Skip to main content
SpringerLink
Log in

Anemia tomentosa var. anthriscifolia in vitro culture: sporophyte development and volatile compound profile of an aromatic fern

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Anemia tomentosa var. anthriscifolia is an aromatic fern with a pleasant woody aroma and antimycobacterial activity. In this paper, we describe for the first time its spore-derived gametophyte development and the effect of indole-3-acetic acid and jasmonic acid on in vitro gametophyte/sporophyte development, as well as volatile compound production. Volatiles were obtained by simultaneous distillation and extraction (SDE) and analyzed by high resolution gas chromatography coupled with mass spectrometry. Spore-derived gametophytes were able to develop into sporophytes independently of the media culture composition, even when no plant growth regulator was added. Fifty different substances were detected in all in vitro A. tomentosa SDE extracts, while 20 were detected in the wild SDE plant extract. Monoterpenes were more prevalent (69.8–89.8%) than sesquiterpenes (9.4–28.7%) in in vitro plants, while sesquiterpenes represent 97.5% of the volatiles produced by the wild-grown plants. The major monoterpene components in in vitro plants were α-pinene (9.3–24.3%), trans-pinocarveol (20.6–27.9%), pinocarvone (15.4–25.1%) and myrtenyl acetate (6.4–12.3%). The triquinane sesquiterpenes silphiperfol-6-ene (0.6–2.9%), α-guaiene (0.5–2.5%), β-barbatene (1.1–3.9%) and 9-epi-presilphiperfolan-1-ol (2.5–5.6%) represent the most abundant sesquiterpenes. The changes in the monoterpene/sesquiterpene rates between micropropagated and wild plants are not related to the presence of JA or IAA in the media culture. Further studies are still needed to obtain a complete understanding of the factors leading to these results, which could be related to differences in the irradiance levels of in vitro plants versus those from a wild environment, as well as the developmental stage of the plants. This is the first report of the use of plant growth regulators on Anemia tomentosa in vitro culture development and their effects on volatile profiles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

SDE:

Simultaneous distillation and extraction

HRGC-MS:

High resolution gas chromatography coupled with mass spectrometry

PGR:

Plant growth regulator

IAA:

Indole-3-acetic acid

JA:

Jasmonic acid

MS:

Murashige and Skoog (1962) medium

GC:

Gas chromatography

FID:

Flame ionization detector

LRI:

Linear retention indices

References

  • Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry, 4th edn. Allured Pub. Corp, Carol Stream

    Google Scholar 

  • Azam M, Jiang Q, Zhang B, Xu C, Chen K (2013) Citrus leaf volatiles as affected by developmental stage and genetic type. Int J Mol Sci 14:17744–17766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassolino L, Giacomelli E, Giovanelli S, Pistelli L, Cassetti A, Damonte G, Bisio A, Ruffoni B (2014) Tissue culture and aromatic profile in Salvia dolomitica Codd. Plant Cell Tissue Organ Cult 1–13

  • Bharati SK, Manabendra DT, Behari MP (2013) In vitro propagation in pteridophytes: a review. Int J Res Ayurveda Pharm 4:297–303

    Article  Google Scholar 

  • Camloh M, Ravnikar M, Zel J (1996) Jasmonic acid promotes division of fern protoplasts, elongation rhizoids and early development of gametophytes. Physiol Plant 97:659–664

    Article  CAS  Google Scholar 

  • Camloh M, Vilhar B, Zel J, Ravnlkar M (1999) Jasmonic acid stimulates development of rhizoids and shoots in fern leaf culture. J Plant Physiol 155:798–801

    Article  CAS  Google Scholar 

  • Chaintreau A (2001) Simultaneous distillation–extraction: from birth to maturity—review. Flavour Fragr J 16:136–148

    Article  CAS  Google Scholar 

  • Chang X, Alderson PG, Wright CJ (2008) Solar irradiance level alters the growth of basil (Ocimum basilicum L.) and its content of volatile oils. Environ Exp Bot 63:216–223

    Article  CAS  Google Scholar 

  • Das S, Choudhury MD, Mazumder PB (2013) In vitro propagation of Cyathea gigantea (Wall ex. Hook)—a tree fern. Int J Rec Scient Res 4:221–224

    Google Scholar 

  • De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2012.03.001

    PubMed  Google Scholar 

  • Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The non mevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102:933–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández H, Revilla MA (2003) In vitro culture of ornamental ferns. Plant Cell Tissue Organ Cult 73:1–13

    Article  Google Scholar 

  • Grausgruber-Gröger S, Schmiderer C, Steinborn R, Novak J (2012) Seasonal influence on gene expression of monoterpene synthases in Salvia officinalis (Lamiaceae). J Plant Physiol 169:353–359

    Article  PubMed  Google Scholar 

  • Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M, Bach TJ (2003) Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J Biol Chem 278:26666–26676

    Article  CAS  PubMed  Google Scholar 

  • Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog Lipid Res 51:95–148

    Article  CAS  PubMed  Google Scholar 

  • Hou G, Hill JP, Blancaflor EB (2004) Developmental anatomy and auxin response of lateral root formation in Ceratopteris richardii. J Exp Bot 55:685–693

    Article  CAS  PubMed  Google Scholar 

  • Juliani HR, Zygadlo JA, Scrivanti R, Sota E, Simon JE (2004) The essential oil of Anemia tomentosa (Savigny) Sw. var. anthriscifolia (Schard.) Mickel. ‎Flavour Fragr J 19:541–543

    Article  CAS  Google Scholar 

  • Kodym A, Lang M, Delpratt J (2016) Propagation by partial tissue culture of Austral Bracken (Pteridium esculentum) for revegetation. Ecol Manag Restor 17:159–163

    Article  Google Scholar 

  • Kosakivska IV, Babenko LM, Shcherbatiuk MM, Vedenicheva NP, Voytenko LV, Vasyuk VA (2016) Phytohormones during growth and development of Polypodiophyta. Adv Biol Earth Sci 1:26–44

    Google Scholar 

  • Kuriyama A, Kawai F, Kanamori M, Dathe W (1993) Inhibitory effect of jasmonic acid on gametophytic growth, initiation and development of sporophytic shoots in Equisetum arvense. J Plant Physiol 141:694–697. https://doi.org/10.1016/S0176-1617(11)81576-2

    Article  CAS  Google Scholar 

  • Makowski D, Tomiczak K, Rybczynski JJ, Mikuła A (2016) Integration of tissue culture and cryopreservation methods for propagation and conservation of the fern Osmunda regalis L. Acta Physiol Plant. https://doi.org/10.1007/s11738-015-2037-y

    Google Scholar 

  • Menéndez V, Arbesú R, Somer M (2010) From spore to sporophyte: how to proceed in vitro. In: Fernandéz H, Kumar A, Revilla A (eds) Working with ferns: issues and applications, 1st edn. Springer, New York, pp 97–110

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tabaco tissue cultures. ‎Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973. https://doi.org/10.1016/j.febslet.2010.05.045

    Article  CAS  PubMed  Google Scholar 

  • NIST/EPA/NIH mass spectral library (NIST8S and NIST08.LIB) and NIST MS Search/Analysis Program and data for Microsoft Windows. (2008) Version 8 and 8 s. Shimadzu

  • Pangesti N, Pineda A, Pieterse CM, Dicke M, van Loon JJ (2013) Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front Plant Sci 23:1–11. https://doi.org/10.3389/fpls.2013.00414

    Google Scholar 

  • Parajuli J, Joshi SD (2014) In vitro study of effects of growth hormones on sporophyte development of Cyathea spinulosa. Int J Biodivers Conserv 6:247–255. https://doi.org/10.5897/IJBC2014.0684

    Article  Google Scholar 

  • Parthier B (1996) Jasmonates: hormonal regulators or stress factors in leaf senescence? J Plant Growth Regul 9:57–63

    Article  Google Scholar 

  • Pinto SC, Leitão GG, Bizzo HR, Martinez N, Dellacassa E, Santos FM Jr, Costa FLP, de Amorim MB, Leitão SG (2009a) Epi-presilphiperfolan-1-ol, a new triquinane sesquiterpene from the essential oil of Anemia tomentosa var. anthriscifolia (Pteridophyta). Tetrahedron Lett 50:4785–4787

    Article  CAS  Google Scholar 

  • Pinto SC, Leitão GG, de Oliveira DR, Bizzo HR, Ramos DF, Coelho TS, Silva PE, Lourenço MC, Leitão SG (2009b) Chemical composition and antimycobacterial activity of the essential oil from Anemia tomentosa var. anthriscifolia. Nat Prod Commun 4:1675–1678

    CAS  PubMed  Google Scholar 

  • Pinto SC, Leitão GG, Castellar A, Bizzo HR, Leitão SG (2013) Chemical composition of the volatile fractions from wild and in vitro plants of Anemia tomentosa var. anthriscifolia (Pteridophyta). J Essent Oil Res 25:198–202

    Article  CAS  Google Scholar 

  • Praptosuwiryo TN (2017) Spore germination and early gametophyte development of Platycerium wandae (Polypodiaceae) from Papua, Indonesia. Biodiversitas 18:175–182. https://doi.org/10.13057/biodiv/d180124

    Article  Google Scholar 

  • Santos MG, Rocha LM, Carvalho ES, Kelecom A (2006) Isoafricanol, um sesquiterpeno incomum encontrado na Pteridófita Anemia tomentosa var. anthriscifolia. Rev Bras Plantas Med 8:71–75

    Google Scholar 

  • Schwartsburd PB, Labiak PH (2007) Pteridófitas do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Hoehnea 34:159–209

    Article  Google Scholar 

  • Sommer M, Arbesu R, Menendez V, Revilla MA, Fernandez H (2010) Sporophyte induction studies in ferns in vitro. Euphytica 171:203–210

    Article  Google Scholar 

  • van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64:251–263. https://doi.org/10.1007/s11103-007-9149-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnol Adv 32:31–39

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Xiu-Qun L, Hua J, Long-Qing C (2010) Effects of light, macronutrients, and sucrose on germination and development of the endangered fern Adiantum reniforme var. sinense (Adiantaceae). Sci Hortic 125:417–421

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Authors wish to thank Profs. Leandro Soter de Mariz e Miranda and Rodrigo Octavio Mendonça from Instituto de Química, UFRJ for the use of the GC–FID and GC–MS equipment, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for funding.

Author information

Authors and Affiliations

  1. Faculdade de Farmácia, Universidade Federal do Rio de Janeiro, Bloco A, 2o andar, Ilha do Fundão, Rio de Janeiro, RJ, 21941-902, Brazil

    Caroline Vianna Velasco Castilho, Suzana Guimarães Leitão, Carolina Santos Barreto & Nina Claudia Barboza da Silva

  2. Programa de Biotecnologia Vegetal, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Jaime Fidalgo Ferra Neto

  3. Curso de Farmácia, Laboratório de Produtos Bioativos, Universidade Federal do Rio de Janeiro, Campus Macaé, Macaé, RJ, Brazil

    Shaft Corrêa Pinto

Authors
  1. Caroline Vianna Velasco Castilho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaime Fidalgo Ferra Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suzana Guimarães Leitão
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carolina Santos Barreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shaft Corrêa Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nina Claudia Barboza da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JFFN, CVVC and CSB conducted the experiments; SCP and CVVC analyzed all chromatographic data, substance identification and assembled the supplementary data; SGL and NCBS conceived this work, analyzed the data and wrote the paper. All authors contributed in the writing of this paper.

Corresponding authors

Correspondence to Suzana Guimarães Leitão or Nina Claudia Barboza da Silva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Sergio J. Ochatt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 235 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castilho, C.V.V., Neto, J.F.F., Leitão, S.G. et al. Anemia tomentosa var. anthriscifolia in vitro culture: sporophyte development and volatile compound profile of an aromatic fern. Plant Cell Tiss Organ Cult 133, 311–323 (2018). https://doi.org/10.1007/s11240-018-1383-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-018-1383-z

Keywords

Search

Navigation