Skip to main content
Log in

Light quality and explant type modulate growth, antioxidant properties and bioactive compounds production of calluses of Passiflora setacea cv BRS Pérola do Cerrado

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

Abstract

Passiflora species have high industrial and medicinal relevance, due to presence of specific metabolites and their recognized pharmacological activities. In vitro systems allow the modulation of secondary metabolites production according to culture conditions. In this work, we report the effect of different light emitting diodes (LED) on induction, metabolite production, and antioxidant properties of calluses derived from stem and leaf segments of P. setacea cv BRS Pérola do Cerrado. Friable calluses were induced on MSM medium supplemented with picloram, under different light qualities (white fluorescent lamps or different types of LEDs) or in the dark. Light quality contributed more significantly for biomass accumulation than the other variables. Callus formation was observed in response to all treatments, although the highest biomass accumulation was induced by red LED. Chromatographic analyses indicated that blue LED induced the highest production of bioactive substances. All samples displayed low antioxidant potential by the DPPH assay, but showed a high capacity to chelate iron. The activity of antioxidant enzymes was also evaluated. The incubation under red LED caused an increase on the activity of superoxide dismutase, catalase and ascorbate peroxidase in calluses derived from internodal segments induced under red LED. This is the first study evaluating the effect of lighting conditions in in vitro systems of P. setacea cv BRS Pérola do Cerrado, thus opening new possibilities of study and utilization.

Key message

Callus induction was affected by light quality, whereas bioactive compounds were modulated by the dedifferentiation process since flavonoids were detected in leaf tissues and fatty acids in calluses extracts.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Code availability

Not applicable.

References

  • Alves J, Marques J, Demarque D, Costa L, Amaral J, Lopes N, Silva-Júnior A, Soares L, Gavioli E, Ferreira L, Zucolotto S (2020) Involvement of isoorientin in the antidepressant bioactivity of a flavonoid-rich extract from Passiflora edulis f. flavicarpa Leaves. Rev Bras Farmacogn 30:1–11. https://doi.org/10.1007/s43450-020-00003-x

    Article  CAS  Google Scholar 

  • Antognoni F, Zheng S, Pagnucco C, Baraldi R, Poli F, Biondi S (2007) Induction of flavonoid production by UV-B radiation in Passiflora quadrangularis callus cultures. Fitoterapia 78:345–352

    Article  CAS  PubMed  Google Scholar 

  • Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292

    Article  CAS  Google Scholar 

  • Batista DS, Felipe SHS, Silva TD, Castro KM, Mamedes- Rodrigues TC, Miranda NA, Ríos-Ríos AM, Faria DV, Fortini EA, Chagas K, Torres-Silva G, Xavier A, Arenciba AD, Otoni WC (2018) Light quality in plant tissue culture: does it matter? In vitro Cell Dev Biol – Plant 54:195–215

    Article  CAS  Google Scholar 

  • Braga MF, Santos EC, Junqueira NTV, Sousa AATC, Faleiro FG, Rezende LN, Junqueira KP (2006) Cutting rooting of three wild Passiflora species. Rev Bras Frutic 28:284–288

    Article  Google Scholar 

  • Brazilian Pharmacopoeia (2019) Agência Nacional de Vigilância Sanitária, 6th edn. Ministério da Saúde, Brasília

    Google Scholar 

  • Carvalho MVO, Oliveira LL, Costa AM (2018) Effect of training system and climate conditions on phytochemicals of Passiflora setacea, a wild Passiflora from Brazilian savannah. Food Chem 266:350–358

    Article  PubMed  Google Scholar 

  • Chandran H, Meena M, Barupal T, Sharma K (2020) Plant tissue culture as a perpetual source for production of industrially important bioactive compounds. Biotechnology Reports 26:e00450. https://doi.org/10.1016/j.btre.2020.e00450

    Article  PubMed  PubMed Central  Google Scholar 

  • Chew YL, Goh JK, Lim YY (2009) Assessment of in vitro antioxidant capacity and polyphenolic composition of selected medicinal herbs from Leguminosae family in Peninsular Malaysia. Food Chem 116:13–18

    Article  CAS  Google Scholar 

  • Corrêa RCG, Peralta RM, Haminiuk CWI, Maciel GMM, Bracht A, Ferreira ICFR (2016) The past decade find ingrelated with nutricional composition, bioactive molecules and biotechnological applications of Passiflora spp. (passion fruit). Trend in Food Science Technology 58:79–95

    Article  Google Scholar 

  • Cotinguiba GG, Silva JRN, Azevedo RRS, Rocha TJM, Santos AF (2013) Methods of the antioxidant defense: A Literature Review. J Health Sci 15(3):231–237

    Google Scholar 

  • Dhawan K, Dhawan S, Sharma A (2004) Passiflora: a review update. J Ethno pharmacol 94:1–23

    Article  CAS  Google Scholar 

  • Faleiro FG, Junqueira NTV, Junghans TG, Jesus ON, Miranda D, Otoni WC (2019) Advances in passion fruit (Passiflora spp.) propagation. Rev Bras Frutic 41(2):e–e155

    Article  Google Scholar 

  • Farag MA, Otify A, Porzel A, Michel CG, Elsayed A, Wessjohann LA (2016) Comparative metabolite profiling and fingerprinting of genus Passiflora leaves using a multiplex approach of UPLC-MS and NMR analyzed by chemometric tools. Anal Bioanal Chem 408:3125–3143

    Article  CAS  PubMed  Google Scholar 

  • Fazal H, Abbasi BH, Ahmad N, Ali SS, Akbar F, Kanwal F (2016) Correlation of different spectral lights with biomass accumulation and production of antioxidant secondary metabolites in callus cultures of medicinally important Prunella vulgaris L. J Photochem Photobiol B Biol 159:1–7

    Article  CAS  Google Scholar 

  • Garcia R, Pacheco G, Falcão E, Borges G, Mansur E (2011) Influence of type of explant, plant growth regulators, salt composition of basal medium, and light on callogenesis and regeneration in Passiflora suberosa L. (Passifloraceae). Plant Cell Tiss Organ Cult 106:47–54

    Article  CAS  Google Scholar 

  • Garcia LC, Garcia R, Mansur E, Sutili F, Souza R, Mansur E, Leal I (2016) Optimized extraction of resveratrol from Arachis repens Handro by ultrasound and microwave: a correlation study with the antioxidant properties and phenol contents. Sci World J. https://doi.org/10.1155/2016/5890897

    Article  Google Scholar 

  • Gosmann G, Provensi G, Comunello LN, Rates SMK (2011) Composição química e aspectos farmacológicos de espécies de Passiflora L. (Passifloraceae). Brazilian Journal of Biosciences 9(1):88–99

    Google Scholar 

  • Gupta SD, Sahoo TK (2015) Light emitting diode (LED)-induced alteration of oxidative events during in vitro shoot organogenesis of Curculigo orchioides Gaertn. Acta Physiol Plant. https://doi.org/10.1007/s11738-015-1990-9

    Article  Google Scholar 

  • He X, Luan F, Yang Y, Wang Z, Zhao Z, Fang J, Wang M, Zuo M, Li Y (2020) Passiflora edulis: An insight into current researches on phytochemistry and pharmacology. Front Pharmacol 11:617. https://doi.org/10.3389/fphar.2020.00617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heo J-W, Kang D-H, Bang H-S, Hong S-G, Chun C-H, Kang K-K (2012) Early growth, pigmentation, protein content, and phenylalanine ammonia-lyase activity of red curled lettuces grown under different lighting conditions. Korean J Hortic Sci Technol 30:6–12

    Article  CAS  Google Scholar 

  • Hernández-Galicia E, Calzada F, Roman-Ramos R, Alarcón-Aguilar FJ (2007) Monoglycerides and fatty acids from Ibervillea sonorae root: Isolation and hypoglycemic activity. Planta Med 73:236–240

    Article  PubMed  Google Scholar 

  • Huan LVT, Tanaka M (2004) Effects of red and blue light-emitting diodes on callus induction, callus proliferation, and protocorm-like body formation from callus in Cymbidium orchid. Environ Control Biol 42:57–64

    Article  Google Scholar 

  • Huché-Thélier L, Crespel L, Le Gourrierec J, Morel P, Sakr S, Leduc N (2016) Light signaling and plant responses to blue and UV radiations—perspectives for applications in horticulture. Environ Exp Bot 121:22–38

    Article  Google Scholar 

  • Kapoor S, Raghuvanshi R, Bhardwaj P, Sood H, Saxena S, Chaurasia OP (2018) Influence of light quality on growth, secondary metabolites production and antioxidant activity in callus culture of Rhodiola imbricate Edgew. J Photochem Photobiol B 183:258–265

    Article  CAS  PubMed  Google Scholar 

  • Leal AEBP, Oliveira AP, Santos RF, Soares JMD, Lavor EM, Pontes MC, Lima JT, Santos ADC, Tomaz JC, Oliveira GG, Neto FC, Lopes NP, Rolim LA, Almeida JRGS (2020) Determination of phenolic compounds, in vitro antioxidant activity and characterization of secondary metabolites in different parts of Passiflora cincinnata by HPLC-DAD-MS/MS analysis. Nat Prod Res 34(7):995–1001

    Article  CAS  PubMed  Google Scholar 

  • Lopes RM, Sevilha AC, Faleiro F, Silva DB, Vieira RF, Agostini-Costa TS (2010) A comparative study of fatty acids profile of Passiflora seed from Brazilian savanna. Rev Bras Frutic 32:498–506. https://doi.org/10.1590/S0100-29452010005000065

    Article  Google Scholar 

  • Lugato D, Simão M, Garcia R, Mansur E, Pacheco G (2014) Determination of antioxidant activity and phenolic content of extracts from in vivo plants and in vitro materials of Passiflora alata Curtis. Plant Cell Tiss Organ Cult 118:339–346

    Article  CAS  Google Scholar 

  • Mamede AMGN, Soares AG, Oliveira EJ, Farah A (2017) Volatile composition of sweet passion fruit (Passiflora alata Curtis). J Chem. https://doi.org/10.1155/2017/3497216

    Article  Google Scholar 

  • Manivannan A, Soundararajan P, Halimah N, Ko CH, Jeong BR (2015) Blue LED light enhances growth, phytochemical contents, and antioxidant enzyme activities of Rehmannia glutinosa cultured in vitro. Hortic Environ Biotech 56(1):105–113

    Article  CAS  Google Scholar 

  • Mattos PRC, Gomes AS, Pereira SF (2015) Volatile compunds in passion fruit seed oil (Passiflora setacea BRS Pérola do Cerrado and Passiflora alata BRS Doce Mel). Chem Eng Trans 44:103–108

    Google Scholar 

  • Mikovski AI, Silva NT, Souza CS, Machado MD, Otoni WC, Carvalho IF, Rocha DI, Silva ML (2019) Tissue culture and biotechnological techniques applied to passion fruit with ornamental potential: an overview. Ornam Hortic 25:189–199. https://doi.org/10.14295/oh.v25i2.2036

    Article  Google Scholar 

  • Monteiro ABC, Higashi EN, Gonçalves NA, Rodriguez APM (2000) A novel approach for the definition of the inorganic medium components for micropropagation of yellow passion fruit (Passiflora edulis Sims. f. flavicarpa Deg.). In Vitro Cell Dev-Plant 36:527–531

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nadeem M, Abbasi BH, Younas M, Ahmad W, Zahir A, Hano C (2019) LED enhanced biosynthesis of biologically active ingredients in callus cultures of Ocimum basilicum. J Photochem Photobiol B 190:172–178

    Article  CAS  PubMed  Google Scholar 

  • Nhut DT, Nguyen H, Ngo T, Nguyen N, Vu L, Vu H, Tung H, Bui VTV, Tran L (2015) Light-emitting diodes and their potential in callus growth, plantlet development and saponin accumulation during somatic embryogenesis of Panax vietnamensis Ha et Grushv. Biotechnol Biotechnol Equip. 29:299–308. https://doi.org/10.1080/13102818.2014.1000210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otify A, George C, Elsayed A, Farag MA (2015) Mechanistic evidence of Passiflora edulis (Passifloraceae) anxiolytic activity in relation to its metabolite fingerprint as revealed via LC-MS and chemometrics. Food Function 6:3807–3817

    Article  CAS  PubMed  Google Scholar 

  • Ozarowski M, Thiem B (2013) Progress in micropropagation of Passiflora spp. to produce medicinal plants: a mini-review. Rev Bras Farmacogn 23:937–947

    Article  CAS  Google Scholar 

  • Ozarowski M, Piasecka A, Paszel-Jaworska A, Siqueira Chaves D, Romaniuk A, Rybczynska M, Gryszczyńska A, Sawikowska A, Kachlicki P, Mikolajczak P, Seremak-Mrozikiewicz A, Klejewski A, Thiem B (2018) Comparison of bioactive compounds content in leaf extracts of Passiflora incarnata, P. caerulea and P. alata and in vitro cytotoxic potential on leukemia cell lines. Braz J Pharmacogn 28:179–191

    Article  CAS  Google Scholar 

  • Patel SS, Mishra HSK, Singhai AK (2011) Recent updates on the genus Passiflora: a review. Res Phytochem Pharmacol 1:1–16

    CAS  Google Scholar 

  • Ramaiya SD, Lee HH, Xiao YJ, Shahbani NS, Zakaria MH, Bujang JS (2021) Organic cultivation practices enhanced antioxidant activities and secondary metabolites in giant granadilla (Passiflora quadrangularis L.). PLoS ONE 16(7):e0255059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rangel Junior IM, Vasconcellos MAS, Rosa RCC, Cruvinel FF (2018) Floral biology and physicochemical characterization of wild passion fruit Passiflora setacea D.C. BRS Pérola do Cerrado cultivated in the state of Rio de Janeiro. Rev Bras Frut 40(6):e041

    Article  Google Scholar 

  • Reische DW, Lillard DA, Eitenmiller RR (2002) Antioxidants. In: Akoh CC, Min DB (eds) Food lipids: chemistry, nutrition, and biotechnology. Marcel Dekker, New York, pp 507–534

    Google Scholar 

  • Rotta EM, Rodrigues CA, Jardim ICSF, Maldaner L, Visentainer JV (2019) Determination of phenolic compounds and antioxidant activity in passion fruit pulp (Passiflora spp.) using a modified QuEChERS method and UHPLC-MS/MS. LWT Food Sci. Technol. Int. 100:397–403. https://doi.org/10.1016/j.lwt.2018.10.052

    Article  CAS  Google Scholar 

  • Sahakyan NZH, Petrosyan MT, Popov YG, Volodin VV, Matistov NV, Gruzdev IV, Shirshova TI (2010) Content of Neutral Lipids and Fatty Acids in Callus Cultures and Leaves of Intact Plants of Ajuga genevensis and Ajuga Chia. Biotechnol Biotechnologic Eq. 24(sup1):87–90

    Article  Google Scholar 

  • Sánchez-Moreno C, Larrauri JA, Saura-Calixto FA (1998) Procedure to measure the antiradical efficiency of polyphenols. J Sci Food Agric 76:270–276

    Article  Google Scholar 

  • Saravanan S, Arunachalam K, Parimelazhagan T (2014) Antioxidant, analgesic, anti-inflammatory and antipyretic effects of polyphenols from Passiflora subpeltata leaves – A promising species of Passiflora. Ind Crops Prod 54:272–280

    Article  CAS  Google Scholar 

  • Sati A, Sati SC, Sati N, Sati OP (2017) Chemical composition and antimicrobial activity of fatty acid methyl ester of Quercus leucotrichophora fruits. Nat Prod Res. https://doi.org/10.1080/14786419.2016.1217202

    Article  PubMed  Google Scholar 

  • Shahidi F, Zhong Y (2015) Measurement of antioxidant activity. J Funct Foods 18:757–781. https://doi.org/10.1016/j.jff.2015.01.047

    Article  CAS  Google Scholar 

  • Shanmugam S, Gomes IA, Denadai M, Lima BS, Araújo AAS, Narain N, Neta MTAL, Serafini MR, Quitans-Júnior LJ, Thangaraj P (2018) UHPLC-QqQ-MS/MS identification, quantification of polyphenols from Passiflora subpeltata fruit pulp and determination of nutritional, antioxidant, α-amylase and α-glucosidase key enzymes inhibition properties. Food Res Int 108:611–620

    Article  CAS  PubMed  Google Scholar 

  • Shanmugam S, Murugaiyan I, Lima BS, Serafini MR, Araujo AAS, Narain N, Quintans-Júnior LJ, Thangaraj P (2019) HPLC–DAD–MS identification of polyphenols from Passiflora leschenaultii and determination of their antioxidant, analgesic, anti-inflammatory and antipyretic properties. Arabian J Chem 12:760–771

    Article  CAS  Google Scholar 

  • Simão MJ, Fonseca E, Garcia RO, Mansur E, Pacheco G (2016) Effects of auxins and different culture systems on the adventitious root development of Passiflora pohlii Mast. and their ability to produce antioxidant compounds. Plant Cell Tiss Organ Cult 124:419–430

    Article  Google Scholar 

  • Simão MJ, Barbosa TJS, Vianna MG, Garcia R, Mansur E, Ignacio ACPR, Pacheco G (2018) A comparative study of phytoconstituents and antibacterial activity of in vitro derived materials of four Passiflora species. Annals Acad Bras Cienc 90(3):2805–2813

    Article  Google Scholar 

  • Simirgiotis MJ, Schmeda-Hirschmann G, Bórquez J, Kennelly EJ (2013) The Passiflora tripartita (Banana Passion) Fruit: A Source of Bioactive Flavonoid C-Glycosides Isolated by HSCCC and Characterized by HPLC–DAD–ESI/MS/MS. Molecules 18(2):1672–1692. https://doi.org/10.3390/molecules18021672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smruthi R, Divya M, Archana K, Ravi M (2021) The active compounds of Passiflora spp and their potential medicinal uses from both in vitro and in vivo evidences. J Adv Biomed Pharm Sci 4:45–55

    Google Scholar 

  • Sozo JS, Cruz DC, Pavei AF, Pereira IMC, Wolfart M, Ramlov F, Montagner DF, Maraschin M, Viana AM (2016) In vitro culture and phytochemical analysis of Passiflora tenuifila Killip and Passiflora setacea DC (Passifloraceae). In: Jain S (ed) Protocols for in vitro cultures and secondary metabolite analysis of aromatic and medicinal plants, vol 1391, 2nd edn. Humana Press, New York, pp 13–30

    Google Scholar 

  • Tremmel M, Kiermaier J, Heilmann J (2021) Vitro metabolism of six C-glycosidic flavonoids from Passiflora incarnata L. Int J Mol Sci 22:6566. https://doi.org/10.3390/ijms22126566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viana ML, Costa AM, Celestino SMC (2016) Informations for the composition of nutritional table of the Passion fruit pulp BRS Pérola do Cerrado. Boletim de Pesquisa e Desenvolvimento – Embrapa Cerrados 335:17–18

  • Vianna MG, Garcia RO, Mansur E, Engelmann F, Pacheco G (2019) Oxidative stress during the cryopreservation of Passiflora suberosa L. shoot tips using the V-Cryo-plate technique: determination of the critical stages of the protocol. Plant Cell Tiss Organ Cult 139:369–379

    Article  CAS  Google Scholar 

  • Wang C, Xu F, Shang J, Xiao H, Fan W, DongF, Hu J, Zhou J (2013) Cycloartane triterpenoid saponins from water soluble of Passiflora edulis Sims and their antidepressant-like effects. J Ethnopharmacol 148:812–817

    Article  CAS  PubMed  Google Scholar 

  • Yu W, Liu Y, Song L, Jacobs DF, Du X, Ying Y, Shao Q, Wu J (2017) Effect of differential light quality on morphology, photosynthesis, and antioxidant enzyme activity in Camptotheca acuminata seedlings. J Plant Growth Regul 36:148–160

    Article  CAS  Google Scholar 

  • Zas P, John S (2017) Phytochemical investigation and antioxidant activities of Passiflora edulis (Passion fruit) leaves from Ukhrul district, Manipur, India. World J Pharm Res 6:793–801

    CAS  Google Scholar 

  • Zeraik ML, Pereira CAM, Zuin VG, Yariwake JH (2010) Maracujá: um alimento funcional? Revista Brasileira de Farmacognosia 20:459–471

    Article  CAS  Google Scholar 

  • Zhao J, Fujita K, Sakai K (2005) Oxidative stress in plant cell culture: a role in production of beta-thujaplicin by Cupresssus lusitanica suspension culture. Biotechnol Bioeng 90(5):62131. https://doi.org/10.1002/bit.20465

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) [Grant Number E-26/010.001840/2019], and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [Grant Number 310238/2018-8]. This study was also funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) [FinanceCode 001].

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Raphaela Santos-Tierno, Renata Garcia, Eduardo Fonseca, Fábio Faleiro and Davyson Moreira. Supervision: Georgia Pacheco and Elisabeth Mansur. The first draft of the manuscript was written by Raphaela Santos-Tierno and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Elisabeth Mansur.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Amita Bhattacharya.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos-Tierno, R., Garcia, R., Fonseca, E. et al. Light quality and explant type modulate growth, antioxidant properties and bioactive compounds production of calluses of Passiflora setacea cv BRS Pérola do Cerrado. Plant Cell Tiss Organ Cult 147, 635–646 (2021). https://doi.org/10.1007/s11240-021-02188-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-021-02188-y

Keywords

Navigation