Transformation of filamental fungi by Agrobacterium: Histoplasma as a model

Authors

DOI:

https://doi.org/10.33448/rsd-v11i7.29427

Keywords:

Molecular biology; Silencing; Virulence.

Abstract

Histoplasma is a pathogenic fungus that causes histoplasmosis, an endemic systemic mycosis due to the occurrence/positivity in specific regions. The virulence of this fungus has been revealed in recent years, aided by the techniques of functional gene characterization, which use gene inactivation, by deletion, or decrease in the production of gene products. Molecular tools for gene transformation, such as Agrobacterium-mediated transformations (ATMT), which favor the formation of RNA interference, have ensured the expansion of knowledge about virulence mechanisms implemented by different pathogenic microorganisms, such as H. capsulatum. In ATMT, a DNA fragment is introduced into the target cell when the bacterium is stimulated by chemical signals. DNA integrates into the genome and provides gene silencing via RNAi, a method of reducing the gene product, due to mRNA degradation, through the formation or introduction of a double-stranded RNA molecule into the target host, which are abhorred by cells eukaryotic. For Histoplasma, the ability of double-stranded RNAs, introduced by the ATMT technique, to trigger depletion of many target genes has been widely demonstrated, and so far has favored a better understanding of the metabolic flexibility of this pathogen.

References

Bakó, L., Umeda, M., Tiburcio, A. F., Schell, J., & Koncz, C. (2003). The VirD2 pilot protein of Agrobacterium-transferred DNA interacts with the TATA box-binding protein and a nuclear protein kinase in plants. Proc Natl Acad Sci U S A. 100(17):10108-13. 10.1073/pnas.1733208100.

Bundock, P., Den Dulk-Ras, A., Beijersbergen, A., & Hooykaas, P. J. (1995). Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J. 14(13):3206-14.

Cangelosi, G. A., Ankenbauer, R. G., & Nester, E. W. (1990). Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. Proc Natl Acad Sci U S A. 87(17):6708-12. 10.1073/pnas.87.17.6708

Citovsky, V., Wong, M. L., & Zambryski, P. (1989). Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: implications for the T-DNA transfer process. Proc Natl Acad Sci U S A. 86(4):1193-7. 10.1073/pnas.86.4.1193.

Falkow, S. (1988). Molecular Koch's postulates applied to microbial pathogenicity. Rev Infect Dis. 10 Suppl 2:S274-6. 10.1093/cid/10.supplement_2.s274.

Fullner, K. J., & Nester, E. W. (1996). Temperature affects the T-DNA transfer machinery of Agrobacterium tumefaciens. J Bacteriol. 178(6):1498-504. 10.1128/jb.178.6.1498-1504.1996.

Garfoot, A. L., Zemska, O., & Rappleye, C. A. (2014). Histoplasma capsulatum depends on de novo vitamin biosynthesis for intraphagosomal proliferation. Infect Immun. 82(1):393-404. 10.1128/IAI.00824-13.

Geley, S., & Müller, C. (2004). RNAi: ancient mechanism with a promising future. Exp Gerontol. Jul;39(7):985-98. 10.1016/j.exger.2004.03.040.

Hooykaas, P. J. J., Van Heusden, G. P. H., Niu, X., Reza Roushan, M., Soltani, J., Zhang, X., & Van Der Zaal, B. J. (2018). Agrobacterium-Mediated Transformation of Yeast and Fungi. Curr Top Microbiol Immunol. 418:349-374.

Hutvágner, G., & Zamore, P. D. (2002). RNAi: nature abhors a double-strand. Curr Opin Genet Dev. 12(2):225-32. 10.1016/s0959-437x(02)00290-3.

Kado, C. I. (2000). The role of the T-pilus in horizontal gene transfer and tumorigenesis. Curr Opin Microbiol. 3(6):643-8. 10.1016/s1369-5274(00)00154-5.

Kemski, M. M, Stevens, B., & Rappleye, C. A. (2013). Spectrum of T-DNA integrations for insertional mutagenesis of Histoplasma capsulatum. Fungal Biol. 117(1):41-51. 10.1016/j.funbio.2012.11.004.

Kügler, S., Young, B., Miller, V. L., & Goldman, W. E. (2000). Monitoring phase-specific gene expression in Histoplasma capsulatum with telomeric GFP fusion plasmids. Cell Microbiol. 2(6):537-47. 10.1046/j.1462-5822.2000.00078.x.

Longo, L. V. G., Ray, S. C., Puccia, R., & Rappleye, C. A. (2018). Characterization of the APSES-family transcriptional regulators of Histoplasma capsulatum. FEMS Yeast Res. 18(8): foy087. 10.1093/femsyr/foy087.

Marion, C. L., Rappleye, C. A., Engle, J. T., & Goldman, W. E. (2006). An alpha-(1,4)-amylase is essential for alpha-(1,3)-glucan production and virulence in Histoplasma capsulatum. Mol Microbiol. 62(4):970-83. 10.1111/j.1365-2958.2006.05436.x.

Michielse, C. B., Hooykaas, P. J., Van Den Hondel, C. A., & Ram, A. F. (2008). Agrobacterium-mediated transformation of the filamentous fungus Aspergillus awamori. Nat Protoc. 3(10):1671-8. 10.1038/nprot.2008.154.

Mullins, E. D., Chen, X., Romaine, P., Raina, R., Geiser, D.M., & Kang, S. (2001). Agrobacterium-Mediated Transformation of Fusarium oxysporum: An Efficient Tool for Insertional Mutagenesis and Gene Transfer. Phytopathology. 91(2):173-80. 10.1094/PHYTO.2001.91.2.173.

Rappleye, C. A., Engle, J. T., & Goldman, W. E. (2004). RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol. 53(1):153-65. 10.1111/j.1365-2958.2004.04131.x.

Regensburg-Tuïnk, A. J., & Hooykaas, P. J. (1993). Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens. Nature. 363(6424):69-71. 10.1038/363069a0.

Sebghati, T. S., Engle, J. T., & Goldman, W. E. (2000). Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science. 290(5495):1368-72. 10.1126/science.290.5495.1368.

Shen, Q., Beucler, M. J., Ray, S. C., & Rappleye, C. A. (2018). Macrophage activation by IFN-γ triggers restriction of phagosomal copper from intracellular pathogens. PLoS Pathog. 14(11):e1007444. 10.1128/MCB.21.2.534-547.2001.

Sullivan, T. D., Rooney, P. J., & Klein, B. S. (2002). Agrobacterium tumefaciens integrates transfer DNA into single chromosomal sites of dimorphic fungi and yields homokaryotic progeny from multinucleate yeast. Eukaryot Cell. Dec;1(6):895-905. 10.1128/EC.1.6.895-905.2002.

Toro, N., Datta, A., Yanofsky, M., & Nester, E. (1988). Role of the overdrive sequence in T-DNA border cleavage in Agrobacterium. Proc Natl Acad Sci U S A. 85(22):8558-62. 10.1073/pnas.85.22.8558.

Turk, S. C., Melchers, L. S., Den Dulk-Ras, H., Regensburg-Tuïnk, A. J., & Hooykaas, P. J. (1991). Environmental conditions differentially affect vir gene induction in different Agrobacterium strains. Role of the VirA sensor protein. Plant Mol Biol. 16(6):1051-9. 10.1007/BF00016076.

Vijn, I., & Govers, F. (2003). Agrobacterium tumefaciens mediated transformation of the oomycete plant pathogen Phytophthora infestans. Mol Plant Pathol. 4(6):459-67. 10.1046/j.1364-3703.2003.00191.x.

Woods, J. P., Heinecke, E. L., & Goldman, W. E. (1998). Electrotransformation and expression of bacterial genes encoding hygromycin phosphotransferase and beta-galactosidase in the pathogenic fungus Histoplasma capsulatum. Infect Immun. 66(4):1697-707. 10.1128/IAI.66.4.1697-1707.1998.

Worsham, P. L., & Goldman, W. E. (1990). Development of a genetic transformation system for Histoplasma capsulatum: complementation of uracil auxotrophy. Mol Gen Genet. 221(3):358-62. 10.1007/BF00259400.

Youseff, B. H., & Rappleye, C. A. (2012). RNAi-based gene silencing using a GFP sentinel system in Histoplasma capsulatum. Methods Mol Biol. 845:151-64. 10.1007/978-1-61779-539-8_10.

Zupan, J., Muth, T. R., Draper, O., & Zambryski, P. (2000). The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J. 23(1):11-28. 10.1046/j.1365-313x.2000.00808.x.

Published

17/05/2022

How to Cite

MORAES, D. Transformation of filamental fungi by Agrobacterium: Histoplasma as a model. Research, Society and Development, [S. l.], v. 11, n. 7, p. e12211729427, 2022. DOI: 10.33448/rsd-v11i7.29427. Disponível em: https://www.rsdjournal.org/index.php/rsd/article/view/29427. Acesso em: 19 apr. 2024.

Issue

Section

Review Article