Elsevier

Redox Biology

Volume 16, June 2018, Pages 388-400
Redox Biology

Research paper
SA inhibits complex III activity to generate reactive oxygen species and thereby induces GA overproduction in Ganoderma lucidum

https://doi.org/10.1016/j.redox.2018.03.018Get rights and content
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Highlights

  • Mitochondria as a source of salicylic acid (SA) induced reactive oxygen species (ROS) production in Ganoderma lucidum.

  • SA induces the accumulation of ganoderic acids in Ganoderma lucidum by mitochondria ROS overproduction.

  • SA inhibits mitochondrial complex III activity to increase ROS and thereby induces ganoderic acids biosynthesis.

Abstract

Ganoderma lucidum has high commercial value because it produces many active compounds, such as ganoderic acids (GAs). Salicylic acid (SA) was previously reported to induce the biosynthesis of GA in G. lucidum. In this study, we found that SA induces GA biosynthesis by increasing ROS production, and further research found that NADPH oxidase-silenced strains exhibited a partial reduction in the response to SA, resulting in the induction of increased ROS production. Furthermore, the localization of ROS shows that mitochondria are sources of ROS production in response to SA treatment. An additional analysis focused on the relationship between SA-induced ROS production and mitochondrial functions, and the results showed that inhibitors of mitochondrial complexes I and II exert approximately 40–50% superimposed inhibitory effects on the respiration rate and H2O2 content when co-administered with SA. However, no obvious superimposed inhibition effects were observed in the sample co-treated with mitochondrial complex III inhibitor and SA, implying that the inhibitor of mitochondrial complex III and SA might act on the same site in mitochondria. Additional experiments revealed that complex III activity was decreased 51%, 62% and 75% after treatment with 100, 200, and 400 µM SA, respectively. Our results highlight the finding that SA inhibits mitochondrial complex III activity to increase ROS generation. In addition, inhibition of mitochondrial complex III caused ROS accumulation, which plays an essential role in SA-mediated GA biosynthesis in G. lucidum. This conclusion was also demonstrated in complex III-silenced strains. To the best of our knowledge, this study provides the first demonstration that SA inhibits complex III activity to increase the ROS levels and thereby regulate secondary metabolite biosynthesis.

Keywords

Salicylic acid
Reactive oxygen species
Mitochondrial complex III
Ganoderic acids

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These authors contributed equally to this work.