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Chemotaxonomic Investigation of Apocynaceae for Retronecine-Type Pyrrolizidine 2 Alkaloids Using HPLC-MS/MS 3 4 Lea A

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Chemotaxonomic Investigation of Apocynaceae for Retronecine-Type Pyrrolizidine 2 Alkaloids Using HPLC-MS/MS 3 4 Lea A bioRxiv preprint doi: https://doi.org/10.1101/2020.08.23.260091; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Chemotaxonomic Investigation of Apocynaceae for Retronecine-Type Pyrrolizidine 2 Alkaloids Using HPLC-MS/MS 3 4 Lea A. Barny1, Julia A. Tasca1,2, Hugo A. Sanchez1, Chelsea R. Smith3, Suzanne Koptur4, Tatyana 5 Livshultz3,5,*, Kevin P. C. Minbiole1,* 6 1Department of Chemistry, Villanova University, Villanova, PA 19085, USA 7 2Department of Biochemistry and Molecular Biophysics, Perelman School of Medicine at the 8 University of Pennsylvania, 3400 Civic Center Blvd, Philadelphia, PA 19104, USA 9 3Department of Biodiversity Earth and Environmental Sciences, Drexel University, PA 19104, 10 USA 11 4Department of Biology, Florida International University, 11200 SW 8th St, Miami, FL 33199 12 5Department of Botany, Academy of Natural Sciences of Drexel University, 1900 Benjamin 13 Franklin Parkway, Philadelphia PA, 19103, USA 14 Email addresses: 15 LAB: [email protected] 16 JAT: [email protected] 17 HAS: [email protected] 18 CRS: [email protected] 19 SK: [email protected] 20 TL: [email protected] 21 KPCM: [email protected] 22 * Authors for correspondence: [email protected] and [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.23.260091; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 23 ABSTRACT: 24 Apocynaceae are well-known for diverse specialized metabolites that are distributed in a 25 phylogenetically informative manner. Pyrrolizidine alkaloids (PAs) have been reported sporadically in 26 one lineage in the family, the APSA clade, but few species had been studied to date. We conduct the 27 first systematic survey of Apocynaceae for retronecine-type PAs, sampling leaves from 231 species from 28 13 of 16 major lineages within the APSA clade using HPLC-MS/MS. We also follow up on preliminary 29 evidence for infra-specific variation of PA detectability in Echites umbellatus Jacq. Four precursor ion 30 scans (PREC) were developed for a high-throughput survey for chemicals containing a structural moiety 31 common to many PAs, the retronecine core. We identified with high confidence PAs in 7 of 8 sampled 32 genera of tribe Echiteae, but not in samples from the closely related Odontadenieae and Mesechiteae, 33 confirming the utility of PAs as a taxonomic character in tribal delimitation. The presence of PAs in 34 Malouetieae was confirmed, as we report with high confidence their presence in Galactophora 35 schomburgkiana Woodson and Eucorymbia alba Stapf, but currently we have low confidence of their 36 presence in Holarrena pubescens Wall. ex G. Don (the one Malouetieae species where they were 37 previously reported), as well as in Kibatalia macrophylla (Pierre ex Hua) Woodson and in Holarrena 38 curtisii King & Gamble. For the first time the presence of PAs in species of Wrightia R. Br. (Wrightieae) 39 and Marsdenia R. Br. (Marsdenieae) was confirmed. Detectability of PAs was found to vary among 40 samples of Echites umbellatus and intra-individual plasticity contributes to this variation. Of toxicological 41 importance, novel potential sources of human exposure to pro-toxic PAs were identified in the 42 medicinal plants, Wrightia tinctoria R.Br. and Marsdenia tinctoria R.Br., and the food plant, Echites 43 panduratus A. DC., warranting immediate further research to elucidate the structures of the candidate 44 PAs identified. Method development and limitations are discussed. 45 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.23.260091; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 46 Keywords: Apocynaceae, chemotaxonomy, pyrrolizidine alkaloids, retronecine, phenotypic 47 plasticity 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.23.260091; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 48 1. Introduction 49 The study of plant specialized metabolites in a phylogenomic framework promises to fulfill the 50 original goal of chemotaxonomy: identification of lineage diagnostic metabolites (Fairbrothers et al., 51 1975). In combination with other –omic, biochemical, and ecological approaches, chemotaxonomy 52 permits the testing of key hypotheses about the evolutionary assembly and fates of novel metabolic 53 pathways (Scossa and Fernie, 2020) as well as the role of plants’ interactions with their environments, 54 including co-evolution with their specialized herbivores, in shaping plant metabolic diversity (Futuyma 55 and Agrawal, 2009). One of the primary impediments to pursuit of this research agenda in large plant 56 families is the fragmentary knowledge of the taxonomic occurrence of specialized metabolites. The 57 published literature on natural products contains multiple biases, with the absence of a class of 58 metabolites in a species being particularly hard to infer from studies that have not specifically targeted a 59 compound class. Systematic surveys for chemicals of interest are often also impeded by availability of 60 tissues across a breadth of species; this can be compounded by the lack of high-throughput, sensitive 61 and selective analytical methods to maximize compound identification from small quantities of test 62 material (Tasca et al., 2018). Infraspecific variation, a ubiquitous feature of plant specialized metabolism 63 (Hartmann, 1996; Moore et al., 2014), can further introduce confusion about the distribution of a 64 metabolite via contradictory reports in the literature. 65 Apocynaceae are the tenth largest angiosperm plant family, with ca. 5300 species classified in 66 378 genera (Endress et al., 2018). The family is of particular importance in natural products research 67 because of the occurrence of multiple medicinally important species and compounds including 68 monoterpenoid indole alkaloids, particularly the chemotherapy drugs vincristine and vinblastine in 69 Catharanthus roseus (L.) G.Don (Aslam et al., 2010). The expense and difficulty of deriving these valuable 70 molecules from natural sources has motivated the complete biochemical elucidation of their 71 biosynthetic pathway as a steppingstone to its genetic engineering (Caputi et al., 2018; Qu et al., 2019). 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.23.260091; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 72 The genus Asclepias L. and its specialized herbivores are a model system in chemical ecology and 73 evolution of reciprocal adaptations between plants and herbivores, with a particular focus on 74 cardenolides (Agrawal et al., 2012). Pyrrolizidine alkaloids are also implicated in co-evolution between 75 Apocynaceae and one of their specialized herbivore lineages, Lepidoptera subfamily Danainae 76 (milkweed and clearwing butterflies), and the evolution of the first gene of their biosynthetic pathway, 77 homospermidine synthase (hss), has been elucidated (Livshultz et al., 2018a). Researchers have 78 detected phylogenetic signals in the distribution of all of these compounds and others, including 79 steroidal and phenanthroindolizidine alkaloids and steroidal glycosides, in Apocynaceae (Endress et al., 80 2018), but knowledge of their taxonomic distribution still lags progress on the phylogeny of the family 81 (Fishbein et al., 2018). 82 83 Pyrrolizidine alkaloids (PAs) are secondary metabolites containing a 1-hydroxymethylated 84 necine core, esterified with a necic acid. The necine base (often referred to as a pyrrolizidine) presents 85 as a heterocycle containing a nitrogen atom positioned at the junction of two fused five-membered 86 rings (Hartmann and Witte, 1995) (Figure 1). Depending on the necine base present, PAs can be 87 classified into five main types: retronecine (155 Da) or its less common diastereomer, heliotridine (155 88 Da), the monocyclic otonecine (185 Da) (These et al., 2013), the fully saturated platynecine (157 Da) (Lin 89 et al., 1998), or the triol rosmarinecine (173 Da) (De Waal, 1941). OH OH OH HO O OH OH HO H HO H HO HO N OH N N N N Otonecine Rosmarinecine 90 (+)-Retronecine (+)-Heliotridine Platynecine 91 Fig. 1. Varied necine base structures found in pyrrolizidine alkaloids. 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.23.260091; this version posted August 24, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 92 Additionally, due to the immense structural diversity imparted by various combinations of 93 necine bases with necic acids, PAs are primarily characterized according to esterification pattern and 94 necic acid type (Hartmann and Witte, 1995) (Fig. 2). O OR R 3 R' R'' R'' 2 R4 O O Necic R' O R' R1 O O O O O O Acid O O HO H O H O H O H Necine N Base N N N monoester 95 (I) Open chain (II) Open chain diester (III) Cyclic diester (IV) Cyclic triester 96 Fig.
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