Cleavage of a pathogen apoplastic protein by plant subtilases activates host immunity

Wang, Shuaishuai; Xing, Rongkang; Wang, Yan; Shu, Haidong; Fu, Shenggui; Huang, Jie; Paulus, Judith K; Schuster, Mariana; Saunders, Diane G. O.; Win, Joe; Vleeshouwers, Vivianne G. A. A.; Wang, Yuanchao; Zheng, Xiaobo; Hoorn, R.A.L. van der; Dong, Suomeng

doi:10.1111/nph.17120

Cited by 32 publications

(13 citation statements)

References 61 publications

(81 reference statements)

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“…The other two residues might be part of epitopes that contribute to the phytotoxic activity and the mutations might lead to exposure of the immunogenic epitopes, resulting in enhanced activity. A similar study recently revealed that the secreted apoplastic protein PC2 from the potato late blight pathogen Phytophthora infestans was cleavage by plant apoplastic proteases, which is the essential process for PC2 to release the immunogenic peptides, thus to activate plant defence responses (Wang et al ., 2021a). Indeed, several studies demonstrated that heat denaturation or structural mutation of some secreted proteins did not abolish the necrosis‐inducing activity (Zhang et al ., 2014a; Zhang et al ., 2014b), indicating that the potential epitopes are sufficient for the plant cell death‐inducing activity.…”

Section: Discussionmentioning

confidence: 99%

Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector

Zhu

et al. 2022

Environmental Microbiology

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Botrytis cinerea is a broad-host-range necrotrophic phytopathogen responsible for serious diseases in leading crops. To facilitate infection, B. cinerea secretes a large number of effectors that induce plant cell death. In screening secretome data of B. cinerea during infection stage, we identified a phytotoxic protein (BcSSP2) that can also induce immune resistance in plants. BcSSP2 is a small, cysteine-rich protein without any known domains. Transient expression of BcSSP2 in leaves caused chlorosis that intensifies with time and eventually leads to death. Point mutations in eight of 10 cysteine residues abolished phytotoxicity, but residual toxic activity remained after heating treatment, suggesting contribution of unknown epitopes to protein phyto-toxicity. The expression of bcssp2 was low during the first 36 h after inoculation and increased sharply upon transition to late infection stage. Deletion of bcssp2 did not cause statistically significant changes in lesions size on bean and tobacco leaves. Further analyses indicated that the phytotoxicity of BcSSP2 is negatively regulated by the receptor-like kinases BAK1 and SOBIR1. Collectively, our findings show that BcSSP2 is an effector protein that toxifies the host cells, but is also recognized by the plant immune system.

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Section: Discussionmentioning

confidence: 99%

Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector

Zhu

et al. 2022

Environmental Microbiology

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“…On the one hand, several secreted fungalysins have been reported to enhance the pathogen invasion by cleaving plant secreted chitinases (Naumann et al, 2011;Jashni et al, 2015a;Sanz-Martín et al, 2016;Ökmen et al, 2018). On the other hand, the host plant can also release proteases to inhibit the growth and invasion of pathogens through direct cleavage of their cell wall protein components or triggering plant defense via cleavage of their secreted effector proteins (Jashni et al, 2015b;Wang et al, 2020Wang et al, , 2021. During the middle and late stages of L. deliciosus-P. taeda EcM development, 81 transcripts coding for secreted proteases accumulated at a much higher level in colonizing L. deliciosus hyphae.…”

Section: Secreted Proteases Are Important Elements In the Symbiotic Toolkit Of Lactariusmentioning

confidence: 99%

Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius–Pinus Symbioses

Tang

Lebreton

et al. 2021

Front. Plant Sci.

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Ectomycorrhizal fungi establish a mutualistic symbiosis in roots of most woody plants. The molecular underpinning of ectomycorrhizal development was only explored in a few lineages. Here, we characterized the symbiotic transcriptomes of several milkcap species (Lactarius, Russulales) in association with different pine hosts. A time-course study of changes in gene expression during the development of L. deliciosus–Pinus taeda symbiosis identified 6 to 594 differentially expressed fungal genes at various developmental stages. Up- or down-regulated genes are involved in signaling pathways, nutrient transport, cell wall modifications, and plant defenses. A high number of genes coding for secreted proteases, especially sedolisins, were induced during root colonization. In contrast, only a few genes encoding mycorrhiza-induced small secreted proteins were identified. This feature was confirmed in several other Lactarius species in association with various pines. Further comparison among all these species revealed that each Lactarius species encodes a highly specific symbiotic gene repertoire, a feature possibly related to their host-specificity. This study provides insights on the genetic basis of symbiosis in an ectomycorrhizal order, the Russulales, which was not investigated so far.

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“…In similar cases, cell death triggered by fungal endopolygalacturonases, the glycoside hydrolase 12 proteins, or elicitins is dependent on the Arabidopsis RLP AtRLP42, N. benthamiana RLP RXEG1, and Solanum microdontum RLP ELR (Zhang et al, 2013; Du et al, 2015; Wang et al, 2018). For many other elicitors, such as P. infestans apoplastic effector PC2, P. sojae effector AEP1, Zymoseptoria tritici effectors Zt9, Zt11, and Zt12 and Ustilaginoidea virens effector SGP1, although the corresponding immune receptors have not yet been identified, cell death activation has been shown to be reliant on membrane‐localized RLK BAK1 and/or SOBIR1 (Kettles et al, 2017; Song et al, 2021; Wang et al, 2021; Xu et al, 2021). One exception is Nep1‐like proteins (NLPs), for which cell death is activated by cytotoxic activity.…”

Section: Discussionmentioning

confidence: 99%

Microbe‐derived non‐necrotic glycoside hydrolase family 12 proteins act as immunogenic signatures triggering plant defenses

Wang

Liu

Zhang

et al. 2022

JIPB

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Plant pattern recognition receptors (PRRs) are sentinels at the cell surface sensing microbial invasion and activating innate immune responses. During infection, certain microbial apoplastic effectors can be recognized by plant PRRs, culminating in immune responses accompanied by cell death. However, the intricated relationships between the activation of immune responses and cell death are unclear. Here, we studied the glycoside hydrolase family 12 (GH12) protein, Ps109281, secreted by Phytophthora sojae into the plant apoplast during infection. Ps109281 exhibits xyloglucanase activity, and promotes P. sojae infection in a manner dependent on the enzyme activity. Ps109281 is recognized by the membrane‐localized receptor‐like protein RXEG1 and triggers immune responses in various plant species. Unlike other characterized GH12 members, Ps109281 fails to trigger cell death in plants. The loss of cell death induction activity is closely linked to a sequence polymorphism at the N‐terminus. This sequence polymorphism does not affect the in planta interaction of Ps109281 with the recognition receptor RXEG1, indicating that cell death and immune response activation are determined using different regions of the GH12 proteins. Such GH12 protein also exists in other Phytophthora and fungal pathogens. Taken together, these results unravel the evolution of effector sequences underpinning different immune outputs.

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Cleavage of a pathogen apoplastic protein by plant subtilases activates host immunity

Cited by 32 publications

References 61 publications

Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector

Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector

Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius–Pinus Symbioses

Microbe‐derived non‐necrotic glycoside hydrolase family 12 proteins act as immunogenic signatures triggering plant defenses

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