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Planta Med 2021; 87(01/02): 113-123
DOI: 10.1055/a-1315-0666
Natural Product Chemistry and Analytical Studies
Original Papers

Molecular Networking Discloses the Chemical Diversity of Flavonoids and Selaginellins in Selaginella convoluta

Fernanda Priscila Santos Reginaldo
1   Department of Pharmacy, Federal University of Rio Grande do Norte (UFRN), Natal/RN, Brazil
,
Paula Carolina Pires Bueno
2   Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo (FCFRP-USP), Ribeirão Preto/SP, Brazil
3   Max-Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany
,
Isabelly CristinaMatos Costa de
1   Department of Pharmacy, Federal University of Rio Grande do Norte (UFRN), Natal/RN, Brazil
,
AlanAraújo Roque de
4   Institute for Sustainable Development and Environment, Dunas Park Herbarium, Natal/RN, Brazil
,
Arthur Germano Fett-Neto
5   Laboratory of Plant Physiology, Center for Biotechnology and Department of Botany, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre/RS, Brazil
,
Alberto José Cavalheiro
6   Institute of Chemistry, São Paulo State University (UNESP), Araraquara/SP, Brazil
,
Raquel Brandt Giordani 
1   Department of Pharmacy, Federal University of Rio Grande do Norte (UFRN), Natal/RN, Brazil
› Author AffiliationsSupported by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Finance Code 001
Supported by: Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq [445149/2014-0]
Supported by: Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq/INCTBioNat [465637/2014-0]
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo #2017/19702-6
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo #2019/08477-7
Supported by: Fundação de Amparo à Pesquisa do Estado de São Paulo FAPESP - INCTBioNat 2014/50926-0
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Abstract

Selaginella convoluta is a desiccation tolerant plant native to the Brazilian semiarid region (Caatinga), endowed with an effective drought resistance mechanism. As part of our research efforts to understand the chemical diversity of S. convoluta, dehydrated (harvested in their natural habitat in the dry season) and hydrated (plant acclimated in a laboratory after rehydration) specimens were analyzed by HR-LC-ESI-MS/MS followed by a structural annotation on the Global Natural Products Social Molecular Networking Web platform. The molecular networking approach allowed for putative annotation of 39 metabolites, mainly selaginellins and flavonoids. Based on MS/MS data, three unprecedented selaginellins were annotated: 29-hydroxy selaginellin O, 29-hydroxy selaginellin A, and 4-{[2-(4-hydrophenyl)-6-[2-(4-hydroxyphenyl)ethynyl]phenyl](4-oxocyclohexa-2,5-dien-1-ylidene)methyl}benzaldehyde. Th results pointed out that valuable scientific knowledge can be obtained from studies conducted with plants in their natural habitat by allowing a more realistic profile of chemical diversity. The present study adds new information on specialized metabolites of S. convoluta, mainly flavonoids and selaginellins, and highlights the species as an untapped source of chemobiodiversity from Caatinga.

Key words

Selaginella convoluta - Selaginellaceae - selaginellins - flavonoids - Caatinga

Supporting Information

    Base peak chromatogram in positive and negative electrospray ionization modes of the methanol extract of shoots and S. convoluta at different hydration states (Fig. 1S), representation of all MN (Fig. 2S), representation of MN after blank removal showing O-glycosyl metabolite clusters (Fig. 3S), the general structure of selaginellins (Fig. 4S), proposal of fragmentation of original selaginellins (Fig. S5), proposal of fragmentation of the annotated selaginellins (Fig. 6S), the MS/MS spectral of the O-glycosyl metabolite cluster (Fig. 7S), and the MS/MS spectral of phenolic derivatives (Fig. 8S) are available as Supporting Information.

  • Supporting Information


Publication History

Received: 30 April 2020

Accepted after revision: 11 November 2020

Article published online:
09 December 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Iturriaga G, Cushman MAF, Cushman JC. An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Sci 2006; 170: 1173-1184
    CrossrefPubMedGoogle Scholar
  • 2 Deeba F, Pandey V, Pathre U, Kanojiya S. Proteome analysis of detached fronds from a resurrection plant Selaginella bryopteris – response to dehydration and rehydration. J Proteomics Bioinform 2009; 2: 108-116
    CrossrefPubMedGoogle Scholar
  • 3 Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S. Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 2010; 9: 6561-6577
    CrossrefPubMedGoogle Scholar
  • 4 Oliveira AAQ, Moraes MG. Dehydration and rehydration in Selaginella sellowii Hieron. aerial parts, a desiccation tolerant species. Bol Mus Biol Mello Leitão 2015; 37: 393-403
    PubMedGoogle Scholar
  • 5 Yordanov I, Velikova V, Tsonev T. Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 2000; 38: 171-186
    CrossrefPubMedGoogle Scholar
  • 6 Blum A. Drought resistance, water-use efficiency, and yield potentialare they compatible, dissonant, or mutually exclusive?. Aust J Agric Res 2005; 56: 1159-1168
    CrossrefPubMedGoogle Scholar
  • 7 Barros ICL, Silva AJR, Silva LLS. Levantamento florístico das pteridófitas ocorrentes na Zona das Caatingas do Estado de Pernambuco. Biol Bras 1989; 1: 143-159
    PubMedGoogle Scholar
  • 8 Ambrósio ST, Melo NF. New records of pteridophytes in the semi-arid region of Brazil. Am Fern J 2001; 91: 227-229
    CrossrefPubMedGoogle Scholar
  • 9 Giorgetti M, Negri G, Rodrigues E. Brazilian plants with possible action on the central nervous system: a study of historical sources from the 16th to 19th century. J Ethnopharmacol 2007; 109: 338-347
    CrossrefPubMedGoogle Scholar
  • 10 de Sá PG, Nunes XP, de Lima JT, de Siqueira Filho JA, Fontana AP, Siqueira Jde S, Quintans-Júnior LJ, Damasceno PK, Branco CR, Branco A, Almeida JR. Antinociceptive effect of ethanolic extract of Selaginella convoluta in mice. BMC Complement Altern Med 2012; 12: 1-7
    CrossrefPubMedGoogle Scholar
  • 11 Agra MF, Baracho GS, Nurit K, Basílio IJ, Coelho VP. Medicinal and poisonous diversity of the flora of “Cariri Paraibano”, Brazil. J Ethnopharmacol 2007; 111: 383-395
    CrossrefPubMedGoogle Scholar
  • 12 de Albuquerque UP, Muniz de Medeiros P, de Almeida AL, Monteiro JM, Machado de Freitas Lins Neto E. Gomes de Melo J, dos Santos JP. Medicinal plants of the caatinga (semi-arid) vegetation of NE Brazil: a quantitative approach. J Ethnopharmacol 2007; 114: 325-354
    CrossrefPubMedGoogle Scholar
  • 13 Santos Reginaldo FP, de Matos Costa IC, Giordani RB. Selaginellaceae: traditional use, phytochemistry and pharmacology. Blacpma 2020; 19: 247-288
    PubMedGoogle Scholar
  • 14 de Sá PGS, Guimarães AL, Oliveira AP, Siqueira Filho JA, Fontana AP, Damasceno PKF, Branco CRC, Branco A, da Silva Almeida JRG. Fenois totais, flavonoides totais e atividade antioxidante de Selaginella convoluta (Arn.) Spring (Selaginellaceae). J Basic Appl Pharm Sci 2012; 33: 561-566
    PubMedGoogle Scholar
  • 15 de Oliveira Macêdo LAR, de Oliveira Júnior RG, Souza GR, de Oliveira AP, de Lavor EM, Gama e Silva M, Pacheco AGM, de Menezes IRA, Coutinho HDM, do Ó Pessoa C, da Costa MP, da Silva Almeida JRG. Chemical composition, antioxidant and antibacterial activities and evaluation of cytotoxicity of the fractions obtained from Selaginella convoluta (Arn.) Spring (Selaginellaceae). Biotechnol Biotechnol Equip 2018; 32: 506-512
    CrossrefPubMedGoogle Scholar
  • 16 Allwood JW, Goodacre R. An introduction to liquid chromatography–mass spectrometry instrumentation applied in plant metabolomic analyses. Phytochem Anal 2010; 21: 33-47
    CrossrefPubMedGoogle Scholar
  • 17 Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T, Porto C, Bouslimani A, Melnik AV, Meehan MJ, Liu WT, Crüsemann M, Boudreau PD, Esquenazi E, Sandoval-Calderón M, Kersten RD, Pace LA, Quinn RA, Duncan KR, Hsu CC, Floros DJ, Gavilan RG, Kleigrewe K, Northen T, Dutton RJ, Parrot D, Carlson EE, Aigle B, Michelsen CF, Jelsbak L, Sohlenkamp C, Pevzner P, Edlund A, McLean J, Piel J, Murphy BT, Gerwick L, Liaw CC, Yang YL, Humpf HU, Maansson M, Keyzers RA, Sims AC, Johnson AR, Sidebottom AM, Sedio BE, Klitgaard A, Larson CB, Boya CA, Torres-Mendoza D, Gonzalez DJ, Silva DB, Marques LM, Demarque DP, Pociute E, OʼNeill EC, Briand E, Helfrich EJN, Granatosky EA, Glukhov E, Ryffel F, Houson H, Mohimani H, Kharbush JJ, Zeng Y, Vorholt JA, Kurita KL, Charusanti P, McPhail KL, Nielsen KF, Vuong L, Elfeki M, Traxler MF, Engene N, Koyama N, Vining OB, Baric R, Silva RR, Mascuch SJ, Tomasi S, Jenkins S, Macherla V, Hoffman T, Agarwal V, Williams PG, Dai J, Neupane R, Gurr J, Rodríguez AMC, Lamsa A, Zhang C, Dorrestein K, Duggan BM, Almaliti J, Allard PM, Phapale P, Nothias LF, Alexandrov T, Litaudon M, Wolfender JL, Kyle JE, Metz TO, Peryea T, Nguyen DT, VanLeer D, Shinn P, Jadhav A, Müller R, Waters KM, Shi W, Liu X, Zhang L, Knight R, Jensen PR, Palsson BØ, Pogliano K, Linington RG, Gutiérrez M, Lopes NP, Gerwick WH, Moore BS, Dorrestein PC, Bandeira N. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotechnol 2016; 34: 828-837
    CrossrefPubMedGoogle Scholar
  • 18 Watrous J, Roach P, Alexandrov T, Heath BS, Yang JY, Kersten RD, van der Voort M, Pogliano K, Gross H, Raaijmakers JM. Mass spectral molecular networking of living microbial colonies. PNAS 2012; 109: E1743-E1752
    CrossrefPubMedGoogle Scholar
  • 19 Ramos AEF, Evanno L, Poupon E, Champy P, Beniddir MA. Natural products targeting strategies involving molecular networking: different manners, one goal. Nat Prod Rep 2019; 36: 960-980
    CrossrefPubMedGoogle Scholar
  • 20 Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TWM, Fiehn O, Goodacre R, Griffin JL, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane AN, Lindon JC, Marriott P, Nicholls AW, Reily MD, Thaden JJ, Viant MR. Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 2007; 3: 211-221
    CrossrefPubMedGoogle Scholar
  • 21 Chen H, Hao ZY, Wang XL, Zheng XK, Feng WS, Wang YZ. Sinensioside A, a new sesquilignan glycoside from Selaginella sinensis . Chin J Nat Med 2014; 12: 148-150
    PubMedGoogle Scholar
  • 22 Guan H, Luo X, Chang X, Su M, Li Z, Li P, Wang X, Shi Y. Identification of the chemical constituents of an anti-arthritic chinese medicine Wen Luo Yin by liquid chromatography coupled with mass spectrometry. Molecules 2019; 24: 233-245
    CrossrefPubMedGoogle Scholar
  • 23 Weng JK, Noel JP. Chemodiversity in Selaginella: a reference system for parallel and convergent metabolic evolution in terrestrial plants. Front Plant Sci 2013; 4: 119-127
    PubMedGoogle Scholar
  • 24 Geng P, Sun J, Zhang M, Li X, Harnly JM, Chen P. Comprehensive characterization of C-glycosyl flavones in wheat (Triticum aestivum L.) germ using UPLC-PDA-ESI/HRMS(n) and mass defect filtering. J Mass Spectrom 2016; 51: 914-930
    CrossrefPubMedGoogle Scholar
  • 25 Woo S, Kang KB, Kim J, Sung SH. Molecular networking reveals the chemical diversity of selaginellin derivatives, natural phosphodiesterase-4 inhibitors from Selaginella tamariscina . J Nat Prod 2019; 82: 1820-1830
    CrossrefPubMedGoogle Scholar
  • 26 Demarque DP, Crotti AE, Vessecchi R, Lopes JL, Lopes NP. Fragmentation reactions using electrospray ionization mass spectrometry: an important tool for the structural elucidation and characterization of synthetic and natural products. Nat Prod Rep 2016; 33: 432-455
    CrossrefPubMedGoogle Scholar
  • 27 Clayton WA, Albert NW, Thrimawithana AH, McGhie TK, Deroles SC, Schwinn KE, Warren BA, McLachlan ARG, Bowman JL, Jordan BR, Davies KM. UVR8-mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants. Plant J 2018; 96: 503-517
    CrossrefPubMedGoogle Scholar
  • 28 Kim E, Kang M, Liu H, Cao C, Liu C, Bentley WE, Qu X, Payne GF. Pro- and anti-oxidant properties of redox-active catechol-chitosan films. Front Chem 2019; 7: 541-548
    CrossrefPubMedGoogle Scholar
  • 29 Karmakar R, Lee D. Total synthesis of selaginpulvilin C and D relying on in situ formation of arynes and their hydrogenation. Org Lett 2016; 18: 6105-6107
    CrossrefPubMedGoogle Scholar
  • 30 Chinta BS, Baire B. Formal total synthesis of selaginpulvilin D. Org Biomol Chem 2017; 15: 5908-5911
    CrossrefPubMedGoogle Scholar
  • 31 Sowden MJ, Sherburn MS. Four-step total synthesis of selaginpulvilin D. Org Lett 2017; 19: 636-637
    CrossrefPubMedGoogle Scholar
  • 32 Fujiwara K, Itagaki T, Kondo Y, Akiba U, Tokiwano T. Total synthesis of selaginellin S. Tetrahedron Lett 2020; 61: 152031
    CrossrefPubMedGoogle Scholar
  • 33 Wu B, Wang J. Phenolic compounds from Selaginella moellendorfii . Chem Biodivers 2011; 8: 1735-1747
    CrossrefPubMedGoogle Scholar
  • 34 Xu KP, Zou H, Tan Q, Li FS, Liu JF, Xiang HL, Zou ZX, Long HP, Li YJ, Tan GS. Selaginellins I and J, two new alkynyl phenols, from Selaginella tamariscina (Beauv.) Spring. J Asian Nat Prod Res 2011; 13: 93-96
    CrossrefPubMedGoogle Scholar
  • 35 Wang G, Yao S, Zhang XX, Song H. Rapid screening and structural characterization of antioxidants from the extract of Selaginella doederleinii hieron with DPPH-UPLC-Q-TOF/MS method. Int J Anal Chem 2015; 2015: 849769
    CrossrefPubMedGoogle Scholar
  • 36 Zhu B, Wang TB, Hou LJ, Lv HX, Liu AM, Zeng P, Li AH. A New selaginellin from Selaginella moellendorffii inhibits hepatitis B virus gene expression and replication. Chem Natl Compd 2016; 52: 624-627
    CrossrefPubMedGoogle Scholar
  • 37 Liu R, Zou H, Xu PS, Zou ZX, Li J, Cheng F, Liu RH, Zhou G, Xu KP, Tan GS. Uncinatic acids A–C, three new carboxylated flavonoids from Selaginella uncinata . Chin Chem Lett 2017; 28: 1465-1468
    CrossrefPubMedGoogle Scholar
  • 38 Yang C, Shao Y, Li K, Xia W. Bioactive selaginellins from Selaginella tamariscina (Beauv.) Spring. Beilstein J Org Chem 2012; 8: 1884-1889
    CrossrefPubMedGoogle Scholar
  • 39 Zou Z, Xu P, Wu C, Zhu W, Zhu G, He X, Zhang G, Hu J, Liu S, Zeng W, Xu K, Tan G. Carboxymethyl flavonoids and a chromone with antimicrobial activity from Selaginella moellendorffii Hieron. Fitoterapia 2016; 111: 124-129
    CrossrefPubMedGoogle Scholar
  • 40 Cheng XL, Ma SC, Yu JD, Yang SY, Xiao XY, Hu JY, Lu Y, Shaw PC, But PPH, Lin RC. Selaginellin A and B, two novel natural pigments isolated from Selaginella tamariscina . Chem Pharm Bull 2008; 56: 982-984
    CrossrefPubMedGoogle Scholar
  • 41 Pi JJ, Wu X, Rui W, Feng YF, Guo J. Identification and fragmentation mechanisms of two kinds of chemical compositions in Eucommia ulmoides by UPLC-ESI-Q-TOF-MS/MS. Chem Nat Compd 2016; 52: 144-148
    CrossrefPubMedGoogle Scholar
  • 42 Liu JF, Xu KP, Li FS, Shen J, Hu CP, Zou H, Yang F, Liu GR, Xiang HL, Zhou YJ, Li YJ, Tan GS. A new flavonoid from Selaginella tamariscina (Beauv.) Spring. Chem Pharm Bull 2010; 58: 549-551
    CrossrefPubMedGoogle Scholar
  • 43 Zou H, Xu KP, Li FS, Zou ZX, Liu R, Liu RH, Li J, Tan LH, Tan GS. Unciflavones A–F, six novel flavonoids from Selaginella uncinata (Desv.) Spring. Fitoterapia 2014; 99: 328-333
    CrossrefPubMedGoogle Scholar
  • 44 Yao H, Chen B, Zhang Y, Ou H, Li Y, Li S, Shi P, Lin X. Analysis of the Total Biflavonoids Extract from Selaginella doederleinii by HPLC-QTOF-MS and Its In Vitro and In Vivo Anticancer Effects. Molecules 2017; 22: 325-342
    CrossrefPubMedGoogle Scholar
  • 45 Nguyen PH, Ji DJ, Han YR, Choi JS, Rhyu DY, Min BS, Woo MH. Selaginellin and biflavonoids as protein tyrosine phosphatase 1B inhibitors from Selaginella tamariscina and their glucose uptake stimulatory effects. Bioorg Med Chem 2015; 23: 3730-3737
    CrossrefPubMedGoogle Scholar