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Redalyc.Tropane Alkaloids and Calystegines As Chemotaxonomic Markers in the Solanaceae

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Redalyc.Tropane Alkaloids and Calystegines As Chemotaxonomic Markers in the Solanaceae Anais da Academia Brasileira de Ciências ISSN: 0001-3765 [email protected] Academia Brasileira de Ciências Brasil Pigatto, Aline G.S.; Blanco, Carolina C.; Mentz, Lilian A.; Soares, Geraldo L.G. Tropane alkaloids and calystegines as chemotaxonomic markers in the Solanaceae Anais da Academia Brasileira de Ciências, vol. 87, núm. 4, octubre-diciembre, 2015, pp. 2139-2149 Academia Brasileira de Ciências Rio de Janeiro, Brasil Available in: http://www.redalyc.org/articulo.oa?id=32743236020 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Anais da Academia Brasileira de Ciências (2015) 87(4): 2139-2149 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201520140231 www.scielo.br/aabc Tropane alkaloids and calystegines as chemotaxonomic markers in the Solanaceae ALINE G.S. Pigatto1, CAROLINA C. BLANCO2, LILIAN A. MENTZ1 and GERALDO L.G. SOARES1 1Programa de Pós-Graduação em Botânica, Universidade Federal do Rio Grande do Sul, Campus do Vale, Av. Bento Gonçalves, 9500, Bairro Agronomia, 91501-970 Porto Alegre, RS, Brasil 2Programa de Pós-Graduação em Ecologia, Laboratório de Ecologia Quantitativa, Universidade Federal do Rio Grande do Sul, Campus do Vale, Av. Bento Gonçalves, 9500, Setor 4, Prédio 43422, Sala 205, Bairro Agronomia, 91501-970 Porto Alegre, RS, Brasil Manuscript received on June 10, 2014; accepted for publication on February 20, 2015 ABSTRACT This study assessed the occurrence and distribution of tropane alkaloids and calystegines in genera of the family Solanaceae to identify patterns of distribution and make evolutionary inferences. A database of tropane alkaloids and calystegines occurrences was constructed from the results of a search of scientific websites and a hand search of periodicals. The terms “Solanaceae”, “tropane alkaloids”, and “calystegines” were used as index terms for a full-text article search unrestricted by date of publications. The number of occurrence and chemical diversity indices were calculated and cluster analysis and principal components analysis were performed. Overall, 996 occurrences were reported, 879 of tropane alkaloids (88.3%) and 117 of calystegines (11.7%). The calystegines were significantly more relevant than tropane alkaloids for characterization of distinct groups of genera on both analyses performed here. This corroborates the trend toward a chemical dichotomy observed on database analysis and somewhat reinforces the correlation between geographic distribution and occurrence of secondary metabolites, as the presence of calystegines alone (without tropane alkaloids) was only reported in genera that have South America as their center of diversity. Key words: chemical diversity, number of occurrence, geographic distribution, multivariate analysis, Solanaceae. INTRODUCTION L., Hyoscyamus niger L., and Datura stramonium L.), species of economic relevance (i.e. Nicotiana Solanaceae Juss. is one of the largest and most tabacum L.) and toxic species (i.e. Nicotiana glauca important families of flowering plants, and major Graham) are also classified in this cosmopolitan crop plants species such as Solanum tuberosum family. The greatest species diversity of Solanaceae L., Solanum lycopersicum L., Solanum melongena is observed in the Americas (Olmstead et al. 2008) L., and Capsicum annum L. belong to this taxa. and according to Hunziker (2001) the center of Several species of pharmaceutical interest due to diversity of this taxa is in South America. their secondary metabolites (i.e. Atropa belladonna The first systematic classification of the th Correspondence to: Aline Grohe Schirmer Pigatto Solanaceae was proposed by Dunal in the mid-19 E-mail: [email protected] century and consisted of a division of the 61 genera An Acad Bras Cienc (2015) 87 (4) 2140 ALINE G.S. Pigatto, CAROLINA C. BLANCO, LILIAN A. MENTZ and GERALDO L.G. SOARES known at the time, into two tribes. Two decades calystegines (CAs) exhibit a pattern of distribution later, in 1873, Bentham and Hooker proposed a and frequency of occurrence that establish them new division of 67 genera into five tribes. In the as chemotaxonomic markers in the Solanaceae late 19th century, Wettstein was the first to divide (Schimming et al. 1998, Hunziker 2001, Griffin the Solanaceae into subfamilies: the Solanoideae and Lin 2000). and Cestroideae, comprising three and two tribes TAs are among the earliest active pharma- respectively. Two additional classifications were ceutical ingredients used by man: the first scientific proposed in the 20th century. In 1979 and 1991, studies of a TA - namely atropine, isolated from D’Arcy added the Nolanoideae subfamily to the Atropa belladonna L. - were published in 1809 (Eich two subfamilies proposed before. In 1987, Tétényi 2008). The broad pharmacological effect profile proposed a classification based on chemical of this class of compounds includes mydriatic, characteristics, dividing the family into three antiemetic, antispasmodic, and bronchodilator subfamilies based on the occurrence of alkaloids activity (Grynkiewicz and Gadzikowska 2008). and steroids. The author stressed that the validity The calystegines, in turn, were only discovered of the chemical pattern is based on the biosynthetic in the 1980s, when a group of French researchers pathways of these substances, rather than on their isolated calystegine A3, B1, and B2 from the roots of isolated occurrences. Calystegia sepium R.Br. (Convolvulaceae) (Tepfer Two proposed classifications are currently et al. 1988). Research interest in the CAs is on the accepted. The first, proposed by Hunziker (2001) rise, particularly in view of their potential antiviral, and based on morphological and chemical criteria, anticancer, and antidiabetic effects (Dräger 2004). comprises approximately 2300 species in 92 genera The TAs and CAs are ornithine-derived distributed across the subfamilies Solanoideae, alkaloids and share the bicyclic tropane skeleton Cestroideae, Juanulloideae, Salpiglossoideae, (8-methyl-8-azabicyclo[3.2.1]octane). The tropane Schizanthoideae, and Anthocercidoideae. The ring consists of a pyrrolidine and a piperidine ring, second, a more recent proposal, was presented fused to form a bridged bicyclic structure. Hydroxyl by Olmstead et al. (2008) in a molecular study substitution of tropane at the C3 position yields one conducted on a sample of 89 genera and 190 of two stereoisomers - tropine or pseudotropine - species. The authors proposed seven subfamilies: depending on the orientation (α or β) of the hydroxyl Solanoideae, Cestroideae, Nicotianoideae, group (Bacchi 2002). Tropane alkaloids with a Petunioideae, Schizanthoideae, Goetzeoideae, 3α-hydroxyl substituent are divided into several and Schwenckioideae. Both proposals agree that different groups according to their structural type Solanoideae is the most derived subfamily in (Eich 2008), including esters of 3α-hydroxytropane relation to the Cestroideae. with aliphatic acids, esters of 3α,6β- or 3α,7β- The wealth of information available on the dihydroxytropane, esters of 3α-hydroxytropane secondary metabolites produced by Solanaceae with phenylpropanoid acids, and esters of 6β,7β- species may be used to elucidate taxonomic epoxy-3α-hydroxytropane with S-(–)-tropic issues at the subspecies, species, or even genus acid. Conversely, the 3β-hydroxyl-substituted level. Alkaloids and steroid derivatives (including tropane alkaloids constitute a rather small group steroidal alkaloids) are known to be the main of compounds, including 3β-acetoxytropane and secondary metabolite classes in the Solanaceae. 3β-tigloyloxytropane. It bears stressing that the Among the nitrogen-containing secondary biosynthetic pathway that leads to the formation metabolites, the tropane alkaloids (TAs) and of these compounds also leads to the formation of An Acad Bras Cienc (2015) 87 (4) CHEMOTAXONOMIC MARKERS IN THE SOLANACEAE 2141 CAs, which are nonesterified polyhydroxylated and trimeric forms. The CAs of interest were nortropane alkaloids whose structure consists trihydroxynortropanes, tetrahydroxynortropanes solely of the tropane ring and a varying number of and pentahydroxynortropanes. hydroxyl substituents (three, four, or five) (Dräger NUMBER OF OccURRENCES (NO) AND DIVERSITY INDEX (DI) 2004). It is believed that elucidation of the pattern The NO and the DI were calculated as reported by of TA and CA distribution in the Solanaceae may Santos et al. (2010). The NO was defined as the aid in the understanding of the subdivisions of this sum of all TA and CA structural types found in each family and its geographic distribution patterns. of the studied species. The number of occurrences Within this context, the present study sought to is an indicator of the degree of importance of a construct a database of the occurrences of TAs and certain category of metabolites within a given taxon CAs in Solanaceae species and ascertain whether (Gottlieb et al. 1996) thus providing a snapshot of the patterns of distribution of these compounds the trend toward production of these compounds. corroborate the phylogenetic classification proposed The DI, a rate that expresses the frequency of by Olmstead et al. (2008) and are associated with distribution of a biosynthetic class (Silva 1988), geographic
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