The Phytophthora nucleolar effector Pi23226 targets host ribosome biogenesis to induce necrotrophic cell death

Lee, Soeui; Kim, Jaehwan; Kim, Myung-Shin; Min, Cheol Woo; Kim, Sun Tae; Choi, Sang‐Bong; Lee, Juhyun; Choi, Doil

doi:10.1016/j.xplc.2023.100606

Cited by 11 publications

(3 citation statements)

References 64 publications

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“…As mentioned above, recent research in the pathogenic field has confirmed the involvement of effector proteins in manipulating not only plant proteins but also the host DNA and RNA [42,57,98,99]. In the published R. clarus effectome, one putative candidate effector protein containing a PWWP domain was identified [21].…”

Section: Protein Domains Identified In the R Irregularis Effector Rep...mentioning

confidence: 85%

Characterization of Arbuscular Mycorrhizal Effector Proteins

Chacón

Dingenen

Goormachtig

2023

IJMS

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Plants are colonized by various fungi with both pathogenic and beneficial lifestyles. One type of colonization strategy is through the secretion of effector proteins that alter the plant’s physiology to accommodate the fungus. The oldest plant symbionts, the arbuscular mycorrhizal fungi (AMF), may exploit effectors to their benefit. Genome analysis coupled with transcriptomic studies in different AMFs has intensified research on the effector function, evolution, and diversification of AMF. However, of the current 338 predicted effector proteins from the AM fungus Rhizophagus irregularis, only five have been characterized, of which merely two have been studied in detail to understand which plant proteins they associate with to affect the host physiology. Here, we review the most recent findings in AMF effector research and discuss the techniques used for the functional characterization of effector proteins, from their in silico prediction to their mode of action, with an emphasis on high-throughput approaches for the identification of plant targets of the effectors through which they manipulate their hosts.

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Section: Protein Domains Identified In the R Irregularis Effector Rep...mentioning

confidence: 85%

Characterization of Arbuscular Mycorrhizal Effector Proteins

Chacón

Dingenen

Goormachtig

2023

IJMS

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“…Recently, a case of necrosis was reported in which a P. infestans RXLR effector induced nucleolar inflammation and interfered with pre-rRNA 25S processing, leading to necrosis through disruption of protein translation (Lee et al 2023). This study identified the RXLR effector Pc12 as a critical factor in necrosis, which causes severe ER stress by preventing Rab13-2 recycling in vesicle trafficking.…”

Section: Discussionmentioning

confidence: 99%

An RXLR effector targets ER-Golgi interface to induce ER stress and necrotic cell death

Kim,

Kaleku,

Woo

et al. 2023

Preprint

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To achieve successful colonization, the pathogen secretes hundreds of effectors into host cells to manipulate the host’s immune response. Despite numerous studies, the molecular mechanisms underlying effector-induced necrotic cell death remain elusive. In this study, we identified a novel virulent RXLR effector named Pc12 fromP. capsici.Pc12 induces necrosis by triggering a distinct ER stress response through its interaction with Rab13-2. Unlike conventional hypersensitive response cell death associated with effector-triggered immunity, Pc12-induced cell death does not coincide with defense gene expression. Instead, it induces the relocalization of ER-resident proteins and confines secretory proteins within the ER. Pc12 interacts with Rab13-2, exhibiting a specific affinity for the active form of Rab13-2. Thus, it mimics the conformation of the inactive state of Rab13-2, subsequently recruiting the Rab-escort protein (REP). This process results in disruptions in vesicle formation within the ER-Golgi trafficking pathway. Furthermore, the substitution of a single amino acid of Rab13-2 structurally predicted to be crucial for the Pc12 interaction decreased the interaction with Pc12 while maintaining the interaction with REP and PRA1. These findings offer valuable insights into the ER stress-triggered cell death as well as a potential strategy for enhancing resistance against pathogens.

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“…Several other effectors, such as BxSapB1, BxSapB2, and BxSapB3, while capable of inducing plant cell death, also function as a virulence factor, during B. xylophilus infection ( Huang et al., 2019 ; Hu et al., 2019 ; Zhao et al., 2020 ). This phenomenon is relatively common in effectors from fungi and oomycetes, such as the Fusarium graminearum effector Fg62 ( Wang et al., 2023 ), the Phytophthora infestans effector Pi23226 ( Lee et al., 2023 ), etc., which can induce host cell death and promote pathogen parasitism.…”

Section: Introductionmentioning

confidence: 99%

A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration

Li,

Wang,

Cao

et al. 2024

Front. Plant Sci.

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The migratory endoparasitic phytonematodes Bursaphelenchus xylophilus is the causal agent of pine wilt disease and causes significant economic damage to pine forests in China. Effectors play a key role in the successful parasitism of plants by phytonematodes. In this study, 210 genes obtained by transcriptomics analyses were found to be upregulated in B. xylophilus infecting Pinus massoniana that were not functionally annotated nor reported previously in B. xylophilus infecting P. thunbergii. Among these differentially expressed genes, a novel effector, BxICD1, that could induce cell death in the extracellular space of Nicotiana benthamiana was identified. BxICD1 was upregulated in the early stages of infection, as shown by RT-qPCR analyses. In situ hybridization analysis showed that BxICD1 was expressed in the esophageal gland of nematodes. The yeast signal sequence trap system indicated that BxICD1 possessed an N-terminal signal peptide with secretion functionality. Using an Agrobacterium-mediated transient expression system, it was demonstrated that the cell death-inducing activity of BxICD1 was dependent on N. benthamiana brassinosteroid-insensitive 1-associated kinase 1 (NbBAK1). Finally, BxICD1 contributed to B. xylophilus virulence and migration in host pine trees, as demonstrated by RNAi silencing assays. These findings indicate that BxICD1 both induces plant cell death and also contributes to nematode virulence and migration in P. massonian.

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The Phytophthora nucleolar effector Pi23226 targets host ribosome biogenesis to induce necrotrophic cell death

Cited by 11 publications

References 64 publications

Characterization of Arbuscular Mycorrhizal Effector Proteins

Characterization of Arbuscular Mycorrhizal Effector Proteins

An RXLR effector targets ER-Golgi interface to induce ER stress and necrotic cell death

A Bursaphelenchus xylophilus effector BxICD1 inducing plant cell death, concurrently contributes to nematode virulence and migration

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