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Artemisia annua L. and photoresponse: from artemisinin accumulation, volatile profile and anatomical modifications to gene expression

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Abstract

Key message

Blue and yellow light affected metabolism and the morphology. Blue and red promote the DOXP/MEP pathway. ADS gene expression was increased in plants cultivated under blue, promoting artemisinin content.

Abstract

Artemisinin-based combination therapies are the most effective treatment for highly lethal malaria. Artemisinin is produced in small quantities in the glandular trichomes of Artemisia annua L. Our aim was to evaluate the effect of light quality in A. annua cultivated in vitro under different light qualities, considering anatomical and morphological changes, the volatile composition, artemisinin content and the expression of two key enzymes for artemisinin biosynthesis. Yellow light is related to the increase in the number of glandular trichomes and this seemed to positively affect the molecular diversity in A. annua. Yellow light-stimulated glandular trichome frequency without triggered area enhancement, whereas blue light stimulated both parameters. Blue light enhanced the thickness of the leaf epidermis. The B-promoting effect was due to increased cell size and not to increased cell numbers. Green and yellow light positively influenced the volatile diversity in the plantlets. Nevertheless, blue and red light seemed to promote the DOXP/MEP pathway, while red light stimulates MVA pathway. Amorpha-4,11-diene synthase gene expression was significantly increased in plants cultivated under blue light, and not red light, promoting artemisinin content. Our results showed that light quality, more specifically blue and yellow light, positively affected secondary metabolism and the morphology of plantlets. It seemed that steps prior to the last one in the artemisinin biosynthesis pathway could be strongly influenced by blue light. Our work provides an alternative method to increase the amount of artemisinin production in A. annua without the use of transgenic plants, by the employment of blue light.

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Data availability statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

ACT:

Artemisinin combination therapies

ADS:

Amorpha-4,11-diene synthase

B:

Monochromatic blue light

CRY:

Cryptochrome

CYP71AV1:

Cytochrome P450 monooxygenase

D:

Darkness

dNTPs:

Deoxyribonucleoside 5′-triphosphate

DOXP/MEP:

2Cmethyl-d-erythritol-4-phosphate pathway

DTT:

Dithiothreitol

FAA:

37% formaldehyde, glacial acetic acid, and 70% ethanol solution

G:

Monochromatic green light

Gl.T:

Glandular trichomes

LED:

Light-emitting diode

LRI:

Linear retention indices

MS:

Murashige and Skoog

MVA:

Mevalonic acid pathway

NIST:

National Institute of Standards and Technology

PAR:

Photosynthetically active radiation

PDMS:

Polydimethylsiloxane

PHOT:

Phototropin

P.P:

Palisade parenchyma

R:

Monochromatic red light

SEM:

Scanning electron microscopy

S.P:

Spongy parenchyma

TT:

T-shape trichome

W:

White fluorescent light

Y:

Monochromatic yellow light

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Acknowledgements

We thank Prof. Pedro Melillo (CPQBA/UNICAMP) for providing the seeds and Durvalina Felix-Whipps and Rosângela de Almeida Epifanio (in memoriam) for technical and scientific support.

Funding

This work was supported by Foundation for Research Support of the State of Rio de Janeiro (FAPERJ) [E-26/111.372/2011]; National Council for Scientific and Technological Development (CNPq) [Grant numbers 310474/2015-9, 159779/2013-8]; Coordination of Improvement of Higher Education Personnel (CAPES); and Federal University of Rio de Janeiro State (UNIRIO).

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Author notes

  1. Arthur L. Macedo

    Present address: Post-Graduate Program in Pharmacy, Laboratory of Natural Products and Mass Spectrometry (LaPNEM), Faculty of Pharmaceutical Sciences, Food and Nutrition, Federal University of Mato Grosso do Sul (UFMS), Campo Grande, MS, Brazil

Authors and Affiliations

  1. Integrated Laboratory of Plant Biology (LIBV), Institute of Biosciences, Department of Botany, Federal University of Rio de Janeiro State (UNIRIO), Avenida Pasteur nº 458, 5th Floor, Room 512, Rio de Janeiro, RJ, CEP: 22290-240, Brazil

    Ellen M. Lopes & Andrea F. Macedo

  2. Laboratory of Plant Molecular Genetics (LGMV), Institute of Biology, Department of Genetics, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, RJ, Brazil

    Fábia Guimarães-Dias & Marcio Alves-Ferreira

  3. Laboratory of Plant Anatomy (LAV), Institute of Biosciences, Department of Botany, University of São Paulo (USP), São Paulo, SP, Brazil

    Thália do S. S. Gama

  4. Laboratory of Natural Products (LaProMar), Institute of Chemistry, Fluminense Federal University (UFF), Niterói, RJ, Brazil

    Arthur L. Macedo & Alessandra L. Valverde

  5. Laboratory of Chromatography and Screening Strategies, Institute of Chemistry, Fluminense Federal University (UFF), Niterói, RJ, Brazil

    Marcela C. de Moraes

  6. Laboratory of Plant Anatomy (LAV), Institute of Biosciences, Department of Botany, Federal University of Rio de Janeiro State (UNIRIO), Rio de Janeiro, RJ, Brazil

    Ana Cristina A. de Aguiar-Dias

  7. Brazilian Agricultural Research Corporation (Embrapa), Food Agroindustry, Rio de Janeiro, RJ, Brazil

    Humberto R. Bizzo

  8. Laboratory of Plant Anatomy, Institute of Biology, Department of Botany, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, RJ, Brazil

    Eliana S. Tavares

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  1. Ellen M. Lopes
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  11. Andrea F. Macedo
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Contributions

AFM supervised the project; AFM, EST, MA-F, HRB, ACAA-D and ALV designed the experiments; EML, EST and AFM wrote the manuscript, with the participation of FG-D, ALM and contributions from all authors; tissue culture experiments were conducted by EML and AFM; morphological assays were conducted by AFM, EST, TSSG and ACAA-D; volatile assays were advised by HRB and conducted by EML and AFM; artemisinin analysis was conducted by ALM under the supervision of ALV and MCM; gene expression assays were conducted by EML and FG-D under the supervision of MA-F. All authors critically revised the manuscript and gave their final approval.

Corresponding author

Correspondence to Andrea F. Macedo.

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Lopes, E.M., Guimarães-Dias, F., Gama, T.d.S.S. et al. Artemisia annua L. and photoresponse: from artemisinin accumulation, volatile profile and anatomical modifications to gene expression. Plant Cell Rep 39, 101–117 (2020). https://doi.org/10.1007/s00299-019-02476-0

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