Ferroptosis induced by the biocontrol agent Pythium oligandrum enhances soybean resistance to Phytophthora sojae

Ferroptosis is a newly discovered form of cell death accompanied by iron accumulation and lipid peroxidation. Both biotic and abiotic stresses can induce ferroptosis in plant cells. In the case of plant interactions with pathogenic Phytophthora oomycetes, the roles of ferroptosis are still largely u...

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Published in:Environmental microbiology 2022-12, Vol.24 (12), p.6267-6278
Main Authors: Cheng, Yang, Zhang, Huanxin, Zhu, Wenyi, Li, Qing, Meng, Rui, Yang, Kun, Guo, Ziqian, Zhai, Ying, Zhang, Haijing, Ji, Rui, Peng, Hao, Dou, Daolong, Jing, Maofeng
Format: Article
Language:English
Subjects:
Accumulation
Apoptosis
Biological control
Cell death
Defence mechanisms
Disease Resistance - genetics
Ferric ions
Ferroptosis
Gene expression
Glutathione
Glycine max - genetics
Infections
Lipid peroxidation
Lipids
Pathogens
Peroxidation
Phytophthora
Phytophthora sojae
Plant cells
Plant Diseases - genetics
Plant Diseases - prevention & control
Plant resistance
Plants
Pythium
Pythium oligandrum
Reactive oxygen species
Soybeans
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Summary:Ferroptosis is a newly discovered form of cell death accompanied by iron accumulation and lipid peroxidation. Both biotic and abiotic stresses can induce ferroptosis in plant cells. In the case of plant interactions with pathogenic Phytophthora oomycetes, the roles of ferroptosis are still largely unknown. Here, we performed transcriptome analysis on soybean plants treated with the biocontrol agent Pythium oligandrum, a soilborne and non‐pathogenic oomycete capable of inducing plant resistance against Phytophthora sojae infection. Expression of homologous soybean genes involved in ferroptosis and resistance was reprogrammed upon P. oligandrum treatment. Typical hallmarks for characterizing ferroptosis were detected in soybean hypocotyl cells, including decreased glutathione (GSH) level, accumulation of ferric ions, and lipid peroxidation by reactive oxygen species (ROS). Meanwhile, ferroptosis‐like cell death was triggered by P. oligandrum to suppress P. sojae infection in soybean. Protection provided by P. oligandrum could be attenuated by the ferroptosis inhibitor ferrostatin‐1 (Fer‐1), suggesting the critical role of ferroptosis in soybean resistance against P. sojae. Taken together, these results demonstrate that ferroptosis is a P. oligandrum‐inducible defence mechanism against oomycete infection in soybean.
ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.16248