The use of chitosan oligosaccharide to improve artemisinin yield in well-watered and drought-stressed plants

Ana L García-García; Ana Rita Matos; Eduardo Feijão; Ricardo Cruz de Carvalho; Alicia Boto; Jorge Marques da Silva; David Jiménez-Arias

doi:10.3389/fpls.2023.1200898

The use of chitosan oligosaccharide to improve artemisinin yield in well-watered and drought-stressed plants

Front Plant Sci. 2023 Jun 2:14:1200898. doi: 10.3389/fpls.2023.1200898. eCollection 2023.

Authors

Ana L García-García^{1

2}, Ana Rita Matos^{3

4}, Eduardo Feijão⁵, Ricardo Cruz de Carvalho^{3

5

6}, Alicia Boto¹, Jorge Marques da Silva⁴, David Jiménez-Arias⁷

Affiliations

¹ Grupo Síntesis de Fármacos y Compuestos Bioactivos, Departamento de Química de Productos Naturales y Sintéticos Bioactivos, Instituto de Productos Naturales y Agrobiología, Consejo Superior de Investigaciones Científicas, San Cristóbal de La Laguna, Spain.
² Programa de Doctorado de Química e Ingeniería Química, Universidad de La Laguna, San Cristóbal de La Laguna, Spain.
³ Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal.
⁴ BioISI - Biosystems and Integrative Sciences Institute, Plant Functional Genomics Group, Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal.
⁵ MARE - Marine and Environmental Sciences Centre and ARNET - Aquatic Research Infrastructure Network Associate Laboratory, Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal.
⁶ Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal.
⁷ ISOPlexis-Center for Sustainable Agriculture and Food Technology, Madeira University, Funchal, Portugal.

Abstract

Introduction: Artemisinin is a secondary metabolite well-known for its use in the treatment of malaria. It also displays other antimicrobial activities which further increase its interest. At present, Artemisia annua is the sole commercial source of the substance, and its production is limited, leading to a global deficit in supply. Furthermore, the cultivation of A. annua is being threatened by climate change. Specifically, drought stress is a major concern for plant development and productivity, but, on the other hand, moderate stress levels can elicit the production of secondary metabolites, with a putative synergistic interaction with elicitors such as chitosan oligosaccharides (COS). Therefore, the development of strategies to increase yield has prompted much interest. With this aim, the effects on artemisinin production under drought stress and treatment with COS, as well as physiological changes in A. annua plants are presented in this study.

Methods: Plants were separated into two groups, well-watered (WW) and drought-stressed (DS) plants, and in each group, four concentrations of COS were applied (0, 50,100 and 200 mg•L-1). Afterwards, water stress was imposed by withholding irrigation for 9 days.

Results: Therefore, when A. annua was well watered, COS did not improve plant growth, and the upregulation of antioxidant enzymes hindered the production of artemisinin. On the other hand, during drought stress, COS treatment did not alleviate the decline in growth at any concentration tested. However, higher doses improved the water status since leaf water potential (YL) improved by 50.64% and relative water content (RWC) by 33.84% compared to DS plants without COS treatment. Moreover, the combination of COS and drought stress caused damage to the plant's antioxidant enzyme defence, particularly APX and GR, and reduced the amount of phenols and flavonoids. This resulted in increased ROS production and enhanced artemisinin content by 34.40% in DS plants treated with 200 mg•L-1 COS, compared to control plants.

Conclusion: These findings underscore the critical role of ROS in artemisinin biosynthesis and suggest that COS treatment may boost artemisinin yield in crop production, even under drought conditions.

Keywords: Artemisia annua; artemisinin; bioactive metabolites; chitosan oligosaccharide; drought; elicitation; stress.

Grants and funding

AG-G was recipient of a predoctoral contract from the Agencia Canaria de Investigación, Innovación y Sociedad de la Información (ACIISI) and European Social Found (ESF) (TESIS2019010072). The research was partially funded by INTERREG-MAC Project APOGEO (MAC2/1.1b/226) with FEDER funds and FCT-Foundation for Science and Technology through projects UIDB/04046/2020 and UIDP/04046/2020 of the Research Unit BioISI-Biosystems and Integrative Sciences Institute (Facultade de Ciências, Universidade de Lisboa).