Skip to main content
SpringerLink
Log in

A myosin passenger protein gene (FaSmy1) is an essential regulator of cell development, pathogenicity, DON biosynthesis, and resistance to the fungicide phenamacril in Fusarium asiaticum

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Kinesins, of which there are 650 members in 15 classes, have two main functions: cell separation and protein transport. In S. cerevisiae, the kinesin-like myosin passenger-protein Smy1(belonging to the TRAFAC class myosin-kinesin ATPase superfamily), which is transported by myosin-5,is part of a negative feedback mechanism that controls actin cable length and prevents overgrowth. The current study determined that defect deletion mutants of FaSmy1 had reduced development of hyphal growth, asexual spore production, pathogenicity, DON biosynthesis, and resistance to phenamacril. These results indicated that FaSmy1 is essential for the growth, development, reproduction and pathogenicity of F. asiaticum. FaSmy1 could be a useful target gene for development of new fungicides for control of Fusarium head blight.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bai, G.-H., Desjardins, A., & Plattner, R. (2002). Deoxynivalenol-nonproducing fusarium graminearum causes initial infection, but does not cause DiseaseSpread in wheat spikes. Mycopathologia, 153, 91–98.

    Article  CAS  PubMed  Google Scholar 

  • Beningo, K. A., Lillie, S. H., & Brown, S. S. (2000). The yeast kinesin-related protein Smy1p exerts its effects on the class V myosin Myo2p via a physical interaction. Molecular Biology of the Cell, 11(2), 691–702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown, D. W., McCormick, S. P., Alexander, N. J., Proctor, R. H., & Desjardins, A. E. (2002). Inactivation of a cytochrome P-450 is a determinant of trichothecene diversity in fusarium species. Fungal Genetics and Biology, 36, 224–233.

    Article  CAS  PubMed  Google Scholar 

  • Brown, D. W., Butchko, R. A., Busman, M., & Proctor, R. H. (2007). The fusarium verticillioides FUM gene cluster encodes a Zn (II) 2Cys6 protein that affects FUM gene expression and fumonisin production. Eukaryotic Cell, 6, 1210–1218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butchko, R. A., Plattner, R. D., & Proctor, R. H. (2003). FUM13 encodes a short chain dehydrogenase/reductase required for C-3 carbonyl reduction during fumonisin biosynthesis in Gibberella moniliformis. Journal of Agricultural and Food Chemistry, 51, 3000–3006.

    Article  CAS  PubMed  Google Scholar 

  • Chan, E. Y. (2001). Molecular motors. In (pp. 759–765). (US).

  • Chen, Y., & Zhou, M. G. (2009). Characterization of Fusarium graminearum isolates resistant to both carbendazim and a new fungicide JS399-19. Phytopathology, 99, 441–446.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y., Chen, C., Wang, J., Jin, L. and Zhou, M. (2007). Genetic study on JS399-19 resistance in hyphal fusion of Fusarium graminearum by using nitrate nonutilizing mutants as genetic markers. Journal of Genetics and Genomics, 34, 469–476.

  • Chen, Y., Li, H.K., Chen, C.J. and Zhou, M.G. (2008). Sensitivity of Fusarium graminearum to fungicide JS399-19: In vitro determination of baseline sensitivity and the risk of developing fungicide resistance. Phytoparasitica, 36, 326–337.

  • Chesarone-Cataldo, M., Guérin, C., Jerry, H. Y., Wedlich-Soldner, R., Blanchoin, L., & Goode, B. L. (2011). The myosin passenger protein Smy1 controls actin cable structure and dynamics by acting as a formin damper. Developmental Cell, 21, 217–230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clayton, J. E., Pollard, L. W., Sckolnick, M., Bookwalter, C. S., Hodges, A. R., Trybus, K. M., et al. (2014). Fission yeast tropomyosin specifies directed transport of myosin-V along actin cables. Molecular Biology of the Cell, 25(1), 66–75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cleveland, T. E., Dowd, P. F., Desjardins, A. E., Bhatnagar, D., & Cotty, P. J. (2003). United States Department of Agriculture—Agricultural Research Service research on pre-harvest prevention of mycotoxins and mycotoxigenic fungi in US crops. Pest Management Science, 59, 629–642.

    Article  CAS  PubMed  Google Scholar 

  • Desjardins, A. E., G-h, B., Plattner, R. D., & Proctor, R. H. (2000). Analysis of aberrant virulence of Gibberella zeae following transformation-mediated complementation of a trichothecene-deficient (Tri5) mutant. Microbiology, 146, 2059–2068.

    Article  CAS  PubMed  Google Scholar 

  • Erik, L., Karenr, B., & Sonjas, K. (2009). Identification of up-regulated genes during zearalenone biosynthesis in fusarium. European Journal of Plant Pathology, 122(4), 505–516.

    Google Scholar 

  • Gale, L. R., Chen, L.-F., Hernick, C., Takamura, K., & Kistler, H. (2002). Population analysis of fusarium graminearum from wheat fields in eastern China. Phytopathology, 92, 1315–1322.

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa, N., Noda, Y., Tanaka, Y., & Niwa, S. (2009). Kinesin superfamily motor proteins and intracellular transport. Nature Reviews Molecular Cell Biology, 10(10), 682–696.

    Article  CAS  PubMed  Google Scholar 

  • Kull, F. J., Sablin, E. P., Lau, R., Fletterick, R. J., & Vale, R. D. (1996). Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature, 380(6574), 550.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H. K., Diao, Y. M., Wang, H. X., Chen, C. J., Ni, J. P., & Zhou, M. G. (2008). JS399-19, a new fungicide against wheat scab. Crop Protection, 27, 90–95.

    Article  CAS  Google Scholar 

  • López-Berges, M. S., Rispail, N., Prados-Rosales, R. C., & Di Pietro, A. (2010). A nitrogen response pathway regulates virulence functions in fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. The Plant Cell, 22, 2459–2475.

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo, J., Vallen, E. A., Dravis, C., Tcheperegine, S. E., Drees, B., & Bi, E. (2004). Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. Journal of Cell Biology, 165(6), 843–855.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller, J. D., Taylor, A., & Greenhalgh, R. (1983). Production ofdeoxynivalenol and related compounds in liquid cultureby fusarium graminearum. Canadian Journal of Microbiology, 29, 1171–1178.

    Article  CAS  Google Scholar 

  • Min, K., Shin, Y., Son, H., Lee, J., Kim, J.-C., Choi, G. J., & Lee, Y.-W. (2012). Functional analyses of the nitrogen regulatory gene areA in Gibberella zeae. FEMS Microbiology Letters, 334, 66–73.

    Article  CAS  PubMed  Google Scholar 

  • Motoyama, T., Hayashi, T., Hirota, H., Ueki, M., & Osada, H. (2012). Terpendole E, a kinesin Eg5 inhibitor, is a key biosynthetic intermediate of Indole-Diterpenes in the producing fungus Chaunopycnis alba. Chemistry & Biology, 19(12), 1611–1619.

    Article  CAS  Google Scholar 

  • Niessen, L. (2007). PCR-based diagnosis and quantification of mycotoxin producing fungi. International Journal of Food Microbiology, 119, 38–46.

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell, K., Ward, T. J., Geiser, D. M., Kistler, H. C., & Aoki, T. (2004). Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the fusarium graminearum clade. Fungal Genetics and Biology, 41, 600–623.

    Article  PubMed  Google Scholar 

  • Placinta, C., D'mello, J., & Macdonald, A. (1999). A review of worldwide contamination of cereal grains and animal feed with fusarium mycotoxins. Animal Feed Science and Technology, 78, 21–37.

    Article  CAS  Google Scholar 

  • Proctor, R. H., Hohn, T. M., & McCormick, S. P. (1995). Reduced virulence of Gibberella zeae caused by disruption of a trichthecine toxin biosynthetic gene. MPMI-Molecular Plant Microbe Interactions, 8, 593–601.

    Article  CAS  Google Scholar 

  • Rosen, L., Chen, L. C., et al. (2010). Abstract 2750: ARQ 621, a novel potent and selective inhibitor of Eg5: preclinical data and early results from a clinical phase 1 study. Cancer Research, 70(8 Supplement), 2750–2750.

    Article  Google Scholar 

  • Schuchardt, I., Assmann, D., Thines, E., Schuberth, C., & Steinberg, G. (2005). Myosin-V, kinesin-1, and kinesin-3 cooperate in hyphal growth of the fungus Ustilago maydis. Molecular Biology of the Cell, 16(11), 5191–5201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seong, K. Y., et al. (2009). Global gene regulation by fusarium transcription factors Tri6 and Tri10 reveals adaptations for toxin biosynthesis. Molecular Microbiology, 72, 354–367.

    Article  CAS  PubMed  Google Scholar 

  • Starkey, D. E., et al. (2007). Global molecular surveillance reveals novel fusarium head blight species and trichothecene toxin diversity. Fungal Genetics and Biology, 44, 1191–1204.

    Article  CAS  PubMed  Google Scholar 

  • Tóth, B., Mesterházy, Á., Horváth, Z., Bartók, T., Varga, M., & Varga, J. (2005). Genetic variability of central European isolates of the fusarium graminearum species complex. European Journal of Plant Pathology, 113, 35–45.

    Article  Google Scholar 

  • Trail, F. (2009). For blighted waves of grain: fusarium graminearum in the postgenomics era. Plant Physiology, 149, 103–110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Liu, W., Hou, Z., Wang, C., Zhou, X., Jonkers, W., Ding, S., Kistler, H. C., & J-R, X. (2011). A novel transcriptional factor important for pathogenesis and ascosporogenesis in fusarium graminearum. Molecular Plant-Microbe Interactions, 24, 118–128.

    Article  CAS  PubMed  Google Scholar 

  • Windels, C. E. (2000). Economic and social impacts of fusarium head blight: changing farms and rural communities in the northern great plains. Phytopathology, 90, 17–21.

    Article  CAS  PubMed  Google Scholar 

  • Wu, A.-B., Li, H.-P., Zhao, C.-S., & Liao, Y.-C. (2005). Comparative pathogenicity of fusarium graminearum isolates from China revealed by wheat coleoptile and floret inoculations. Mycopathologia, 160, 75–83.

    Article  PubMed  Google Scholar 

  • Xu, X.-M., et al. (2008). Within-field variability of fusarium head blight pathogens and their associated mycotoxins. European Journal of Plant Pathology, 120, 21–34.

    Article  CAS  Google Scholar 

  • Zhang, J.-B., Li, H.-P., Dang, F.-J., Qu, B., Y-B, X., Zhao, C.-S., & Liao, Y.-C. (2007). Determination of the trichothecene mycotoxin chemotypes and associated geographical distribution and phylogenetic species of the fusarium graminearum clade from China. Mycological Research, 111, 967–975.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C., Chen, Y., Yin, Y., et al. (2015). A small molecule species specifically inhibits Fusarium myosin I. Environmental Microbiology, 17(8), 2735–2746.

  • Zheng, Z., Gao, T., Zhang, Y., Hou, Y., Wang, J., & Zhou, M. (2014). FgFim, a key protein regulating resistance to the fungicide JS399-19, asexual and sexual development, stress responses and virulence in fusarium graminearum. Molecular Plant Pathology, 15, 488–499.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, Z., Hou, Y., Cai, Y., Zhang, Y., Li, Y., & Zhou, M. (2015). Whole-genome sequencing reveals that mutations in myosin-5 confer resistance to the fungicide phenamacril in fusarium graminearum. Scientific Reports, 5, 82–48.

    Google Scholar 

  • Zheng, Z., Liu, X., Li, B., Cai, Y., Zhu, Y., & Zhou, M. (2016). Myosins FaMyo2B and FaMyo2 AffectAsexual and sexual development, ReducesPathogenicity, and FaMyo2B acts jointly with the myosin passenger protein FaSmy1 to affect resistance to phenamacril in fusarium asiaticum. PloS One, 11(4), e0154058. doi:10.1371/journal.pone.0154058.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was funded by the National Natural Science Foundation of China (31572025), the Fund for Independent Innovation of Agricultural Science and Technology in Jiangsu Province of China (CX(15)1001) and the Special Fund for Agro-scientific Research in the Public Interest of China (201303023).

Author’s contributions

Conceived and designed the experiments: MGZ XML. Performed the experiments: XML ZTZ BL YQC. Analyzedthe data: XML ZTZ. Wrote the paper: XML MGZ.

Author information

Authors and Affiliations

  1. College of Plant Protection, State & Local Joint Engineering Research Center of Green Pesticide Invention and Application, Nanjing Agricultural University, Nanjing, Jiangsu Province, 210095, China

    Xiumei Liu, Zhitian Zheng, Bin Li, Yiqiang Cai, Xuewei Mao & Mingguo Zhou

Authors
  1. Xiumei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhitian Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yiqiang Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xuewei Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mingguo Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mingguo Zhou.

Additional information

Xiumei Liu and Zhitian Zheng made the same contribution to this report.

Electronic supplementary material

Table S1

(DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Zheng, Z., Li, B. et al. A myosin passenger protein gene (FaSmy1) is an essential regulator of cell development, pathogenicity, DON biosynthesis, and resistance to the fungicide phenamacril in Fusarium asiaticum . Eur J Plant Pathol 148, 709–722 (2017). https://doi.org/10.1007/s10658-016-1129-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-016-1129-x

Keywords

Search

Navigation