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Expression difference of P450–1 and P450–4 between G- and F-groups of Fusarium fujikuroi

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Abstract

Fusarium fujikuroi is the pathogen of rice bakanae disease and has been intensively studied for gibberellin (GA) production. F. fujikuroi is phylogenetically subclassified into G- and F-groups, which differ in GA and fumonisin production. A higher amount of GA is produced by the G-group than the F-group. A previous study found that the GA production difference between the G-group strain Gfc0801001 and the F-group strain Gfc0825009 was due to the GA gene cluster. In this study, higher expression of P450–1 and P450–4 in the GA gene cluster were detected in G-group strains than in F-group strains. The nucleotide sequence of the bidirectional promoter region between P450–1 and P450–4 and expression of P450–1 and P450–4 were compared between G- and F-group strains. The promoter sequence was identical among G-group strains while nucleotide substitutions were detected at various locations in F-group strains. Most F-group strains did not share the same substitutions. These results combined with the ancestral position of the F-group in the phylogenetic tree suggest that the population carrying highly expressed sequence generates the G-group rather than the low expression of P450–1 and P450–4 in the F-group due to a specific mutation occured in G-group.

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References

  • Bacon, C. W., Porter, J. K., Norred, W. P., & Leslie, J. F. (1996). Production of fusaric acid by Fusarium species. Applied and Environmental Microbiology, 62(11), 4039–4043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao, W. X., Nakasaga, T., Inagaki, S., Tatabayashi, S., Imazaki, I., Fuji, S., et al. (2020). A single gene transfer of gibberellin biosynthesis gene cluster increases gibberellin production in a Fusarium fujikuroi strain with gibberellin low producibility. Plant Pathology, 69, 901–910.

    Article  CAS  Google Scholar 

  • Barrero, A. F., Sánchez, J. F., Oltra, J. E., Tamayo, N., Cerdá-Olmedo, E., Candau, R., et al. (1991). Fusarin C and 8Z-fusarin C from Gibberella fujikuroi. Phytochemistry, 30(7), 2259–2263.

    Article  CAS  Google Scholar 

  • Busman, M., Desjardins, A. E., & Proctor, R. H. (2012). Analysis of fominisin contamination and presence of Fusarium in wheat with kernel black point disease in the United States. Food Additives & Contaminants: Part A, 29(7), 1092–1100.

    Article  CAS  Google Scholar 

  • Fox, E. M., & Howlett, B. J. (2008). Secondary metabolism: Regulation and role in fungal biology. Current Opinion in Microbiology, 11(6), 481–487.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, A. K., Solanki, I. S., Bashyal, B. M., Singh, Y., & Srivastava, K. (2015). Bakanae of rice-an emerging disease in Asia. Journal of Animal & Plant Science, 25(6), 1499–1514.

    CAS  Google Scholar 

  • Hedden, P., Phillips, A. L., Rojas, M. C., Carrera, E., & Tudzynski, B. (2001). Gibberellin biosynthesis in plants and fungi: A case of convergent evolution? Journal of Plant Growth Regulation, 20(4), 319–331.

    Article  CAS  PubMed  Google Scholar 

  • Imazaki, I., & Kadota, I. (2015). Molecular phylogeny and diversity of Fusarium endophytes isolated from tomato stems. FEMS Microbiology Ecology, 91, 1–15.

    Article  Google Scholar 

  • Ito, S., & Shimada, S. (1931). On the nature of the growth promoting substance excreted by the “bakanae” fungus. Japanese Journal of Phytopathology, 2(4), 322–338.

    Article  Google Scholar 

  • Keyser, K., Vismer, H. F., Klaasen, J. A., Snjiman, P. W., & Marasas, W. F. O. (1999). The antifungal effect of fumonisin B1 on Fusarium and other fungal species. South African Journal of Science, 95, 455–458.

    CAS  Google Scholar 

  • Kvas, M., Marasas, W. F. O., Wingfield, B. D., Wingfield, M. J., & Steenkamp, E. T. (2009). Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Diversity, 34, 1–21.

    Google Scholar 

  • Malonek, S., & Tudzynski, B. (2003). Evolutionary aspects of gibberellin biosynthesis in the Gibberella fujikuroi species complex. Fungal Genetics Newsletter, 50, 140.

    Google Scholar 

  • Malonek, S., Bömke, C., Bornberg-Bauer, E., Rojas, M. C., Hedden, P., Hopkins, P., & Tudzynski, B. (2005a). Distribution of gibberellin biosynthetic genes and gibberellin production in the Gibberella fujikuroi species complex. Phytochemistry, 66(11), 1296–1311.

    Article  CAS  PubMed  Google Scholar 

  • Malonek, S., Rojas, M. C., Hedden, P., Gaskin, P., Hopkins, P., & Tudzynski, B. (2005b). Functional characterization of two cytochrome P450 monooxygenase genes, P450–1 and P450–4, of the gibberellic acid gene cluster in Fusarium proliferatum (Gibberella fujikuroi MP-D). Applied and Environmental Microbiology, 71(3), 1462–1472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michielse, C. B., Pfannmüller, A., Macios, M., Rengers, P., Dzikowska, A., & Tudzynski, B. (2014). The interplay between the GATA transcription factors AreA, the global nitrogen regulator and AreB in Fusarium fujikuroi. Molecular Microbiology, 91(3), 472–493.

    Article  CAS  PubMed  Google Scholar 

  • Mihlan, M., Homann, V., Liu, T. W., & Tudzynski, B. (2003). AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Molecular Microbiology, 47(4), 975–991.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, P. E. (1992). Taxonomy and biology of Fusarium moniliforme. Mycopathologia, 117, 29–36.

    Article  CAS  PubMed  Google Scholar 

  • Niehaus, E.-M., Kim, H.-K., Münsterkötter, M., Janevska, S., Arndt, B., Kalinina, S. A., et al. (2017). Comparative genomics of geographically distant Fusarium fujikuroi isolates revealed two distinct pathotypes correlating with secondary metabolite profiles. PLoS Pathogens, 13, e1006670.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Donnell, K., Cigelnik, E., & Nirenberg, H. I. (1998). Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia, 90(3), 465–493.

    Article  Google Scholar 

  • Prado-Cabrero, A., Schaub, P., Díaz-Sánchez, V., Estrada, A. F., Al-Babili, S., & Avalos, J. (2009). Deviation of the neurosporaxanthin pathway towards β-carotene biosynthesis in Fusarium fujikuroi by a point mutation in the phytoene desaturase gene. The FEBS Journal, 276(16), 4582–4597.

    Article  CAS  PubMed  Google Scholar 

  • Proctor, R. H., Plattner, R. D., Brown, D. W., Seo, J. A., & Lee, Y. W. (2004). Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycological Research, 108(7), 815–822.

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Oriz, R., Limn, M. C., & Avalos, J. (2009). Regulation of carotenogenesis and secondary metabolism by nitrogen in wild-type Fusarium fujikuroi and carotenoid-overproducing mutants. Applied and Environmental Microbiology, 75(2), 405–413.

    Article  Google Scholar 

  • Rojas, M. C., Urrutia, O., Cruz, C., Gaksin, P., Tudzynski, B., & Hedden, P. (2001). Kaurenolides and fujunoic acids are side products of the gibberellin P450-1 monooxygenase in Gibberella fujikuroi. Phytochemistry, 65(7), 821–830.

    Article  Google Scholar 

  • Rosewich, U. L., & Kistler, H. C. (2000). Role of horizontal gene transfer in the evolution of fungi. Annual Review of Phytopathology, 38, 325–363.

    Article  CAS  PubMed  Google Scholar 

  • Smith, K. M., Phatale, P. A., Bredeweg, E. L., Pomraning, K. R., & Freitag, M. (2012). Epigenetics of filamentous fungi. In R. A. Meyers (Ed.), Epigenetics of filamentous Fungi (pp. 1063–1107). Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA.

    Google Scholar 

  • Strauss, J., & Reyes-Dominguez, Y. (2011). Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genetics and Biology, 48(1), 62–69.

    Article  CAS  PubMed  Google Scholar 

  • Studt, L., & Tudzynski, B. (2014). Gibberellins and the red pigments bikaverin and fusarubin. In J.-F. Martín, S. Zeilinger, & C. García-Estrada (Eds.), Biosynthesis and molecular genetics of fungal secondary metabolites (pp. 209–238). Berlin: Springer Science.

    Google Scholar 

  • Studt, L., Wiemann, P., Kleigrewe, K., Humpf, H. U., & Tudzynski, B. (2012). Biosynthesis of fusarubins accounts for pigmentation of Fusarium fujikuroi perithecia. Applied and Environmental Microbiology, 78(12), 4460–4480.

    Article  Google Scholar 

  • Suga, H., Karugia, G. W., Ward, T., Gale, L. R., Tomimura, K., Nakajima, T., Miyasaka, A., Koizumi, S., Kageyama, K., & Hyakumachi, M. (2008). Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology, 98(2), 159–166.

    Article  CAS  PubMed  Google Scholar 

  • Suga, H., Kitajima, M., Nagumo, R., Tsukiboshi, T., Uegaki, R., Nakajima, T., et al. (2014). A single nucleotide polymorphism in the translation elongation factor 1α gene correlates with ability to produce fumonisin in Japanese Fusarium fujikuroi. Fungal Biology, 118, 402–412.

    Article  CAS  PubMed  Google Scholar 

  • Suga, H., Arai, M., Fukasawa, E., Motohashi, K., Nakagawa, H., Tateishi, H., et al. (2019). Genetic differentiation associated with fumonisin and gibberellin production in Japanese Fusarium fujikuroi. Applied and Environmental Microbiology, 85(1), e02414–e04218.

    CAS  PubMed  Google Scholar 

  • Tateishi, H., & Chida, T. (2000). Sensitivity of Fusarium moniliforme isolates to ipconazole. Journal of General Plant Pathology, 66(4), 353–359.

    Article  CAS  Google Scholar 

  • Tudzynski, B., & Hӧler, K. (1998). Gibberellin biosynthetic pathway in Gibberella fujikuroi: Evidence for a gene cluster. Fungal Genetics and Biology, 25(3), 157–170.

    Article  CAS  PubMed  Google Scholar 

  • Tudzynski, B., Homann, V., Feng, B., & Marzluf, G. A. (1999). Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Molecular and General Genetics, 261(1), 106–114.

    Article  CAS  PubMed  Google Scholar 

  • Tudzynski, B., Rojas, M. C., Gaksin, P., & Hedden, P. (2002). The gibberellin 20-oxidase of gibberella fujikuroi is a multifunctional monooxygenase. Journal of Biological Chemistry, 277(24), 21246–21253.

    Article  CAS  Google Scholar 

  • Tudzynski, B., Mihlan, M., Rojas, M. C., Linnemannstӧns, P., Gaskin, P., & Hedden, P. (2003). Characterization of the final two genes of the gibberellin biosynthesis gene cluster of Gibberella fujikuroi. Journal of Biological Chemistry, 278(31), 28635–28643.

    Article  CAS  Google Scholar 

  • Wiemann, P., Seiber, C. M. K., Bargen, K. W., Studt, L., Niehuas, E.-M., Espino, J. J., et al. (2013). Deciphering the cryptic genome: Genome-wide analyses of rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathogens, 9, e1003475.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Tomomi Katsu (Gifu University, Japan) and Ayako Usui (Gifu University, Japan) for technical support.

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The datasets generated during the current study are available from the corresponding author on reasonable request.

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Correspondence to H. Suga.

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Bao, W.X., Inagaki, S., Tatebayashi, S. et al. Expression difference of P450–1 and P450–4 between G- and F-groups of Fusarium fujikuroi. Eur J Plant Pathol 159, 27–36 (2021). https://doi.org/10.1007/s10658-020-02133-3

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