Advertisement

The velvet repressed vidA gene plays a key role in governing development in Aspergillus nidulans

  • Min-Ju Kim
  • Won-Hee Jung
  • Ye-Eun Son
  • Jae-Hyuk Yu
  • Mi-Kyung Lee
  • Hee-Soo ParkEmail author
Article
  • 39 Downloads

Abstract

Fungal development is regulated by a variety of transcription factors in Aspergillus nidulans. Previous studies demonstrated that the NF-κB type velvet transcription factors regulate certain target genes that govern fungal differentiation and cellular metabolism. In this study, we characterize one of the VosA/VelB-inhibited developmental genes called vidA, which is predicted to encode a 581-amino acid protein with a C2H2 zinc finger domain at the C-terminus. Levels of vidA mRNA are high during the early and middle phases of asexual development and decrease during the late phase of asexual development and asexual spore (conidium) formation. Deletion of either vosA or velB results in increased vidA mRNA accumulation in conidia, suggesting that vidA transcript accumulation in conidia is repressed by VosA and VelB. Phenotypic analysis demonstrated that deletion of vidA causes decreased colony growth, reduced production of asexual spores, and abnormal formation of sexual fruiting bodies. In addition, the vidA deletion mutant conidia contain more trehalose and β-glucan than wild type. Overall, these results suggest that VidA is a putative transcription factor that plays a key role in governing proper fungal growth, asexual and sexual development, and conidia formation in A. nidulans.

Keywords

asexual development velvet beta-glucan Aspergillus nidulans 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

The work by HSP was supported by the National Research Foundation of Korea (NRF) grant to HSP funded by the Korean government (NRF-2016R1C1B2010945). The work at UW-Madison (JHY) was primarily supported by the Intelligent Synthetic Biology Center of Global Frontier Project funded by the Ministry of Education, Science and Technology of Korea (No. 2011-0031955). The work by MKL was supported by the KRIBB Research Initiative Program (KGM-5231921).

Supplementary material

12275_2019_9214_MOESM1_ESM.pdf (3.5 mb)
Supplemental Materials

References

  1. Adams, T.H., Boylan, M.T., and Timberlake, W.E. 1988. brlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans. Cell 54, 353–362.CrossRefGoogle Scholar
  2. Adams, T.H., Deising, H., and Timberlake, W.E. 1990. brlA requires both zinc fingers to induce development. Mol. Cell. Biol. 10, 1815–1817.CrossRefGoogle Scholar
  3. Adams, T.H., Wieser, J.K., and Yu, J.H. 1998. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62, 35–54.Google Scholar
  4. Ahmed, Y.L., Gerke, J., Park, H.S., Bayram, O., Neumann, P., Ni, M., Dickmanns, A., Kim, S.C., Yu, J.H., Braus, G.H., et al. 2013. The velvet family of fungal regulators contains a DNA-binding domain structurally similar to NF-κB. PLoS Biol. 11, e1001750.CrossRefGoogle Scholar
  5. Andrianopoulos, A. and Timberlake, W.E. 1991. ATTS, a new and conserved DNA binding domain. Plant Cell 3, 747–748.Google Scholar
  6. Andrianopoulos, A. and Timberlake, W.E. 1994. The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol. Cell. Biol. 14, 2503–2515.CrossRefGoogle Scholar
  7. Bayram, O.S., Bayram, O., Valerius, O., Park, H.S., Irniger, S., Gerke, J., Ni, M., Han, K.H., Yu, J.H., and Braus, G.H. 2010. LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet. 6, e1001226.CrossRefGoogle Scholar
  8. Bayram, O. and Braus, G.H. 2012. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol. Rev. 36, 1–24.CrossRefGoogle Scholar
  9. Boylan, M.T., Mirabito, P.M., Willett, C.E., Zimmerman, C.R., and Timberlake, W.E. 1987. Isolation and physical characterization of three essential conidiation genes from Aspergillus nidulans. Mol. Cell. Biol. 7, 3113–3118.CrossRefGoogle Scholar
  10. Casselton, L. and Zolan, M. 2002. The art and design of genetic screens: filamentous fungi. Nat. Rev. Genet. 3, 683–697.CrossRefGoogle Scholar
  11. Chang, Y.C. and Timberlake, W.E. 1993. Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 133, 29–38.Google Scholar
  12. de Vries, R.P., Riley, R., Wiebenga, A., Aguilar-Osorio, G., Amillis, S., Uchima, C.A., Anderluh, G., Asadollahi, M., Askin, M., Barry, K., et al. 2017. Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biol. 18, 28.CrossRefGoogle Scholar
  13. Dyer, P.S. and O’Gorman, C.M. 2012. Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol. Rev. 36, 165–192.CrossRefGoogle Scholar
  14. Fesel, P.H. and Zuccaro, A. 2016. β-Glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genet. Biol. 90, 53–60.CrossRefGoogle Scholar
  15. Fillinger, S., Chaveroche, M.K., van Dijck, P., de Vries, R., Ruijter, G., Thevelein, J., and d’Enfert, C. 2001. Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology 147, 1851–1862.CrossRefGoogle Scholar
  16. Han, K.H. 2009. Molecular genetics of Emericella nidulans sexual development. Mycobiology 37, 171–182.CrossRefGoogle Scholar
  17. Harris, S.D. 2011. Hyphal morphogenesis: an evolutionary perspective. Fungal Biol. 115, 475–484.CrossRefGoogle Scholar
  18. Kafer, E. 1977. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv. Genet. 19, 33–131.CrossRefGoogle Scholar
  19. Kwon, N.J., Shin, K.S., and Yu, J.H. 2010. Characterization of the developmental regulator FlbE in Aspergillus fumigatus and Aspergillus nidulans. Fungal Genet. Biol. 47, 981–993.CrossRefGoogle Scholar
  20. Lee, M.K., Park, H.S., Han, K.H., Hong, S.B., and Yu, J.H. 2017. High molecular weight genomic DNA mini-prep for filamentous fungi. Fungal Genet. Biol. 104, 1–5.CrossRefGoogle Scholar
  21. Marshall, M.A. and Timberlake, W.E. 1991. Aspergillus nidulans wetA activates spore-specific gene expression. Mol. Cell. Biol. 11, 55–62.CrossRefGoogle Scholar
  22. Martinelli, S.D. 1994. Aspergillus nidulans as an experimental organism. Prog. Ind. Microbiol. 29, 33–58.Google Scholar
  23. Mirabito, P.M., Adams, T.H., and Timberlake, W.E. 1989. Interactions of three sequentially expressed genes control temporal and spatial specificity in Aspergillus development. Cell 57, 859–868.CrossRefGoogle Scholar
  24. Ojeda-López, M., Chen, W., Eagle, C.E., Gutiérrez, G., Jia, W.L., Swilaiman, S.S., Huang, Z., Park, H.S., Yu, J.H., Cánovas, D., et al. 2018. Evolution of asexual and sexual reproduction in the aspergilli. Stud. Mycol. 91, 37–59.CrossRefGoogle Scholar
  25. Park, H.S., Lee, M.K., Han, K.H., Kim, M.J., and Yu, J.H. 2019. Developmental decisions in Aspergillus nidulans, pp. 63–80. In Hoffmeister, D. and Gressler, M. (eds.), Biology of the fungal cell. Springer, Cham.CrossRefGoogle Scholar
  26. Park, H.S., Lee, M.K., Kim, S.C., and Yu, J.H. 2017. The role of VosA/VelB-activated developmental gene vadA in Aspergillus nidulans. PLoS One 12, e0177099.CrossRefGoogle Scholar
  27. Park, H.S., Nam, T.Y., Han, K.H., Kim, S.C., and Yu, J.H. 2014. VelC positively controls sexual development in Aspergillus nidulans. PLoS One 9, e89883.CrossRefGoogle Scholar
  28. Park, H.S., Ni, M., Jeong, K.C., Kim, Y.H., and Yu, J.H. 2012. The role, interaction and regulation of the velvet regulator VelB in Aspergillus nidulans. PLoS One 7, e45935.CrossRefGoogle Scholar
  29. Park, H.S. and Yu, J.H. 2012a. Genetic control of asexual sporulation in filamentous fungi. Curr. Opin. Microbiol. 15, 669–677.CrossRefGoogle Scholar
  30. Park, H.S. and Yu, J.H. 2012b. Multi-copy genetic screen in Aspergillus nidulans. Methods Mol. Biol. 944, 183–190.Google Scholar
  31. Park, H.S. and Yu, J.H. 2016a. Molecular biology of asexual sporulation in filamentous fungi. In Hoffmeister, D. (ed.), Biochemistry and molecular biology. The mycota (A comprehensive treatise on fungi as experimental systems for basic and applied research). Springer, Cham.Google Scholar
  32. Park, H.S. and Yu, J.H. 2016b. Velvet regulators in Aspergillus spp. Microbiol. Biotechnol. Lett. 44, 409–419.CrossRefGoogle Scholar
  33. Park, H.S., Yu, Y.M., Lee, M.K., Maeng, P.J., Kim, S.C., and Yu, J.H. 2015. Velvet-mediated repression of beta-glucan synthesis in Aspergillus nidulans spores. Sci. Rep. 5, 10199.CrossRefGoogle Scholar
  34. Sewall, T.C., Mims, C.W., and Timberlake, W.E. 1990. abaA controls phialide differentiation in Aspergillus nidulans. Plant Cell 2, 731–739.Google Scholar
  35. Shaaban, M.I., Bok, J.W., Lauer, C., and Keller, N.P. 2010. Suppressor mutagenesis identifies a velvet complex remediator of Aspergillus nidulans secondary metabolism. Eukaryot. Cell 9, 1816–1824.CrossRefGoogle Scholar
  36. Shelest, E. 2017. Transcription factors in fungi: TFome dynamics, three major families, and dual-specificity TFs. Front. Genet. 8, 53.CrossRefGoogle Scholar
  37. Timberlake, W.E. 1990. Molecular genetics of Aspergillus development. Annu. Rev. Genet. 24, 5–36.CrossRefGoogle Scholar
  38. Wu, M.Y., Mead, M.E., Kim, S.C., Rokas, A., and Yu, J.H. 2017. WetA bridges cellular and chemical development in Aspergillus flavus. PLoS One 12, e0179571.CrossRefGoogle Scholar
  39. Wu, M.Y., Mead, M.E., Lee, M.K., Loss, E.M.O., Kim, S.C., Rokas, A., and Yu, J.H. 2018. Systematic dissection of the evolutionarily conserved WetA developmental regulator across a genus of filamentous fungi. mBio 9, e01130–18.Google Scholar
  40. Yu, J.H., Hamari, Z., Han, K.H., Seo, J.A., Reyes-Dominguez, Y., and Scazzocchio, C. 2004. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41, 973–981.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea 2019

Authors and Affiliations

  • Min-Ju Kim
    • 1
  • Won-Hee Jung
    • 1
  • Ye-Eun Son
    • 1
  • Jae-Hyuk Yu
    • 2
    • 3
  • Mi-Kyung Lee
    • 4
  • Hee-Soo Park
    • 1
    Email author
  1. 1.School of Food Science and Biotechnology, Institute of Agricultural Science and TechnologyKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Departments of Bacteriology and GeneticsUniversity of WisconsinMadisonUSA
  3. 3.Department of Systems BiotechnologyKonkuk UniversitySeoulRepublic of Korea
  4. 4.Biological Resource Center (BRC)Korea Research Institute of Bioscience and Biotechnology (KRIBB)JeongeupRepublic of Korea

Personalised recommendations