Inhibition of mitochondrial complex I by the novel compound FSL0260 enhances high salinity-stress tolerance in Arabidopsis thaliana

Kaori Sako,Yasumitsu Kondoh,Takeshi Shimizu,Takeshi Nakano,Harumi Aono,Yushi Futamura,Hiroyuki Hirano,Maho Tanaka,Makoto Muroi,Ko Noguchi,Kaori Honda,Makoto Kawatani,Hiroyuki Osada,Motoaki Seki,Akihiro Matsui,Kenshirou Shimizu

doi:10.1038/s41598-020-65614-9

Abstract

Chemical priming is an attractive and promising approach to improve abiotic stress tolerance in a broad variety of plant species. We screened the RIKEN Natural Products Depository (NPDepo) chemical library and identified a novel compound, FSL0260, enhancing salinity-stress tolerance in Arabidopsis thaliana and rice. Through transcriptome analysis using A. thaliana seedlings, treatment of FSL0260 elevated an alternative respiration pathway in mitochondria that modulates accumulation of reactive oxygen species (ROS). From comparison analysis, we realized that the alternative respiration pathway was induced by treatment of known mitochondrial inhibitors. We confirmed that known inhibitors of mitochondrial complex I, such as rotenone and piericidin A, also enhanced salt-stress tolerance in Arabidopsis. We demonstrated that FSL0260 binds to complex I of the mitochondrial electron transport chain and inhibits its activity, suggesting that inhibition of mitochondrial complex I activates an alternative respiration pathway resulting in reduction of ROS accumulation and enhancement of tolerance to salinity in plants. Furthermore, FSL0260 preferentially inhibited plant mitochondrial complex I rather than a mammalian complex, implying that FSL0260 has a potential to be an agent for improving salt-stress tolerance in agriculture that is low toxicity to humans.

Highlights

Www.nature.com/scientificreports over-reduction of mETC and for mitigating reactive oxygen species (ROS) production[7]
Arabidopsis wild-type Columbia-0 (Col-0) seeds were grown in liquid culture medium containing each compound for 4 days, and plants were treated with 100 mM NaCl
We focused on 2-[[[(4-methylphenyl)sulfonyl]oxy]methyl]-2H-1-benzopyran-3-yl]methylpyridin-1-ium 4-methylbenzenesulfonate (1:1) (FSL0260) (Fig. 1a), because it showed the strongest tolerance to salinity stress

Summary

Introduction

Www.nature.com/scientificreports over-reduction of mETC and for mitigating ROS production[7]. In Arabidopsis, there are seven type II NDs (NDB1–4, NDA1–2 and NDC1) and five AOXs (AOX1a–d and AOX2) These alternative respiration pathway genes are induced at a gene, protein and activity level by a variety of stress conditions[10], suggesting that this pathway is important for stress response. We previously showed that histone deacetylase inhibitors and ethanol enhanced salinity-stress tolerance in plants including Arabidopsis, rice and cassava[12,13,14,15]. Those studies indicated that chemical compounds have the potential to improve tolerance in various agricultural crops. We demonstrated that FSL0260 works as an inhibitor of mitochondrial complex I and enhances an alternative respiration pathway, resulting in reduction of ROS accumulation and enhancement of salt-stress tolerance

Methods

Results

Conclusion