An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection

Jiang, Cong; Cao, Shulin; Wang, Zeyi; Xu, Huaijian; Liang, Jie; Liu, Huiquan; Wang, Guanghui; Ding, Mingyu; Wang, Qinhu; Gong, Chen; Feng, Chanjing; Hao, Chaofeng; Xu, Jin‐Rong

doi:10.1038/s41564-019-0468-8

Cited by 73 publications

(87 citation statements)

References 59 publications

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“…The Ste2-mediated response to HRP was found to be governed by the cell wall integrity pathway, similar to that observed in F. oxysporum 5 . Consistent Interestingly, a recent study by Jiang et al found that wild type F. graminearum exhibits a two and a half-fold increase in phosphorylation of FgGpmk1 and negligible increase in phosphorylation of Mgv1 when treated with dissected flowering wheat spikelets 66 . The discrepancy between the aforementioned study and the findings presented here is likely related to methodological differences, where dissected tissues may have a loss of enzymatically activate peroxidases compared to the live plant.…”

Section: Discussionmentioning

confidence: 79%

Ste2 receptor-mediated chemotropism of Fusarium graminearum contributes to its pathogenicity against wheat

Sridhar

Trofimova

Subramaniam

et al. 2020

Sci Rep

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Fusarium Head Blight of wheat, caused by the filamentous fungus Fusarium graminearum, leads to devastating global food shortages and economic losses. While many studies have addressed the responses of both wheat and F. graminearum during their interaction, the possibility of fungal chemotropic sensing enabling pathogenicity remains unexplored. Based on recent findings linking the pheromone-sensing G-protein-coupled receptor Ste2 to host-directed chemotropism in Fusarium oxysporum, we investigated the role of the Ste2 receptor and its downstream signaling pathways in mediating chemotropism of F. graminearum. Interestingly, a chemotropic response of growing hyphae towards catalytically active Triticum aestivum 'Roblin' cultivar secreted peroxidases was detected, with deletion of STE2 in F. graminearum leading to loss of the observed response. At the same time, deletion of STE2 significantly decreased infection on germinating wheat coleoptiles, highlighting an association between Ste2, chemotropism and infection by F. graminearum. Further characterization revealed that the peroxidase-directed chemotropism is associated with stimulation of the fungal cell wall integrity mitogen-activated protein kinase signaling cascade. Altogether, this study demonstrates conservation of Ste2-mediated chemotropism by Fusarium species, and its important role in mediating pathogenicity.

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Section: Discussionmentioning

confidence: 79%

Ste2 receptor-mediated chemotropism of Fusarium graminearum contributes to its pathogenicity against wheat

Sridhar

Trofimova

Subramaniam

et al. 2020

Sci Rep

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show abstract

“…1a) and tend to be less transcribed or transcribed at lower levels ( Fig. 1b) based on published RNA-seq data 20,30 . Fifty of them were predicted to encode proteins with signal peptides (SPs) and named OSP genes in this study.…”

Section: Resultsmentioning

confidence: 90%

“…Gene replacement constructs were generated with the split-marker approach and transformed into protoplasts of PH-1 17,20 . For each OSP gene, at least two independent gene replacement mutants were identified.…”

Section: Methodsmentioning

confidence: 99%

“…DON production in the inoculated spikelets sampled at 14 dpi was assayed by GCMS-QP2010 system with AOC-20i autoinjector (Shimadzu Co. Japan). To assay infection cushion formation, infected lemmas were sampled at 2 dpi, fixed with 4% (vol/vol) glutaraldehyde, and coated with gold-palladium before examination with a JEOL 6360 scanning electron microscope (Jeol Ltd., Japan) 14,20,76 . For assaying infectious growth, infected rachis tissues were embedded in Spurr resin after fixation with 3% glutaraldehyde and dehydration in graded series of 30-100% of ethanol before being sectioned 77 .…”

Section: Methodsmentioning

confidence: 99%

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An orphan protein of Fusarium graminearum modulates host immunity by mediating proteasomal degradation of TaSnRK1α

et al. 2020

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Fusarium graminearum is a causal agent of Fusarium head blight (FHB) and a deoxynivalenol (DON) producer. In this study, OSP24 is identified as an important virulence factor in systematic characterization of the 50 orphan secreted protein (OSP) genes of F. graminearum. Although dispensable for growth and initial penetration, OSP24 is important for infectious growth in wheat rachis tissues. OSP24 is specifically expressed during pathogenesis and its transient expression suppresses BAX-or INF1-induced cell death. Osp24 is translocated into plant cells and two of its 8 cysteine-residues are required for its function. Wheat SNF1-related kinase TaSnRK1α is identified as an Osp24-interacting protein and shows to be important for FHB resistance in TaSnRK1α-overexpressing or silencing transgenic plants. Osp24 accelerates the degradation of TaSnRK1α by facilitating its association with the ubiquitin-26S proteasome. Interestingly, TaSnRK1α also interacts with TaFROG, an orphan wheat protein induced by DON. TaFROG competes against Osp24 for binding with the same region of TaSnRKα and protects it from degradation. Overexpression of TaFROG stabilizes TaSnRK1α and increases FHB resistance. Taken together, Osp24 functions as a cytoplasmic effector by competing against TaFROG for binding with TaSnRK1α, demonstrating the counteracting roles of orphan proteins of both host and fungal pathogens during their interactions.

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“…Protein domain prediction analysis showed that each flippase in F. graminearum has more than seven transmembrane motifs distributed along the protein ( Figure S4), which is consistent with their predicted roles as transporters on the membrane. (Liu et al, 2016;Jiang et al, 2019). The expression profiles showed that all the five flippases had increased expression levels at the sexual reproduction stage but reduced during pathogenesis ( Figure S6a).…”

Section: The Different Flippases Have Different Cellular Localizatimentioning

confidence: 99%

Flippases play specific but distinct roles in the development, pathogenicity, and secondary metabolism of Fusarium graminearum

Yun

Guo

Zhang

et al. 2020

Molecular Plant Pathology

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The membrane trafficking system is important for compartmentalization of the biosynthesis pathway and secretion of deoxynivalenol (DON) mycotoxin (a virulence factor) in Fusarium graminearum. Flippases are transmembrane lipid transporters and mediate a number of essential physiological steps of membrane trafficking, including vesicle budding, charging, and protein diffusion within the membrane. However, the roles of flippases in secondary metabolism remain unknown in filamentous fungi. Herein, we identified five flippases (FgDnfA, FgDnfB, FgDnfC1, FgDnfC2, and FgDnfD) in F. graminearum and established their specific and redundant functions in the development and pathogenicity of this phytopathogenic fungus. Our results demonstrate that FgDnfA is critical for normal vegetative growth while the other flippases are dispensable. FgDnfA and FgDnfD were found crucial for the fungal pathogenesis, and a remarkable reduction in DON production was observed in ΔFgDNFA and ΔFgDNFD. Deletion of the FgDNFB gene increased DON production to about 30 times that produced by the wild type. Further analysis showed that FgDnfA and FgDnfD have positive roles in the regulation of trichothecene (TRI) genes (TRI1, TRI4, TRI5, TRI6, TRI12, and TRI101) expression and toxisome reorganization, while FgDnfB acts as a negative regulator of DON synthesis. In addition, FgDnfB and FgDnfD have redundant functions in the regulation of phosphatidylcholine transport, and double deletion of FgDNFB and FgDNFD showed serious defects in fungal development, DON synthesis, and virulence. Collectively, our findings reveal the distinct and specific functions of flippase family members in F. graminearum and principally demonstrate that FgDnfA, FgDnfD, and FgDnfB have specific spatiotemporal roles during toxisome biogenesis.

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An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection

Cited by 73 publications

References 59 publications

Ste2 receptor-mediated chemotropism of Fusarium graminearum contributes to its pathogenicity against wheat

Ste2 receptor-mediated chemotropism of Fusarium graminearum contributes to its pathogenicity against wheat

An orphan protein of Fusarium graminearum modulates host immunity by mediating proteasomal degradation of TaSnRK1α

Flippases play specific but distinct roles in the development, pathogenicity, and secondary metabolism of Fusarium graminearum

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