Abstract
Tropical black sage (Varronia curassavica Jacq., Cordiaceae) is a species native to ecosystems subject to strong anthropic action, and thus is at risk of genetic erosion. However, little is known about this important genetic resource, with possible uses in the aromas, fragrances, and pharmaceutical sectors. The objective of this work was to prospect and study native specimens of tropical black sage regarding the content (%, w/w), chemical profile, and trypanocidal activity of the volatile oils. For this purpose, we collected in situ 47 specimens. The volatile oils were obtained by distillation from leaves, quantified, and analyzed by gas chromatography with flame ionization detection and gas chromatography coupled with mass spectrometry. The resulting data were submitted to descriptive statistical and multivariate analyses. The content of volatile oil ranged from 0.3 to 4.2% based on dry leaves. The volatile oils had average contents of 33.4 and 44.9% of oxygenated and non-oxygenated sesquiterpenes, respectively. The proportion of the compound α-humulene varied from 0.3 to 11.1%, with frequency of 100%. Cluster analysis indicated the formation of 10 groups with 50% similarity among the volatile oil samples. The sample with the best trypanocidal activity was ESB45, with IC50 of 74.6 µg/ml and 100% inhibition of the viability of the epimastigote form of Trypanosoma cruzi at the concentration of 300 µg/ml. Tropical black sage is a source of oxygenated sesquiterpenes, an important chemical class for synthesis and development of medicines. For this reason, efforts are necessary to preserve the genetic information about the species.
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Ache (2023) Acheflan. In: Aché Laboratórios Farm. S.A. https://www.ache.com.br/wp-content/uploads/application/pdf/Bula-Acheflan-Creme-2.pdf. Accessed 17 Apr 2023
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectroscopy, 4th edn. Allured Publishing Corporation, Carol Stream
Alves MS, Santos DP, Silva LCP, Pontes EG, Souza MAA (2015) Essential oils composition and toxicity tested by fumigation against Callosobruchus maculatus (Coleoptera: Bruchidae) pest of stored cowpea. Rev Virtual Quim 7:2387–2399. https://doi.org/10.5935/1984-6835.20150142
Alves MS, Silva LCP, Pereira EAD, Espósito EP, Fagundes LM, Faria TS, Santos AM, Chaves DSA, Castro RN, de Souza MAA (2019) Essential oils chemical diversity from UFRRJ Botanical Garden and other locations plants based on analysis of image and multivariate statistic. Rev Virtual Quim 11:1635–1656. https://doi.org/10.21577/1984-6835.20190115
Bakir B, Him A, Özbek H, Düz E, Tütüncü M (2008) Investigation of the anti-inflammatory and analgesic activities of β-caryophyllene. Int J Essent Oil Ther 2:41–44
Bristot SF, Colle MP, Della, Rossato AE, Citadini-Zanette V (2021) Uso medicinal de Varronia curassavica Jacq. Erva-baleeira (Boraginaceae): estudo de caso no Sul do Brasil/Medicinal use of Varronia curassavica Jacq. Erva-baleeira (Boraginaceae): case study in Southern Brazil. Brazilian J Anim Environ Res 4:170–182. https://doi.org/10.34188/bjaerv4n1-016
Calixto JB (2005) Twenty-five years of research on medicinal plants in Latin America. J Ethnopharmacol 100:131–134. https://doi.org/10.1016/j.jep.2005.06.004
Carvalho PM, Rodrigues RFO, Sawaya ACHF, Marques MOM, Shimizu MT (2004) Chemical composition and antimicrobial activity of the essential oil of Cordia Verbenacea D.C. J Ethnopharmacol 95:297–301. https://doi.org/10.1016/j.jep.2004.07.028
Carvalho VRA, Silva MKN, Aguiar JJS, Bitu V, de CN, Costa JGM, da, Ribeiro-Filho J, Coutinho HDM, Pinho AI, Fagner Ferreira Matias E (2017) Antibiotic-modifying activity and chemical profile of the essential oil from the leaves of Cordia Verbenacea DC. J Essent Oil Bear Plants 20:337–345. https://doi.org/10.1080/0972060X.2017.1301220
Carvalho Castro KN, Costa-Júnior LM, Lima DF, Canuto KM, Sousa De Brito E, De Andrade IM, Teodoro MS, Oiram-Filho F, Dos Santos RC, Mayo SJ (2019) Acaricidal activity of cashew nut shell liquid associated with essential oils from Cordia verbenacea and Psidium guajava on Rhipicephalus microplus. J Essent Oil Res 31:297–304. https://doi.org/10.1080/10412905.2019.1580225
Castro MJP, Baldin ELL, Cruz PL, Souza CM, Silva PHS (2013) Characterization of cowpea genotype resistance to Callosobruchus maculatus. Pesq Agropec Bras 48:1201–1209. https://doi.org/10.1590/S0100-204X2013000900003
Costa GM, Pereira JDS, Martins MLL, Aona LYS (2018) Florística em fitofisionomias de restinga na Bahia, nordeste do Brasil. Rev Biol Neotrop/J Neotrop Biol 15:78. https://doi.org/10.5216/rbn.v15i2.53845
Cunha TR, Borges RP, Seabra AA (2020) A urgência de monitorar remanescentes florestais em áreas urbanas situadas na restinga. Res Soc Dev 9:e11791210794. https://doi.org/10.33448/rsd-v9i12.10794
de Araújo Delmondes G, Bezerra DS, de Queiroz Dias D, de Souza Borges A, Araújo IM, Lins da Cunha G, Bandeira PFR, Barbosa R, Melo Coutinho HD, Felipe CFB, Barbosa-Filho JM, de Menezes IR, Kerntopf MR (2019) Toxicological and pharmacologic effects of farnesol (C15H26O): a descriptive systematic review. Food Chem Toxicol 129:169–200. https://doi.org/10.1016/j.fct.2019.04.037
de Castro Nizio DA, Fujimoto RY, Maria AN, Carneiro PCF, França CCS, da Costa Sousa N, de Andrade Brito F, Sampaio TS, Arrigoni-Blank Fátima M, Blank AF, Blank AF (2018) Essential oils of Varronia curassavica accessions have different activity against white spot disease in freshwater fish. Parasitol Res 117:97–105. https://doi.org/10.1007/s00436-017-5673-x
de Souza W, Rodrigues JCF (2009) Sterol biosynthesis pathway as target for anti-trypanosomatid drugs. Interdiscip Perspect Infect Dis 2009:642502. https://doi.org/10.1155/2009/642502
Dos Santos ADC, Pedroso Junior NN (2021) Mitigation and adaptation of cities to climate change: socio-environmental vulnerabilities and legal conflicts in the protection of urban Permanent Preservation Areas in Brazil/Mitigação e adaptação das cidades às alterações climáticas: vulnerabilidades socioambientais e conflitos jurídicos na tutela das Áreas urbanas de Preservação Permanente no Brasil. Rev Dir Da Cid 13:1720–1739. https://doi.org/10.12957/rdc.2021.61081
Dutra FL, Oliveira MM, Santos RS, Silva WS, Alviano DS, Vieira DP, Lopes AH (2016) Effects of linalool and eugenol on the survival of Leishmania (L.) infantum chagasi within macrophages. Acta Trop 164:69–76. https://doi.org/10.1016/j.actatropica.2016.08.026
El Toghlobi GSS, Arantes RA, Knudsen BG, Tabach R, Pereira MAA, Carvalho RG, Ferraz RRN, Rodrigues FSM (2022) Usos clínicos do fitoterápico da erva-baleeira (Varronia curassavica jacq.): revisão da literatura. Int J Heal Manag Rev 8. https://doi.org/10.37497/ijhmreview.v8i1.300
Fernandes ES, Passos GF, Medeiros R, da Cunha FM, Ferreira J, Campos MM, Pianowski LF, Calixto JB (2007) Anti-inflammatory effects of compounds alpha-humulene and (-)-trans-caryophyllene isolated from the essential oil of Cordia Verbenacea. Eur J Pharmacol 569:228–236. https://doi.org/10.1016/j.ejphar.2007.04.059
Gilbert B, Favoreto R (2012) Cordia Verbenacea DC Boraginaceae. Rev Fitos 7:17–25. https://doi.org/10.32712/2446-4775.2012.133
Gimenes L, Silva JCRL, Facanali R, Hantao LW, Siqueira WJ, Marques MOM (2021) Essential oils of new Lippia alba genotypes analyzed by flow-modulated comprehensive two-dimensional gas chromatography (GC×GC) and chemometric analysis. Molecules 26:2332. https://doi.org/10.3390/molecules26082332
Gonçalves CFL, de Freitas ML, Fortunato RS, Miranda-Alves L, Carvalho DP, Ferreira ACF (2018) Rutin scavenges reactive oxygen species, inactivates 5′-adenosine monophosphate-activated protein kinase, and increases sodium–iodide symporter expression in thyroid PCCL3 cells. Thyroid 28:265–275. https://doi.org/10.1089/thy.2016.0585
Hernández D, Orozco J, Serrano R, Duran A, Meraz S, Avila JG, Hernández T, Jimenez-Estrada M, García-Bores A (2014) Temporal variation of chemical composition and antimicrobial activity of the essential oil of Cordia curassavica (Jacq.) Roemer and Schultes: Boraginaceae. Bol Latinoam Caribe Plantas Med Aromat 13:100–108
Jannuzzi H, Mattos JKA, Vieira RF, Silva DB, Bizzo HR, Gracindo LA (2010) Avaliação agronômica e identificação de quimiotipos de erva cidreira no Distrito Federal. Hortic Bras 28:412–417. https://doi.org/10.1590/S0102-05362010000400006
Jannuzzi H, Mattos J, Silva DB, Gracindo LAM, Vieira RF (2011) Avaliação agronômica e química de dezessete acessos de erva-cidreira [Lippia alba (Mill.) N.E.Brown] - quimiotipo citral, cultivados no Distrito Federal. Rev Bras Plantas Med 13:258–264. https://doi.org/10.1590/S1516-05722011000300002
Kessler A, Kalske A (2018) Plant secondary metabolite diversity and species interactions. Annu Rev Ecol Evol Syst 49:115–138. https://doi.org/10.1146/annurev-ecolsys-110617-062406
Marques MCM, Swaine MD, Liebsch D (2011) Diversity distribution and floristic differentiation of the coastal lowland vegetation: implications for the conservation of the Brazilian Atlantic Forest. Biodivers Conserv 20:153–168. https://doi.org/10.1007/s10531-010-9952-4
Marques APS, Bonfim FPG, Dantas WFC, Puppi RJ, Marques MOM (2019) Chemical composition of essential oil from Varronia curassavica Jacq. Accessions in different seasons of the year. Ind Crops Prod 140:111656. https://doi.org/10.1016/j.indcrop.2019.111656
Morais MC, Souza JV, Dolabella C, Sousa SS (2020) Trypanocidal essential oils: a review. Molecules 25:4568. https://doi.org/10.3390/molecules25194568
Nascimento RV (2021) Estudo da espécie Varronia curassavica (Boraginaceae) em fragmentos da Mata Atlântica do Estado do Rio de Janeiro, com base no perfil químico dos óleos essenciais. https://sucupira.capes.gov.br/sucupira/public/consultas/coleta/trabalhoConclusao/viewTrabalhoConclusao.jsf?popup=true&id_trabalho=11810661#. Accessed 17 Apr 2023
NIST (2008) National Institute of Standards and Technology. Mass Spectral Library (NIST/EPA/NIH). https://www.nist.gov/programs-projects/electron-ionization-library-component-nistepanih-mass-spectral-library-and-nist-gc. Accessed 17 Apr 2023
Nizio DAC, Brito FA, Sampaio TS, Melo JO, Silva FLS, Gagliardi PR, Arrigoni-Blank MF, Anjos CS, Alves PB, Wisniewski Junior A, Blank AF (2015) Chemical diversity of native populations of Varronia curassavica Jacq. And antifungal activity against Lasiodoplodia theobromae. Ind Crops Prod 76:437–448. https://doi.org/10.1016/j.indcrop.2015.07.026
Nizio DAC, Blank AF, Sampaio TS, Brito FA, Andrade TM, Arrigoni- Blank MF, Maria AN (2018) Distillation methods affect the chemical composition of Varronia curassavica Jacq. Essential oil? Biosci J 34:629–639. https://doi.org/10.14393/BJ-v34n3a2018-39372
Oliveira BMS, Melo CR, Santos ACC, Nascimento LFA, Nízio DAC, Cristaldo PF, Blank AF, Bacci L (2019) Essential oils from Varronia curassavica (Cordiaceae) accessions and their compounds (E)-caryophyllene and α-humulene as an alternative to control Dorymyrmex Thoracius (Formicidae: Dolichoderinae). Environ Sci Pollut Res 26:6602–6612. https://doi.org/10.1007/s11356-018-4044-1
Oliveira BMS, Blank AF, Nizio DADC, Nogueira PCDL, Arrigoni-Blank MDF, Bacci L, Melo CR, Nascimento LFDA, Sampaio TS (2020) Chemical analyses of the essential oils from Varronia curassavica accessions in two seasons. J Essent Oil Res 32:494–511. https://doi.org/10.1080/10412905.2020.1789001
Pereira PS, Oliveira CVB, Maia AJ, Tintino SR, Oliveira-Tintino CDM, Vega-Gomez MC, Rolón M, Coronel C, Duarte AE, Barros LM, Kamdem JP, Siyadatpanah A, Wilairatana P, Coutinho HDM (2021) Cytotoxicity of essential oil Cordia verbenaceae against Leishmania brasiliensis and Trypanosoma Cruzi. Molecules 26:4485. https://doi.org/10.3390/molecules26154485
Petrén H, Köllner TG, Junker RR (2023) Quantifying chemodiversity considering biochemical and structural properties of compounds with the R package. New Phytol 237:2478–2492. https://doi.org/10.1111/nph.18685
Pinheiro LS, Andrade-Neto VV, Mantuano-Barradas M, Pereira EC, Barbosa RCF, de Oliveira MCC, Menna-Barreto RFS, Cunha-Júnior EF, Torres-Santos EC (2023) Biological effects of trans, trans-farnesol in Leishmania amazonensis. Front Cell Infect Microbiol 13:1221246. https://doi.org/10.3389/fcimb.2023.1221246
Polatoglu K (2013) Chemotypes– A fact that should not be ignored in natural product studies. Nat Prod J 3:10–14. https://doi.org/10.2174/2210315511303010004
Queiroz TB, Mendes ADR, Silva JCRL, Fonseca FSA, Martins ER (2016) Teor E composição química do óleo essencial de erva-baleeira (Varronia curassavica Jaqc.) Em função dos horários de coleta. Rev Bras Plantas Med 18:356–362. https://doi.org/10.1590/1983-084X/15_116
Queiroz TB, Fonseca FSA, Mendes ADR, Azevedo AM, Martins ER (2019) Chemical diversity of accessions of the in vivo germplasm bank of Varronia curassavica (Jacq.). Acta Sci Agron 42:e42726. https://doi.org/10.4025/actasciagron.v42i1.42726
Ramos YJ, Gouvêa-Silva JG, de Brito Machado D, Felisberto JS, Pereira RC, Sadgrove NJ, de Lima MD (2022) Chemophenetic and chemodiversity approaches: new insights on modern study of plant secondary metabolite diversity at different spatiotemporal and organizational scales. Rev Bras Farmacogn 33:49–72. https://doi.org/10.1007/s43450-022-00327-w
Reis DB (2017) Síntese, caracterização e avaliação biológica de terpenóides diaminados e seus derivados análogos ao SQ109. Universidade Federal de Itajubá. https://repositorio.unifei.edu.br/xmlui/handle/123456789/680. Accessed 17 Apr 2023
Ribeiro MC, Martensen AC, Metzger JP, Tabarelli M, Scarano F, Fortin M-J (2011) The Brazilian atlantic forest: a shrinking biodiversity hotspot. In: Zachos F, Habel J (eds) Biodiversity hotspots. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 405–434. https://doi.org/10.1007/978-3-642-20992-5_21
Santos AV, ADefaveri AC, Bizzo HR, San Gil RAS, Sato A (2013) In vitro propagation, histochemistry, and analysis of essential oil from conventionally propagated and in vitro-propagated plants of Varronia curassavica Jacq. Vitr Cell Dev Biol Plant 49:405–413. https://doi.org/10.1007/s11627-013-9528-6
Saúde-Guimarães DA, Faria AR (2007) Substâncias Da Natureza com atividade anti-Trypanosoma cruzi. Rev Bras Farmacogn 17:455–465. https://doi.org/10.1590/S0102-695X2007000300021
Sciarrone D, Giuffrida D, Rotondo A, Micalizzi G, Zoccali M, Pantò S, Donato P, Rodrigues-das-Dores RG, Mondello L (2017) Quali-quantitative characterization of the volatile constituents in Cordia Verbenacea D.C. essential oil exploiting advanced chromatographic approaches and nuclear magnetic resonance analysis. J Chromatogr A 1524:246–253. https://doi.org/10.1016/j.chroma.2017.10.007
Sharma H, Sehgal R, Jhacak S, Deshmukh K, Nada R (2023) Evaluation of farnesol orally and topically against experimental cutaneous leishmaniasis: in-vivo analysis. PLoS ONE 18:e0290297. https://doi.org/10.1371/journal.pone.0290297
Silva AC, de Souza PE, de Resende MLV, da Silva MB, Ribeiro PM, Zeviani WM (2014) Local and systemic control of powdery mildew in eucalyptus using essential oils and decoctions from traditional Brazilian medicinal plants. Pathol 44:145–153. https://doi.org/10.1111/efp.12079
Singh AK, Raina VK, Naqvi AA, Patra NK, Kumar B, Ram P, Khanuja SPS (2005) Essential oil composition and chemoarrays of menthol mint (Mentha arvensis L. f. piperascens Malinvaud ex. Holmes) cultivars. Flavour Fragr J 20:302–305. https://doi.org/10.1002/ffj.1417
Soares CHN, Damasceno PC, Campos IM, Amorim GTS, Carmo MGF, Chaves DSA, Souza MAA (2019) Selection of genotypes (citral chemotype) of Lippia alba (Mill.) N. E. Brown regarding seasonal stability of the essential oils chemical profile. Ind Crops Prod 139:111497. https://doi.org/10.1016/j.indcrop.2019.111497
Sokal RR, Rohlf FJ (1962) The comparison of dendrograms by objective methods. Taxon 11:33–40. https://doi.org/10.2307/1217208
Thon FM, Müller C, Wittmann MJ (2024) The evolution of chemodiversity in plants—from verbal to quantitative models. Ecol Lett 27:e14365. https://doi.org/10.1111/ele.14365
Trindade H, Pedro LG, Figueiredo AC, Barroso JG (2018) Chemotypes and terpene synthase genes in Thymus genus: state of the art. Ind Crops Prod 124:530–547. https://doi.org/10.1016/j.indcrop.2018.08.021
Zappi DC, Filardi FLR, Leitman P, Souza VC, Walter BMT, Pirani JR, Morim MP, Queiroz LP, Cavalcanti TB, Mansano VF, Forzza RC, Abreu MC, Acevedo-Rodríguez P, Agra MF, Almeida EB Jr, Almeida GSS et al (2015) Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085–1113. https://doi.org/10.1590/2175-7860201566411
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We gratefully acknowledge support from Professor Rosane Nora Castro (IQ-UFRRJ), the Postgraduate Program in Chemistry (PPFQ-IQ-UFRRJ), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
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This study was financed in part by Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ Codes: E-26/211374/2021 and E-26/211.547/2021) and by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES Code 001).
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EADPM, RVN: conceptualization, formal analysis, supervision, writing of the original draft; EBDJ, CSBP, YNM, ASMMV: investigation, formal analysis; DD-R, MEFL, AMS, PCD-Jr, MAAS: supervision; AMS, PCD-Jr, MAAS: funding acquisition, writing, review, and editing; MAAS: conceptualization, project administration, funding acquisition, writing, review, and editing.
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de Medeiros, E.A.D.P., Nascimento, R.V., Duarte Junior, E.B. et al. Chemodiversity and Trypanocidal Activity of the Volatile Oils of Tropical Black Sage. Rev. Bras. Farmacogn. (2024). https://doi.org/10.1007/s43450-024-00562-3
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DOI: https://doi.org/10.1007/s43450-024-00562-3