Mitochondrial‐targeting effector RsIA_CtaG/Cox11 in Rhizoctonia solani AG‐1 IA has two functions: plant immunity suppression and cell death induction mediated by a rice cytochrome c oxidase subunit

Abstract

Rhizoctonia solani AG‐1 IA causes a necrotrophic rice disease and is a serious threat to rice production. To date, only a few effectors have been characterized in AG‐1 IA. We previously identified RsIA_CtaG/Cox11 and showed that infiltration of the recombinant protein into rice leaves caused disease‐like symptoms. In the present study, we further characterized the functionality of RsIA_CtaG/Cox11. RsIA_CtaG/Cox11 is an alternative transcript of cytochrome c oxidase copper chaperone Cox11 that starts from the second AUG codon, but contains a functional secretion signal peptide. RNA interference with RsIA_CtaG/Cox11 reduced the pathogenicity of AG‐1 IA towards rice and Nicotiana benthamiana without affecting its fitness or mycelial morphology. Transient expression of the RsIA_CtaG/Cox11‐GFP fusion protein demonstrated the localization of RsIA_CtaG/Cox11 to mitochondria. Agro‐infiltration of RsIA_CtaG/Cox11 into N. benthamiana leaves inhibited cell death by BAX and INF1. In contrast to rice, agro‐infiltration of RsIA_CtaG/Cox11 did not induce cell death in N. benthamiana. However, cell death was observed when it was coinfiltrated with Os_CoxVIIa, which encodes a subunit of cytochrome c oxidase. Os_CoxVIIa appeared to interact with RsIA_CtaG/Cox11. The cell death triggered by coexpression of RsIA_CtaG/Cox11 and Os_CoxVIIa is independent of the leucine‐rich repeat receptor kinases BAK1/SOBIR1 and enhanced the susceptibility of N. benthamiana to AG‐1 IA. Two of the three evolutionarily conserved cysteine residues at positions 25 and 126 of RsIA_CtaG/Cox11 were essential for its immunosuppressive activity, but not for cell death induction. This report suggests that RsIA_CtaG/Cox11 appears to have a dual role in immunosuppression and cell death induction during pathogenesis.

Host organelles and transporters in underground plant-pathogen interactions

“…It also regulates ROS production. R. solani AG1-1A secretes a protein that interacts with the same enzyme, which enhances virulence and may cause cell death (Zhang et al 2023a).…”

“…In the second scenario, evidence of ROS, PTI and ETI inhibiting R. solani effectors accumulates. The lysin motif protein RsLysM, rare lipoprotein A (RsRlpa), a glycosyltransferase (RsIA_GT) and RsIA_CtaG/COX11 all suppress immune responses (Dölfors et al 2019;Charova et al 2020;Zhang et al 2022Zhang et al , 2023a. Dampening of mitochondrial ROS signalling is a strategy proposed for use by R. solani AG-1A (Zhang et al 2023a).…”

“…The lysin motif protein RsLysM, rare lipoprotein A (RsRlpa), a glycosyltransferase (RsIA_GT) and RsIA_CtaG/COX11 all suppress immune responses (Dölfors et al 2019;Charova et al 2020;Zhang et al 2022Zhang et al , 2023a. Dampening of mitochondrial ROS signalling is a strategy proposed for use by R. solani AG-1A (Zhang et al 2023a). However, whether an increase in defence-related ROS-signalling and programmed cell death or a suppression of defences is more important for the R. solani infection process is unclear.…”

Methionine biosynthetic genes and methionine sulfoxide reductase A are required for Rhizoctonia solaniAG1‐IA to cause sheath blight disease in rice

“…Rhizoctonia solani is a necrotrophic fungal pathogen that causes economically important diseases in various cereals, vegetables and ornamental plants (Francis et al., 2023 ; Liao et al., 2022 ; Molla et al., 2020 ; Zrenner et al., 2020 ). The pathogen has been broadly classified into 14 different anastomosis groups and its strains belonging to AG1‐IA are known to cause sheath blight disease, one of the most devastating diseases in rice (Ghosh et al., 2014 , 2017 ; Senapati et al., 2022 ; Singh et al., 2019 ; Zhang et al., 2024 ). Considering that the source of complete disease resistance against this deadly pathogen is not available in the rice germplasm (Molla et al., 2020 ), efforts have been made to identify various molecular determinants that play important roles during host‐pathogen interactions (Dauda et al., 2023 ; Francis et al., 2023 ; Ghosh et al., 2019 , 2021 ; Wibberg et al., 2016 ; Yang et al., 2023 ; Zheng et al., 2013 ).…”