Impact of cytotoxic plant naphthoquinones, juglone, plumbagin, lawsone and 2-methoxy-1,4-naphthoquinone, on Chlamydomonas reinhardtii reveals the biochemical mechanism of juglone toxicity by rapid depletion of plastoquinol

Hydrophilic, untethered 1,4-naphthoquinones (1,4-NQs) are plant secondary metabolites that are often excreted into the environment and play a role in various plant-microbial, plant-fungal, plant-insect and plant-plant interactions. The biological activity of 1,4-NQs is mainly related to their redox properties, i.e. the ability to undergo redox cycling in cells. These compounds may also undergo electrophilic addition to thiol-containing compounds. The aim of this study was to compare the impact of juglone, plumbagin, lawsone and 2-methoxy1,4-naphthoquinone (2-met-NQ) on the antioxidant response of the green microalga Chlamydomonas reinhardtii. The algae were incubated with the examined compounds under low light for 6 h and the content of photosynthetic pigments, prenyllipid antioxidants, ascorbate, soluble thiols, proline, and superoxide dismutase activity was assessed. To examine the interaction between photosynthetic activity and naphthoquinone toxicity, we carried out the second experiment, in which C. reinhardtii was incubated with 1,4-NQs for 1 h under high light or in darkness. The pro-oxidant action of the examined 1,4-NQs depended on their reduction potentials, which decrease in order: juglone > plumbagin > 2-met-NQ > lawsone. Lawsone did not display pro-oxidant properties. Exposure to high light strongly enhanced the pro-oxidant effect of juglone, plumbagin, and 2-met-NQ, which is thought to result from the interception of the electrons from photosynthetic electron transfer chain. Only juglone was able to cause a fast depletion of plastoquinol, which may be an important mode of action of this allelochemical, responsible for its high toxicity to plants.

Automated summary

In this study, the impact of different 1,4-naphthoquinone compounds on the antioxidant response of green algae was compared. The results showed that the redox properties and reduction potentials of these compounds influenced their pro-oxidant effects. High light intensity further enhanced the pro-oxidant effect of some compounds. These findings provide insights into the toxic mechanisms of these compounds on plants.