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Asteraceae: Vernonieae) in a Phylogenetic Context

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Asteraceae: Vernonieae) in a Phylogenetic Context RESEARCH ARTICLE Comprehensive untargeted metabolomics of Lychnnophorinae subtribe (Asteraceae: Vernonieae) in a phylogenetic context Maria Elvira Poleti Martucci1, Benoit Loeuille2, Jose Rubens Pirani2, Leonardo Gobbo- Neto1* 1 University of São Paulo, School of Pharmaceutical Sciences of Ribeirão Preto, Ribeirão Preto, Sao Paulo, Brazil, 2 University of São Paulo, Institute of Biosciences, Department of Botany, São Paulo, Sao Paulo, Brazil a1111111111 a1111111111 * [email protected] a1111111111 a1111111111 a1111111111 Abstract Members of the subtribe Lychnophorinae occur mostly within the Cerrado domain of the Brazilian Central Plateau. The relationships between its 11 genera, as well as between OPEN ACCESS Lychnophorinae and other subtribes belonging to the tribe Vernonieae, have recently been Citation: Martucci MEP, Loeuille B, Pirani JR, investigated upon a phylogeny based on molecular and morphological data. We report Gobbo-Neto L (2018) Comprehensive untargeted the use of a comprehensive untargeted metabolomics approach, combining HPLC-MS and metabolomics of Lychnnophorinae subtribe GC-MS data, followed by multivariate analyses aiming to assess the congruence between (Asteraceae: Vernonieae) in a phylogenetic context. metabolomics data and the phylogenetic hypothesis, as well as its potential as a chemotax- PLoS ONE 13(1): e0190104. https://doi.org/ 10.1371/journal.pone.0190104 onomic tool. We analyzed 78 species by UHPLC-MS and GC-MS in both positive and nega- tive ionization modes. The metabolic profiles obtained for these species were treated in Editor: Doralyn S Dalisay, University of San Agustin, PHILIPPINES MetAlign and in MSClust and the matrices generated were used in SIMCA for hierarchical cluster analyses, principal component analyses and orthogonal partial least square discrimi- Received: July 25, 2017 nant analysis. The results showed that metabolomic analyses are mostly congruent with the Accepted: December 10, 2017 phylogenetic hypothesis especially at lower taxonomic levels (Lychnophora or Eremanthus). Published: January 11, 2018 Our results confirm that data generated using metabolomics provide evidence for chemo- Copyright: © 2018 Martucci et al. This is an open taxonomical studies, especially for phylogenetic inference of the Lychnophorinae subtribe access article distributed under the terms of the and insight into the evolution of the secondary metabolites of this group. Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information Introduction files. Vernonieae contains 21 currently recognized subtribes [1±4]. Among these, the subtribe Lych- Funding: This work was supported by FundacËão de nophorinae is nearly endemic to Brazil [1,2,5,6]. Additionally, it contains 18 genera and ca. Amparo à Pesquisa do Estado de São Paulo (http:// 120 species [1,2,5,6]. Most species are restricted to campo rupestre (literally rocky fields) in www.fapesp.br/) (grants 2010/51454-3 J.R.P. and the highlands of southeastern and northeastern Brazil and to the Cerrado domain (Brazilian L.G.N. and 2012/16646-4 M.E.P.M.), Conselho savanna). From a phytochemical point of view, these species exhibit high diversity of com- Nacional de Desenvolvimento CientõÂfico e TecnoloÂgico (http://cnpq.br/) (grant 471615/2013- pounds. Flavonoids and terpenoids have been extensively identified; reviewing the absence of 7 - L.G.N.) and Alexander von Humboldt Stiftung diterpenes and the extensive reports of sesquiterpene lactones (SLs) from the germacranolides (https://www.humboldt-foundation.de/web/home. (specifically germacrolides and heliangolides sub-types) and guaianolides types [7±10]. In a PLOS ONE | https://doi.org/10.1371/journal.pone.0190104 January 11, 2018 1 / 13 Untargeted metabolomics of Lychnnophorinae subtribe (Asteraceae: Vernonieae) html) L.G.N. The funders had no role in study review of American Vernonieae [11, 12], was proposed a morphological definition of Lychno- design, data collection and analysis, decision to phorinae that is rather consistent with the recent phylogeny of the American Vernonieae [3]. publish, or preparation of the manuscript. This latter work also indicates the inclusion in Lychnophorinae of two small subtribes (Cen- Competing interests: The authors have declared tratherinae, Sipolisiinae) and three small genera (Albertinia, Blanchetia and Gorceixia) previ- that no competing interests exist. ously placed in subtribes Vernoniinae and Piptocarphinae. However, the subtribe holds a high proportion of monotypic genera (42%), reflecting how poorly understood relationships between the genera of the group are. The generic limits of the two diversified genera (ca. 50%), Eremanthus and Lychnophora, are controversial [3,5]. Haplos- tephium [10,13,14,15], Lychnophoriopsis [5] and Paralychnophora [6,16] have been variously recognized at a generic level. Also, several species of Lychnophorinae have an uncertain generic position (in Eremanthus, Lychnophora or Piptolepis) [17,18]. In a phylogeny of Lych- nophorinae based on DNA sequences and morphological data [5], the richest genus of the sub- tribe was Lychnophora, with 32 described species, but it emerged as polyphyletic, involving three main lineages not closely related. Most of the obtained clades were associated with some existing generic concepts and they can be defined by a simple combination of morphological characteristics Albertinia, Blanchetia and Gorceixia are the earliest diverging lineages, whereas Eremanthus and Lychnophora strict sensu emerged as the most derived clade, which contains half of the species of the subtribe. However, relationships between the remaining clades persist partially unresolved, and some generic concepts require further refinement. Metabolomics involves the study of metabolites in biological systems and aims to establish chemical or metabolite differences among samples, relating them to genotypes of each species [19,20]. The untargeted metabolomics analysis aims to establish global metabolite signals mea- sured by one or more analytical platforms [21]. During the last decades, these approaches have benefited by improvements in hyphenated mass spectrometry (UHPLC-MS and GC-MS), which has become highly sensitive and allows a more complete chemical profile of the ana- lyzed samples [20]. Metabolomics approaches may be a valuable tool for chemotaxonomic characterization and providing primary data for phylogenetic inference. In a recent study, we used metabolo- mics aimed at higher plant chemotaxonomical purposes, showing the applicability of untar- geted analysis to help with taxonomical classifications [22]. In this study, we report the use of a comprehensive untargeted metabolomics approach, employing UHPLC(DAD)-MS(ESI-ORBITRAP) and GC-MS(EI) data combined, followed by multivariate analyses. Thereafter, we compared our results to the phylogenetic hypothesis pro- posed by Loeuille et al. (2015b). Finally, we evaluated the possibility of employment of untar- geted metabolomics as a chemotaxonomic tool for Lychnophorinae subtribe classification. Materials and methods Plant material Seventy-eight species (Supporting Material) belonging to the Lychnophorinae subtribe were analyzed in this study. Collection and access of samples from the Brazilian Genetic Heritage was authorized by IEF and CNPq/CGen (010091/2011-4) respectively. The samples used for the metabolomics approach were the same used in phylogenetic analyses by Loeuille et al. (2015b). In this study, similar with that of Loeuille et al. (2015b), only one specimen of each species was analyzed for the purpose of mutual comparison. Furthermore, there are substantial evidences that there is no significant chemical qualitative variation between individuals from the same population of plants from this subtribe [5,7,8,23]. In addition, most of the species studied are micro-endemics with very few populations, such a scenario offers a low probability for infraspecific chemical qualitative variation. One replicate of each species was sampled for PLOS ONE | https://doi.org/10.1371/journal.pone.0190104 January 11, 2018 2 / 13 Untargeted metabolomics of Lychnnophorinae subtribe (Asteraceae: Vernonieae) both UHPLC-MS and GC-MS analyses. To avoid analytical variations, the analyses were per- formed injecting 10 samples/batch and the injection of all samples was performed within a four days interval. To detect eventual variations, the same sample was analyzed before and after each batch. Eventual deviations in the internal standard retention times and areas in all the chromatograms were also checked. Instrumentation The UHPLC-MS and UHPLC-HCD MS/MS experiments were performed using an Accela UHPLC apparatus with a diode array detector (Accela) coupled to an ESI-Orbitrap mass spec- trometer Exactive Plus (Thermo Scientific). The GC-MS experiments were performed using GC coupled to an EI mass spectrometer QP2010 Shimadzu. UHPLC-MS and UHPLC-HCD MS/MS analyses. UHPLC-MS and UHPLC-HCD MS/ MS analyses were performed using a core shell column (Kinetex 1.7 μm XB-C18, 150 X 2.1 mm, Phenomenex) connected to a guard cartridge of the same material. Separation was per- -1 formed at a flow rate of 400 μL.min and a gradient of H2O-HCO2H (0.1%) (v/v) (A) and CH3CN (B) as mobile phases; the elution profile was: 0±2 min, 5% B; 2±30 min, 5±100% B; 30±34 min (column washing), 100% B; 34±37 min, 100±5%
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