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

Abstract

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.

Ferroptosis induction in host rice by endophyte OsiSh-2 is necessary for mutualism and disease resistance in symbiosis

“…M. oryzae suppress or induces ferroptosis at a basal/minimal level in blast-susceptible rice plants, thus enabling its successful invasion 19 . By inducing ferroptosis, the soilborne biocontrol agent Pythium oligandrum has been reported to enhance soybean resistance to Phytophthora sojae 39 . However, the role of ferroptosis in host–microbe interactions is still underestimated.…”

The mycoparasite Pythium oligandrum induces legume pathogen resistance and shapes rhizosphere microbiota without impacting mutualistic interactions

“…The ability of P. oligandrum to promote plant growth and nutrition may account for this improved resistance to the disease. In addition, the production of elicitors such as POD1 and POD2 cell wall proteins or of oligandrin by P. oligandrum can activate jasmonate and ethylene signaling; the oomycete can trigger host plant ferroptosis as well ( Picard et al., 2000 ; Takenaka et al., 2003 ; Hase et al., 2006 ; Hase et al., 2008 ; Takenaka, 2015 ; Cheng et al., 2022 ). Collectively, these different mechanisms may account for the plant protection against A. euteiches.…”

“…The root colonization by P. oligandrum is associated with induced plant growth promotion (via the production of tryptamine, an auxin precursor ( Le Floch et al., 2003 ). P. oligandrum can also trigger plant immunity by releasing two major glycoproteins with elicitin activity, namely, POD-1 and POD-2, and by interplaying with iron homeostasis in roots ( Takenaka et al., 2011 ; Bělonožníková et al., 2020 ; Cheng et al., 2022 ).…”

Inhibition and biocontrol potential of <i>Ochrobactrum pseudogrignonense </i>NC1 against four <i>Phytophthora </i>species

“…Sang & Kim (2014) proved that two strains of Pseudomonas corrugata: CCR04 and CCR80 resided in chili roots and effectively suppressed Phytophthora blight disease compared to Escherichia coli DH5α. Cheng et al (2022) discovered that ferroptosis induced by the biocontrol agent Pythium oligandrum could enhance soybean resistance to Ps. This study adds to this list and demonstrates the potential of O. pseudogrignonense as a biological control agent against Phytophthora blight.…”