Inappropriate Expression of an NLP Effector in <i>Colletotrichum orbiculare</i> Impairs Infection on Cucurbitaceae Cultivars via Plant Recognition of the C-Terminal Region

Azmi, Nur Sabrina Ahmad; Singkaravanit-Ogawa, Suthitar; Ikeda, Kyoko; Kitakura, Saeko; Inoue, Yushi; Narusaka, Yoshihiro; Shirasu, Ken; Kaido, Masanori; Mise, Kazuyuki; Takano, Yoshitaka

doi:10.1094/mpmi-04-17-0085-fi

Cited by 30 publications

(32 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This idea is consistent with the findings that NLP expression is restricted to the late infection phase of hemi-biotrophic pathogens 31,39,40 . However, our previous work on C. orbiculare-cucurbit interactions suggested another explanation for the restriction of NLP expression to the late phase 25 . We generated a transgenic strain of C. orbiculare that expressed the NLP gene not only at the late infection phase but also at the early infection phase, and found that the generated C. orbiculare transformants failed to infect cucurbits by activating their pre-invasive resistance 25 .…”

Section: Discussionmentioning

confidence: 89%

“…The recognition of nlp20 is also observed in other plants of the Brassicaceae family, i.e., Arabis alpina, Thlaspi arvense and Draba rigida, and the Asteraceae family, i.e., Lactuca sativa 2 . In contrast, it was reported that cucurbits recognize the C-terminal amino acids of NLPs 25 . Recently, an LRR-receptor protein (LRR-RP) termed RLP23 was identified as the receptor for nlp20 in A. thaliana 26 .…”

mentioning

confidence: 87%

See 1 more Smart Citation

RLP23 is required for Arabidopsis immunity against the grey mould pathogen Botrytis cinerea

Ono

Mise

Takano

2020

Sci Rep

Self Cite

View full text Add to dashboard Cite

Necrosis-and ethylene-inducing-like proteins (NLPs) are secreted by fungi, oomycetes and bacteria. Conserved nlp peptides derived from NLPs are recognized as pathogen-associated molecular patterns (PAMPs), leading to PAMP-triggered immune responses. RLP23 is the receptor of the nlp peptides in Arabidopsis thaliana; however, its actual contribution to plant immunity is unclear. Here, we report that RLP23 is required for Arabidopsis immunity against the necrotrophic fungal pathogen Botrytis cinerea. Arabidopsis rlp23 mutants exhibited enhanced susceptibility to B. cinerea compared with the wild-type plants. Notably, microscopic observation of the B. cinerea infection behaviour indicated the involvement of RLP23 in pre-invasive resistance to the pathogen. B. cinerea carried two NLP genes, BcNEP1 and BcNEP2; BcNEP1 was expressed preferentially before/during invasion into Arabidopsis, whereas BcNEP2 was expressed at the late phase of infection. Importantly, the nlp peptides derived from both BcNEP1 and BcNEP2 induced the production of reactive oxygen species in an RLP23dependent manner. In contrast, another necrotrophic fungus Alternaria brassicicola did not express the NLP gene in the early infection phase and exhibited no enhanced virulence in the rlp23 mutants. Collectively, these results strongly suggest that RLP23 contributes to Arabidopsis pre-invasive resistance to B. cinerea via NLP recognition at the early infection phase. Plants activate immunity against pathogenic microorganisms through their perception of pathogen-associated molecular patterns (PAMPs), for protection against pathogen infection 1. Many types of PAMPs have been reported, such as flg22 (derived from bacterial flagellin), elf18 (derived from the bacterial elongation factor-Tu), chitin (derived from fungal cell wall), and the nlp peptides derived from secreted proteins termed necrosis-and ethylene-inducing-like proteins (NLPs), conserved in a broad range of fungi, bacteria and oomycetes 2-6. PAMPs are recognized by corresponding pattern-recognition receptors (PRRs) localized on the plasma membrane of plant cells 1. For instance, the flg22 is recognized by a leucine-rich repeat receptor-like kinase (LRR-RK) termed FLAGELLIN SENSITIVE 2 (FLS2) 3. FLS2 interacts with its co-receptor, BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1), and the two factors trans-phosphorylate each other after perception of flg22 7,8. A series of phosphorylation events lead to the subsequent activation of PAMP-triggered immune responses, such as reactive oxygen species (ROS) burst, mitogen-activated protein kinase (MAPK) activation and callose deposition 9. Regarding the limited PRR genes, it was reported that the deletion of a single of these genes reduces the resistance against particular pathogens. For example, Arabidopsis fls2 mutants are more susceptible to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000, as assessed via spray-inoculation of the fls2 mutants with a suspension of the pathogen 10. The Arabidopsis CHITIN ELICITOR RECEPTOR KINASE...

show abstract

Section: Discussionmentioning

confidence: 89%

mentioning

confidence: 87%

RLP23 is required for Arabidopsis immunity against the grey mould pathogen Botrytis cinerea

Ono

Mise

Takano

2020

Sci Rep

Self Cite

View full text Add to dashboard Cite

show abstract

“…As the timing of gene expression and transcript abundance are often crucial for virulence, phytopathogens may employ transcriptional plasticity to optimise infection on a given host ( Fig. 1; Azmi et al, 2018). This form of adaptation will lead to isolates with diverse transcriptional profiles, which could also have different fitness optima on the same host.…”

Section: Transcriptional Plasticity In Stressful Environmentsmentioning

confidence: 99%

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

et al. 2019

View full text Add to dashboard Cite

Rapid (co-)evolution at multiple timescales is a hallmark of plant-microbe interactions. The mechanistic basis for the rapid evolution largely rests on the features of the genomes of the interacting partners involved. Here, we review recent insights into genomic characteristics and mechanisms that enable rapid evolution of both plants and phytopathogens. These comprise fresh insights in allelic series of matching pairs of resistance and avirulence genes, the generation of novel pathogen effectors, the recently recognised small RNA warfare, and genomic aspects of secondary metabolite biosynthesis. In addition, we discuss the putative contributions of permissive host environments, transcriptional plasticity and the role of ploidy on the interactions. We conclude that the means underlying the rapid evolution of plant-microbe interactions are multifaceted and depend on the particular nature of each interaction.

show abstract

“…However, there are many proteins with no clear functions in various fungi ( Supplementary Table S3). For example, MgNLP was not required in Mycosphaerella graminicola (Motteram et al, 2009), but CoNLP could impair infection in Colletotrichum orbiculare (Azmi et al, 2018). The hypothetical proteins may be involved in virulence of V. pyri, but further analysis need detail characterization in the future.…”

Section: Discussionmentioning

confidence: 99%

“…Among them, pisatin demethylase, fumitremorgin C monooxygenase and trichodiene oxygenase belong to the P450 family and are important for pathogenic fungus infection (Funnell and VanEtten, 2002;Siewers et al, 2005;Alexander et al, 2008;Zhang et al, 2012). Orthologs of NPP1 in different fungi have various roles (Motteram et al, 2009;Azmi et al, 2018). Although the level of NPP1 expression was significantly reduced in the deletion mutant, further characterization is needed to confirm its roles in V. pyri.…”

Section: Discussionmentioning

confidence: 99%

The Fungal-Specific Transcription Factor VpFSTF1 Is Required for Virulence in Valsa pyri

Kange

Xia

et al. 2020

Front. Microbiol.

View full text Add to dashboard Cite

Valsa pyri is the causal agent of pear canker disease, which leads to enormous losses of pear production in eastern Asian, especially China. In this study, we identified a fungal-specific transcription factor 1 (termed as VpFSTF1) from V. pyri, which is highly conserved in fungi. To characterize its functions, we generated mutant and complementation strains in V. pyri and found that VpFSTF1 mutants lost the ability to form fruiting bodies along with the reduced virulence. The radial growth of VpFSTF1 mutant was sensitive to increasing concentrations of hydrogen peroxide (H 2 O 2) and salicylic acid (SA). Moreover, RNA-sequencing (RNA-Seq) analysis of wild-type (WT) and VpFSTF1 mutant strains was performed, and the results revealed 1,993 upregulated, and 2006 downregulated differentially expressed genes (DEGs) in the mutant. The DEGs were corresponding to the genes that are involved in amino acid metabolism, starch, and sucrose metabolism, gluconeogenesis, citrate cycle, and carbon metabolism. Interestingly, pathogen host interaction (PHI) analysis showed that 69 downregulated genes were related to virulence, suggesting that they might function downstream of VpFSTF1. Nine DEGs were further validated by quantitative reverse transcriptionpolymerase chain reaction (qRT-PCR), and the results were consistent with RNA-seq analysis. Furthermore, promoter regions were predicted, and VpFSTF1 binding activity was assessed. We demonstrated that five promoters are directly or indirectly targeted by VpFSTF1, including catalase-related peroxidase (VPIG_01209) and P450 family genes. Taken together, these findings indicate that VpFSTF1 is crucial for the virulence of V. pyri via direct or indirect regulation of downstream genes expression and lay an important foundation for understanding the molecular mechanism of V. pyri infection.

show abstract

Inappropriate Expression of an NLP Effector in Colletotrichum orbiculare Impairs Infection on Cucurbitaceae Cultivars via Plant Recognition of the C-Terminal Region

Cited by 30 publications

References 41 publications

RLP23 is required for Arabidopsis immunity against the grey mould pathogen Botrytis cinerea

RLP23 is required for Arabidopsis immunity against the grey mould pathogen Botrytis cinerea

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

The Fungal-Specific Transcription Factor VpFSTF1 Is Required for Virulence in Valsa pyri

Contact Info

Product

Resources

About