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R-SNARE FgSec22 is essential for growth, pathogenicity and DON production of Fusarium graminearum

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Abstract

SNAREs (soluble N-ethylmaleimide-sensitive factor attachment protein receptors) facilitate intracellular vesicle trafficking and membrane fusion in eukaryotic cells, and play a vital role in growth, development and pathogenicity of phytopathogens. Fusarium head blight (FHB) caused by F. graminearum is one of the most devastating diseases of wheat and barley worldwide. Sec22 is a member of the SNARE family of proteins and its homologues have been shown to have diverse biological roles in different organisms. However, the functions of this protein in the development and pathogenesis of F. graminearum are currently unknown. In this study, we employed integrated biochemical, microbiological and molecular genetic approaches to investigate the roles of FgSec22 in F. graminearum. Our data reveal that this SNARE protein is localized to endoplasmic reticulum (ER) and is indispensable for normal conidiation, conidial morphology and pathogenesis of this phytopathogenic fungus. Our biochemical assay of deoxynivalenol (DON) reveals the active involvement of this protein in the production of this mycotoxin in F. graminearum. This has further been confirmed by qRT-PCR analyses of trichothecene (TRI) genes’ expression where the ΔFgsec22 deletion mutant demonstrated a significant down-regulation of these genes in comparison to the wild-type PH-1. Unlike the wild-type and the complemented strain, the mutant strain presents a remarkable defect in colony formation which reflects the critical role it plays in vegetative growth. Collectively, our data support that the SNARE protein FgSec22 is required for vegetative growth, pathogenesis and DON biosynthesis in F. graminearum.

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Acknowledgements

We really appreciate Prof. Zonghua Wang (Fujian Agriculture and Forestry University), Prof. Daniel J. Ebbole (Texas A&M University), Prof. Stefan Olsson (Fujian Agriculture and Forestry University) and Dr. Justice Norvienyeku (Fujian Agriculture and Forestry University) for their valuable suggestions and fruitful discussions.

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  1. Muhammad Adnan and Wenqin Fang contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, 350002, Fuzhou, China

    Muhammad Adnan, Wenqin Fang, Peng Sun, Yangling Zheng, Jing Zhang, Yi Lou, Wenhui Zheng & Guo-dong Lu

  2. Key Laboratory of Biopesticides and Chemical Biology of Education Ministry, Fujian Agriculture and Forestry University, 350002, Fuzhou, China

    Muhammad Adnan, Wenqin Fang, Peng Sun, Yangling Zheng, Jing Zhang, Yi Lou, Wenhui Zheng & Guo-dong Lu

  3. Temasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore

    Wenhui Zheng

  4. Department of Biochemistry, Faculty of Life Sciences, Ahmadu Bello University, Zaria, Nigeria

    Yakubu Saddeeq Abubakar

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Contributions

Conceptualization: MA, WZ, GL; data curation: MA, YZ, YS, YL, WF, JZ; formal analysis: MA, YZ, YS, JZ; funding acquisition: WZ, GL; investigation: MA, YZ, YL, WF, JZ; methodology: MA, YZ, YL, WF, JZ; supervision: WZ, GL; validation: YL, WZ, GL; visualization: MA, YZ, WZ, GL; writing—original draft: MA, YS, WZ, GL; writing—review and editing: YZ, YL, YS, WF, JZ.

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Correspondence to Wenhui Zheng or Guo-dong Lu.

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Fig. S1.

Phylogenetic analysis and domain architecture of FgSec22 and its orthologs. Phylogenetic tree of Sec22 from fungi to mammals was constructed based on the alignment of sequences of Sec22. The neighbor-joining tree was built with MEGA7 software based on the amino acid sequence of Sec22 from each species. The conserved regions or domains are represented with different colored boxes

Fig. S2

Gene knockout and southern blot analysis of ΔFgsec22 mutant in F. graminearum. A. Split marker approach was adopted to generate ΔFgsec22 gene knockout using HPH sequence instead of FgSEC22 in the wild-type PH-1 of F. graminearum. B. Southern blot analysis of FgSEC22 gene deletion. FgSEC22 deletion mutants were confirmed by southern blot analysis, DNA was digested using Xho I and Hind III restriction enzymes. FgSec22-AF (1F) and FgSec22-AR (2R) primer pair was used to amplify the upstream region of respective gene and used this fragment as a probe during hybridization

Fig. S3.

Sexual reproduction of F. graminearumA. Carrot agar plates, black perithecia were formed on carrot agar 21 dpi. B. Cirri (masses of ascospores) formed on top of perithecium of PH-1 and ΔFgsec22-Com complemented strains and perithecium of ΔFgsec22 mutant strain as well. C. Fascicles of asci observed under microscope after squeezing the perithecia. Sexual reproduction revealed that there was no obvious variation among the wild-type and mutant strains. The carrot agar plates produced abundant perithecia in all strains. Similarly, cirri were also observed in all strains. Particular rosette-like morphology of asci was observed after breaking the perithecium in all of the strains

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Adnan, M., Fang, W., Sun, P. et al. R-SNARE FgSec22 is essential for growth, pathogenicity and DON production of Fusarium graminearum. Curr Genet 66, 421–435 (2020). https://doi.org/10.1007/s00294-019-01037-y

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