Apoplastic Cell Death-Inducing Proteins of Filamentous Plant Pathogens: Roles in Plant-Pathogen Interactions

Li, Ya; Han, Yijuan; Qu, Mengyu; Chen, Jia; Chen, Xiaofeng; Geng, Xueqing; Wang, Zonghua; Chen, Songbiao

doi:10.3389/fgene.2020.00661

Cited by 32 publications

(28 citation statements)

References 190 publications

(230 reference statements)

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“…In addition, six genes encoding plant CDIPs (Li et al ., 2020) were upregulated in IC: BcPg2 and BcPg3 (Kars et al ., 2005), BcXyn11A (Brito et al ., 2006), BcNep2 (Schouten et al ., 2008), BcXyg1 (Zhu et al ., 2017) and the homologue of VmE02 (Nie et al ., 2019). The subcategory of CDIP is significantly enriched among the upregulated genes in IC (Table 1) and this would suggest that IC actively participate in the triggering of plant cell death.…”

Section: Resultsmentioning

confidence: 99%

“…(2013); **FCWE, fungus cell wall enzymes; ***Bcin proteins displaying an ‘IPR’ InterPro domain (http://www.ebi.ac.uk/interpro/; Mitchell et al ., 2018) were searched on the Botportal database (https://bioinfo.bioger.inra.fr/botportalpublic/; Simon and Viaud, 2018); ****CAZy database (Lombard et al ., 2014; http://www.cazy.org/). Six plant cell death–inducing proteins (CDIP; Li et al ., 2020) are shown in bold. (Additional information is provided in Table S3).…”

Section: Resultsmentioning

confidence: 99%

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The infection cushion of Botrytis cinerea: a fungal ‘weapon’ of plant‐biomass destruction

Choquer

Rascle

Gonçalves

et al. 2021

Environmental Microbiology

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The necrotrophic plant-pathogen fungus Botrytis cinerea produces multicellular appressoria dedicated to plant penetration, named infection cushions (IC). A microarray analysis was performed to identify genes upregulated in mature IC. The expression data were validated by RT-qPCR analysis performed in vitro and in planta, proteomic analysis of the IC secretome and biochemical assays. 1231 upregulated genes and 79 up-accumulated proteins were identified. The data support the secretion of effectors by IC: phytotoxins, ROS, proteases, cutinases, plant cell wall-degrading enzymes and plant cell death-inducing proteins. Parallel upregulation of sugar transport and sugar catabolism-encoding genes would indicate a role of IC in nutrition. The data also reveal a substantial remodelling of the IC cell wall and suggest a role for melanin and chitosan in IC function. Lastly, mutagenesis of two upregulated genes in IC identified secreted fasciclin-like proteins as actors in the pathogenesis of B. cinerea. These results support the role of IC in plant penetration and also introduce other unexpected functions for this fungal organ, in colonization, necrotrophy and nutrition of the pathogen.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

The infection cushion of Botrytis cinerea: a fungal ‘weapon’ of plant‐biomass destruction

Choquer

Rascle

Gonçalves

et al. 2021

Environmental Microbiology

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“…For example, RXEG1, an LRR‐RLP identified from N. benthamiana through a high‐throughput VIGS screen, can specifically recognize the GH12 family cell death‐inducing protein PsXEG1 (Wang et al., 2018). However, some cell surface receptors, such as RLP23, ELR, and RXEG1, have extracellular LRRs but lack a cytoplasmic signalling domain (Li et al., 2020). The LRR receptor‐like kinases (LRR‐RLKs) BAK1 and SOBIR1 were shown to be essential for RLP23, ELR, or RXEG1‐induced cell death and immune responses that act as coreceptors to transduce signals to downstream components (Li et al., 2020).…”

Section: Discussionmentioning

confidence: 99%

“…However, some cell surface receptors, such as RLP23, ELR, and RXEG1, have extracellular LRRs but lack a cytoplasmic signalling domain (Li et al., 2020). The LRR receptor‐like kinases (LRR‐RLKs) BAK1 and SOBIR1 were shown to be essential for RLP23, ELR, or RXEG1‐induced cell death and immune responses that act as coreceptors to transduce signals to downstream components (Li et al., 2020). Moreover, BAK1 was required for the attenuation of EIX‐induced defence responses by the decoy receptor LeEIX1 (Bar et al., 2010), and SOBIR1 can interact with tomato RLPs Sl EIX2, which was involved in plant immunity (Liebrand et al., 2013).…”

Section: Discussionmentioning

confidence: 99%

FoEG1, a secreted glycoside hydrolase family 12 protein from Fusariumoxysporum, triggers cell death and modulates plant immunity

Zhang

Yan

et al. 2021

Molecular Plant Pathology

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Fusarium oxysporum is an important soilborne fungal pathogen with many different formae speciales that can colonize the plant vascular system and cause serious crop wilt disease worldwide. We found a glycoside hydrolase family 12 protein FoEG1, secreted by F. oxysporum, that acted as a pathogen‐associated molecular pattern (PAMP) targeting the apoplast of plants to induce cell death. Purified FoEG1 protein triggered cell death in different plants and induced the plant defence response to enhance the disease resistance of plants. The ability of FoEG1 to induce cell death was mediated by leucine‐rich repeat (LRR) receptor‐like kinases BAK1 and SOBIR1, and this ability was independent of its hydrolase activity. The mutants of cysteine residues did not affect the ability of FoEG1 to induce cell death, and an 86 amino acid fragment from amino acid positions 144 to 229 of FoEG1 was sufficient to induce cell death in Nicotiana benthamiana. In addition, the expression of FoEG1 was strongly induced in the early stage of F. oxysporum infection of host plants, and FoEG1 deletion or loss of enzyme activity reduced the virulence of F. oxysporum. Therefore, our results suggest that FoEG1 can contribute to the virulence of F. oxysporum depending on its enzyme activity and can also act as a PAMP to induce plant defence responses.

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“…Actually, numerous phytopathogens secrete several toxins or effectors to induce cell death. Around 180 apoplastic cell death-inducing proteins (CDIPs) have been identified and for some of them, the associated receptors are known ( 203 , 204 ). Other toxins are internalized in host cells and interact in some case with NB-LRR ( 182 ).…”

Section: Cell Death Regulations In Mammals and Plantsmentioning

confidence: 99%

Cross Kingdom Immunity: The Role of Immune Receptors and Downstream Signaling in Animal and Plant Cell Death

et al. 2021

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Both plants and animals are endowed with sophisticated innate immune systems to combat microbial attack. In these multicellular eukaryotes, innate immunity implies the presence of cell surface receptors and intracellular receptors able to detect danger signal referred as damage-associated molecular patterns (DAMPs) and pathogen-associated molecular patterns (PAMPs). Membrane-associated pattern recognition receptors (PRRs), such as Toll-like receptors (TLRs), C-type lectin receptors (CLRs), receptor-like kinases (RLKs), and receptor-like proteins (RLPs) are employed by these organisms for sensing different invasion patterns before triggering antimicrobial defenses that can be associated with a form of regulated cell death. Intracellularly, animals nucleotide-binding and oligomerization domain (NOD)-like receptors or plants nucleotide-binding domain (NBD)-containing leucine rich repeats (NLRs) immune receptors likely detect effectors injected into the host cell by the pathogen to hijack the immune signaling cascade. Interestingly, during the co-evolution between the hosts and their invaders, key cross-kingdom cell death-signaling macromolecular NLR-complexes have been selected, such as the inflammasome in mammals and the recently discovered resistosome in plants. In both cases, a regulated cell death located at the site of infection constitutes a very effective mean for blocking the pathogen spread and protecting the whole organism from invasion. This review aims to describe the immune mechanisms in animals and plants, mainly focusing on cell death signaling pathways, in order to highlight recent advances that could be used on one side or the other to identify the missing signaling elements between the perception of the invasion pattern by immune receptors, the induction of defenses or the transmission of danger signals to other cells. Although knowledge of plant immunity is less advanced, these organisms have certain advantages allowing easier identification of signaling events, regulators and executors of cell death, which could then be exploited directly for crop protection purposes or by analogy for medical research.

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Apoplastic Cell Death-Inducing Proteins of Filamentous Plant Pathogens: Roles in Plant-Pathogen Interactions

Cited by 32 publications

References 190 publications

The infection cushion of Botrytis cinerea: a fungal ‘weapon’ of plant‐biomass destruction

The infection cushion of Botrytis cinerea: a fungal ‘weapon’ of plant‐biomass destruction

FoEG1, a secreted glycoside hydrolase family 12 protein from Fusariumoxysporum, triggers cell death and modulates plant immunity

Cross Kingdom Immunity: The Role of Immune Receptors and Downstream Signaling in Animal and Plant Cell Death

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