetical biosynthetic scenarios of senecionine diversification. Both scenarios contain two major reactions: the conversion of the necine base moiety retronecine into the otonecine moiety and site-specific epoxidations within the necic acid moiety. Further reactions are site-specific hydroxylations, sometimes followed by O-acetylations, site-specific dehydrogenations, E, Z-isomerizations, and epoxide hydrolysis and chlorolysis. The GC-MS data and both biosynthetic scenarios were subsequently used to study the evolution of PA formation in sect. Jacobaea by reconstructing the evolutionary history of qual- itative PA variation in this section. This was achieved by optimizing additive presence/absence data of PAs and types of enzymatic conversions on a maximum parsimony cladogram of section Jacobaea inferred from DNA sequence and morphological data. Besides showing large intra- and interspecific variation, PA distribution appears to be largely incidental within the whole clade. These results together with the finding that all but one of the PAs identified in sect. Jacobaea are also present in species of other sections of Senecio indicate that differences in PA profiles in Senecio can not be explained by the gain and loss of PA specific genes, but rather by a transient switch-off and switch-on of the expression of genes encoding PA pathway-specific enzymes. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Section Jacobaea; Senecio; Character optimization; Pyrrolizidine alkaloid; Biosynthesis; Chemical diversity; Evolution; Chemical defense 1. Introduction Pyrrolizidine alkaloids (PAs) are secondary metabo- * Corresponding authors. Tel.: +1 513 529 4270; fax: +1 513 529 lites which are only found in the angiosperms. They oc- 4243 (P.B. Pelser), Tel.: +49 531 391 5681; fax: +49 531 391 8104 (T. cur scattered and often sporadically in distantly related Hartmann). E-mail addresses: [email protected] (P.B. Pelser), t.hartmann@ families. PAs are frequently found in some genera of tu-bs.de (T. Hartmann). the tribes Senecioneae and Eupatorieae of the family 0031-9422/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.phytochem.2005.04.015 1286 P.B. Pelser et al. / Phytochemistry 66 (2005) 1285–1295 Asteraceae, many genera of the Boraginaceae, the genus variation in Senecio section Jacobaea (Mill.) Dumort. Crotalaria (Fabaceae), several orchid genera (e.g., Pha- This section has a mainly Eurasian distribution and con- laenopsis), and few genera of the Apocynaceae (e.g., tains 26 species, of which 24 were included in our stud- Parsonsia. In addition, isolated PA occurrences are ies. The biosynthetic relationships of all PAs identified known from single species of the Celastraceae, Convol- in the species of sect. Jacobaea were deduced and related vulaceae, Ranunculaceae, Santalaceae, and Sapotaceae. to the phylogeny of the section, which has recently been Five structural PA-types representing monoesters and elucidated with phylogenetic analyses of nuclear and open-chain or macrocyclic diesters with more than 400 plastid DNA sequences, Amplified Fragment Length compounds are known (Hartmann and Witte, 1995; Polymorphism markers (AFLPs), and morphological Rizk, 1991). PAs of the macrocyclic senecionine type characters (Pelser et al., 2002, 2003, 2004). This ap- comprise a diverse class of more than 100 structures, proach allowed us to quantify variation in PA composi- which are characteristic for PA containing species of tion within a group of closely related species and to infer the tribe Senecioneae, which are primarily species that the evolutionary origin of the variation found. are usually assigned to the genus Senecio. PA biosynthesis has been extensively studied in Sene- cio (Hartmann and Ober, 2000). In all species studied so 2. Results and discussion far, senecionine N-oxide was identified as the primary product of biosynthesis (Hartmann and Toppel, 1987; 2.1. PA diversity in Senecio sect. Jacobaea Toppel et al., 1987) and can be regarded as the back- bone structure of most PAs. It is synthesized in the roots The results of GC-MS analyses of samples of flower- (Sander and Hartmann, 1989) and translocated into the heads of 24 Senecio species of sect. Jacobaea are summa- shoots via the phloem-path (Hartmann et al., 1989) rized in Table 1. Eight of these species have not been where it is transformed into the species-specific PA pro- studied before. A total of 24 PAs were detected and files (Hartmann and Dierich, 1998). Although PAs are identified by their RIs, molecular masses, and mass frag- spatially mobile within the plant, they are stored in vac- mentation patterns in comparison to defined reference uoles (Ehmke et al., 1988) and typically accumulate in compounds or reference data from our PA database the inflorescences and the peripheral stem tissues, i.e. (Witte et al., 1993). The identified PAs cover exclusively epidermal and sub-epidermal cell layers (Hartmann macrocyclic alkaloids of the senecionine type, contain- and Zimmer, 1986; Hartmann et al., 1989). Tracer stud- ing as necine base either retronecine or otonecine (Fig. ies with 14C-labeled senecionine N-oxide applied to a 1(a)). The respective macrocyclic esters of the two necine number of Senecio species (i. e., S. erucifolius, S. inaequi- bases give senecionine (2) and its analog senkirkine (8) dens, S. jacobaea, S. vernalis, and S. vulgaris) revealed and their various derivatives. According to their struc- that the structural diversification of senecionine N-oxide tures, six groups of macrocyclic ester PAs can be distin- requires just one or very few enzymatic modifications guished: (i) senecivernine (Fig. 1(b)), (ii) simple (Hartmann and Dierich, 1998). Besides structural diver- senecionine derivatives (Fig. 1(c)), (iii) simple senkirkine sification, PAs do not underlie any turnover or degrada- derivatives (Fig. 1(d)), (iv) jacobine-related epoxides and tion (Sander and Hartmann, 1989; Hartmann and their derivatives (Fig. 1(e1)), (v) erucifoline-related Dierich, 1998). epoxides (Fig. 1(e2)), and (vi) otosenine related epoxides PAs are known to be deterrent and toxic to most verte- and derivatives (Fig. 1(f)). brates and insects (Boppre´, 1986; Schneider, 1987; Macel, With one exception all identified PAs are also known 2003). Their toxicity bases primarily on the bioactivation to occur in species of other sections of Senecio (Hart- of the molecules by means of cytochrome P450 enzymes mann and Witte, 1995). Only senecicannabine (20) ap- creating pyrrolic intermediates that are highly reactive pears to be unique for two species of sect. Jacobaea with biological nucleophiles, causing cytotoxicity, muta- (i.e., S. ambiguus and S. cannabifolius). An evaluation genicity, and genotoxicity (Frei et al., 1992; Fu et al., of reference data from previous reports on the occur- 2004). PAs therefore probably evolved as plant defensive rence of PAs in species of sect. Jacobaea revealed the chemicals under the selection pressure of herbivory. The presence of additional PAs in some species that were efficiency of PAs as defense compounds is highlighted not identified in the present study. In Table 1 these by the fact that various adapted insects sequester PAs structures are indicated by letters and related to the from their food-plants and utilize them for their own pro- respective references. Two PAs reported in the literature tection against predators and parasitoids. Among those for species of sect. Jacobaea could not be identified in adapted insects are leaf beetles, moths, butterflies, grass- our study. These are retrorsine (Fig. 1(c), A1) (the 20- hoppers, and aphids (for a review see Hartmann, 1999, Z-isomer of usaramine (16), reported from S. jacobaea), 2004; Hartmann and Ober, 2000). and onetine (Fig. 1(f), A2) (the otonecine analog of jac- In order to learn more about the evolutionary diver- oline (9), reported from S. othonnae)(Hartmann and sification of PAs in
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