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Fungal elicitor-mediated enhancement in phenylpropanoid and naphtodianthrone contents of Hypericum perforatum L. cell cultures

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Abstract

Hypericum perforatum cell suspensions were evaluated for their growth, phenylpropanoid and naphtodianthrone productions, and antioxidant activity after treatments with fungal elicitors Fusarium oxysporum, Phoma exigua and Botrytis cinerea. Elicited cells displayed a reduced biomass production, a rapid stimulation of secondary metabolites production and a modification of cell redox state compared to control. Cells responded strongly towards the applied elicitors through the enhanced production of naphtodianthrones. Hypericin and pseudohypericin production was significantly increased (up to fourfold) in the early growth phase and remained stable all along the post-elicitation period. Significant increase in contents of total phenolics, total flavonoids and total anthocyanins was observed during the entire period of cultivation, while total flavanols were enhanced at the end of post-elicitation. The enzymatic activities of phenylalanine ammonia lyase and chalcone isomerase were remarkably elevated in elicited cells confirming a strong activation of phenylpropanoid/flavonoid pathways. The fingerprint profile of Fourier transform infrared spectroscopy spectra from the cell walls showed a little variation in lignin accumulation between elicited and control samples. With regards to the antioxidant state, an early up-regulation of peroxidase activity was observed in elicited cells, whereas non-enzymatic properties and catalase activity were enhanced at the end of post-elicitation. These findings suggest the involvement of an efficient antioxidant defense system in the adaptive response of cells to fungal elicitation. Altogether, these results indicated that H. perforatum elicited cells represent a promising experimental system for scale-up production of naphtodianthrones for medicinal uses.

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Abbreviations

CAT:

Catalase

CHI:

Chalcone isomerase

FTIR:

Fourier transform infrared spectroscopy

HYP:

Hypericin

JA:

Jasmonic acid

NEAOP:

Non-enzymatic antioxidant properties

PAL:

Phenylalanine ammonia lyase

PHYP:

Pseudohypericin

POD:

Peroxidase

ROS:

Reactive oxygen species

SA:

Salicylic acid

TA:

Total anthocyanins

TFL:

Total flavanols

TF:

Total flavonoids

TP:

Total phenolics

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Acknowledgments

This work and a Ph.D. grant (Sonja Gadzovska) was supported by the Ministère des Affaires Etrangères (Programme COCOP: Réseau d’Enseignement régional Postgraduate en Biologie, Grant No. DSUR-NGE-4B1-505). We thank Dr S. Ounnnar, S. Pochon, G. Moreau for their technical help. We acknowledge Dr F. Brignolas for his help in statistical analyses.

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Authors and Affiliations

  1. Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC) INRA USC1328, ITP SBCV, UPRES EA 1207, University of Orléans, rue de Chartres, BP6759, 45067, Orléans Cedex 2, France

    Sonja Gadzovska Simic, Stéphane Maury, Alain Delaunay & Claude Joseph

  2. Laboratory for Plant Cell and Tissue Culture, Faculty of Natural Sciences and Mathematics, Institute of Biology, University “Ss. Cyril and Methodius”, Archimedova str. 3, 1000, Skopje, Macedonia

    Sonja Gadzovska Simic & Oliver Tusevski

  3. Laboratory of Wood and Crop Biology, Antenne Scientifique Universitaire de Chartres (ASUC), Université d’Orléans, 21 rue de Loigny la Bataille, 28000, Chartres, France

    Christophe Hano, Frédéric Lamblin, Eric Lainé & Daniel Hagège

  4. INRA Parois Végétales et Matériaux Fibreux UMR FARE, 2 esplanade Roland Garros, BP224, 51686, Reims, France

    Brigitte Chabbert

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  1. Sonja Gadzovska Simic
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Correspondence to Sonja Gadzovska Simic.

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Gadzovska Simic, S., Tusevski, O., Maury, S. et al. Fungal elicitor-mediated enhancement in phenylpropanoid and naphtodianthrone contents of Hypericum perforatum L. cell cultures. Plant Cell Tiss Organ Cult 122, 213–226 (2015). https://doi.org/10.1007/s11240-015-0762-y

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