Abstract
The life cycle of Ustilago maydis involves alternation of a haploid saprophytic yeast-like stage and a dikaryotic hyphal virulent form. Under in vitro conditions, basidiocarps are formed. Analysis of the transcriptional network of basidiocarp formation revealed the possible involvement of a Tec transcription factor (Tec1, UMAG_02835) in the process. In some Ascomycota, Tec factors are involved in mycelial formation, pathogenesis, and interaction with other regulatory elements, but their role in Basidiomycota species is almost unknown. Accordingly, we proceeded to determine the role of this gene in U. maydis by its mutation. Tec1 was found to be a crucial factor for normal mating, basidiocarp development, and virulence, all of the functions related to the dikaryotic stage dependent of the b genes, whereas dimorphism and resistance to different stress conditions occurring in the haploid stage were not affected in tec1 mutants. The observation that mutants showed a low residual wild-type phenotype suggests the presence of a secondary mechanism that partially compensates the loss of Tec1.
Similar content being viewed by others
Data availability
Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.
Code availability
No applicable.
References
Andrianopoulos A, Timberlake WE (1991) ATTS, a new and conserved DNA binding domain. Plant Cell 3:747–748. https://doi.org/10.1105/tpc.3.8.747
Banuett F, Herskowitz I (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA 86:5878–5882. https://doi.org/10.1073/pnas.86.15.5878
Banuett F, Herskowitz I (1994) Identification of Fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and–independent steps in the fungal life cycle. Genes Dev 8:1367–1378. https://doi.org/10.1101/gad.8.12.1367
Benhaddou A, Keime C, Ye T, Morlon A, Michel I, Jost B, Mengus G, Davidson I (2012) Transcription factor TEAD4 regulates expression of myogenin and the unfolded protein response genes during C2C12 cell differentiation. Cell Death Differ 19:220–231. https://doi.org/10.1038/cdd.2011.87
Bölker M, Urban M, Kahmann R (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68(3):441–450. https://doi.org/10.1016/0092-8674(92)90182-c
Boylan MT, Mirabito PM, Willet CE, Zimmerman CR, Timberlake WE (1987) Isolation and physical characterization of three essential conidiation genes from Aspergillus nidulans. Mol Cell Biol 7(9):3113–3118. https://doi.org/10.1128/mcb.7.9.3113
Brückner S, Kern S, Birke R, Saugar I, Ulrich HD, Mösch H-U (2011) The TEA transcription factor Tec1 links TOR and MAPK pathways to coordinate yeast development. Genetics 189:479–494. https://doi.org/10.1534/genetics.111.133629
Cabrera-Ponce JL, León-Ramírez CG, Verver-Vargas A, Palma-Tirado L, Ruiz-Herrera J (2012) Metamorphosis of the basidiomycota Ustilago maydis: transformation of yeast-like cells into basidiocarps. Fungal Gen Biol 49:765–771. https://doi.org/10.1016/j.fgb.2012.07.005
Chavez-Ontiveros J, Martinez-Espinoza AD, Ruiz-Herrera J (2000) Double chitin synthetase mutants from the corn smut fungus Ustilago maydis. New Phytol 146:335–341. https://doi.org/10.1046/j.1469-8137.2000.00635.x
Elorza MV, Rico H, Gozalbo D, Sentandreu R (1983) Cell wall composition and protoplast regeneration in Candida albicans. Antoine Van Leewenhoek 49:457–469. https://doi.org/10.1007/BF00399324
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Grünler A, Walther A, Lämmel J, Wendland J (2010) Analysis of flocculins in Ashbya gossypii reveals FIG2 regulation by TEC1. Fungal Gen Biol 47:619–628. https://doi.org/10.1016/j.fgb.2010.04.001
Guo B, Styles CA, Feng Q, Fink GR (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci USA 97(22):12158–12163. https://doi.org/10.1073/pnas.220420397
Hoffman CS, Winston F (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57:267–272. https://doi.org/10.1016/0378-1119(87)90131-4
Holliday R (1974) Ustilago maydis. In: King RC (ed) The handbook of genetics. Plenum Press, New York, pp 575–595
Hwang JJ, Chambon P, Davidson I (1993) Characterization of the transcription activation function and the DNA binding domain of transcriptional enhancer factor-1. J EMBO 12(6):2334–2348. https://doi.org/10.1002/j.1460-2075.1993.tb05888.x
Klose J, de Sá MM, Kronstad JW (2004) Lipid-induced filamentous growth in Ustilago maydis. Mol Microbiol 52:823–835. https://doi.org/10.1111/j.1365-2958.2004.04019.x
Laloux I, Dubois E, Dewerchin M, Jacobs E (1990) Tec1, a gene involved in the activation of Ty1 and Ty1-mediated gene expression in Saccharomyces cerevisiae: cloning and Molecular Analysis. Mol Cell Biol 10(7):3541–3550. https://doi.org/10.1128/MCB.10.7.3541
Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25(7):1307–1320. https://doi.org/10.1093/molbev/msn067
León-Ramírez CG, Cabrera-Ponce JL, Martínez-Soto D, Sánchez-Arreguín JA, Aréchiga-Carvajal E, Ruiz-Herrera J (2017) Transcriptomic analysis of basidiocarps development in Ustilago maydis (CD) Cda. Fungal Gen Biol 101:34–45. https://doi.org/10.1016/j.fgb.2017.02.007
Liu H (2001) Transcriptional control of dimorphism in Candida albicans. Curr Opin Microbiol 4:728–735. https://doi.org/10.1016/S1369-5274(01)00275-2
Mayorga ME, Gold S (1998) Characterization and molecular genetic complementation of mutants affecting dimorphism in the fungus Ustilago maydis. Fungal Gen Biol 24:364–376. https://doi.org/10.1006/fgbi.1998.1078
Monteiro PT, Mendes ND, Teixeira MC, d’Orey S, Tenreiro S, Mira NP, Sa-Correia I (2007) YEASTRACT-DISCOVERER: new tools to improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 36(1):132–136. https://doi.org/10.1093/nar/gkm976
Nobile CJ, Mitchell AP (2005) Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 15:1150–1155. https://doi.org/10.1016/j.cub.2005.05.047
Pobbati AV, Han X, Hung AW, Weiguang S, Huda N, Chen G-Y, Kang CB, Chia CSB, Luo X, Hong W, Poulsen A (2015) Targeting the central pocket in human transcription factor TEAD as a potential cancer therapeutic strategy. Structure 23:1–11. https://doi.org/10.1016/j.str.2015.09.009
Ruiz-Herrera J, León-Ramírez CG, Guevara-Olvera L, Cárabez-Trejo A (1995) Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis. Microbiology 141:695–703. https://doi.org/10.1099/13500872-141-3-695
Sahni N, Yi S, Daniels KJ, Huang G, Srikantha T, Soll DR (2010) Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways. Plos Biol 8(5):e1000363. https://doi.org/10.1371/journal.pbio.1000363
Sánchez-Arreguín JA, Cabrera-Ponce JL, León-Ramírez CG, Camargo-Escalante MO, Ruiz-Herrera J (2020) Analysis of the photoreceptors involved in the light-depending basidiocarp formation in Ustilago maydis. Arch Microbiol 202(1):93–103. https://doi.org/10.1007/s00203-019-01725-w
Schweizer A, Rupp S, Taylos B, Röllinghoff M, Schröppel K (2000) The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol Microbiol 38(3):435–445. https://doi.org/10.1046/j.1365-2958.2000.02132.x
Schmitz L, Schwier MA, Heimel K (2019) The unfolded protein response regulates pathogenic development of Ustilago maydis by Rok1-dependent inhibition of mating-type signaling. Mbio 10(6):e02756-e2819. https://doi.org/10.1128/mBio.02756-19
Snetselaar K (1993) Microscopic observation of Ustilago maydis mating interactions. Exp Mycol 17:345–355. https://doi.org/10.1006/emyc.1993.1033
Staib P, Binder A, Kretschmar M, Nichterlein T (2004) Tec1p-independent activation of a hypha-associated Candida albicans virulence gene during infection. Infect Inmmun 72(4):2386–2389. https://doi.org/10.1128/IAI.72.4.2386-2389.2004
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, von Mering C (2018) String v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47:D607–D613. https://doi.org/10.1093/nar/gky1131
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Teixeira MC, Monteiro PT, Palma M, Costa C, Godinho CP, Pais P, Cavalheiro M, Antunes M, Lemos A, Pedreira T, Sá-Correia I (2017) YEASTRACT: an upgraded database for the analysis of transcription regulatory networks in Saccharomyces cerevisiae. Nucleic Acids Res 46:348–353. https://doi.org/10.1093/nar/gkx842
Tian W, Yu J, Tomchick DR, Pan D, Luo X (2010) Structural and functional analysis of the YAP-binding domain of human TEAD2. Proc Natl Acad Sci 107(106):7293–7298. https://doi.org/10.1073/pnas.1000293107
Tsukuda T, Carleton S, Fotheringham S, Holloman WK (1988) Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol Cell Biol 8(9):3703–3709. https://doi.org/10.1128/MCB.8.9.3703
Yu J-H, Hamari Z, Han KH, Seo JA, Reyes-Dominguez Y, Scazzocchio C (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Gen Biol 41:973–981. https://doi.org/10.1016/j.fgb.2004.08.001
Yockey CE, Shimizu N (1998) cDNA cloning and characterization of mouse DTEF-1 and ETF, members of the TEA/ATTS family of transcription factors. DNA Cell Biol 17(2):187–196. https://doi.org/10.1089/dna.1998.17.187
Acknowledgements
Thanks are given to JA Cisneros-Duran and JE Reynoso-Jiménez for their technical assistance.
Funding
This work was partially supported by Consejo Nacional de Ciencia y Tecnología (CONACYT), México.
Author information
Authors and Affiliations
Contributions
CGLR, JASA, MFSC, and JLCP designed and did the experimental work; CGLR, JASA, and JRH were involved in writing the manuscript; JRH obtained the funding and supervised the work; DMS, ETAC, and MLOC did the bioinformatic and data analysis; LSS was responsible for all microscopic analyses.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
All authors agree on what is described about their participation in this work.
Consent to publication
All authors agree on the submission of the manuscript.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary Information Fig. 1.
FUZ reaction between the Δtec1-1 and Δtec1-2 mutants. (JPG 78 KB)
Supplementary Information Fig. 2.
Cell morphology of U. maydis strains grown on minimal medium containing different carbon sources and pH. Notice the magnification on the pictures. U. maydis cells (a2b2 wt and Δtec1-2) strains A) grown in pH7 minimal medium with a fatty acid and stained with calcofluor white, B) grown in pH3 minimal medium with glucose and stained with calcofluor white. (PDF 936 KB)
Supplementary Information Fig. 3.
3. Effect of different types of stress. Decimal dilutions of cell suspensions (107) cells/ mL) (a1b1, a2b2) Δtec1-1 and 1-2 mutants and wt strains were spotted on MM pH7 plates and grown for 72 h at 28oC. 1.5 M Sorbitol; 120 μg/mL Rose bengal; 5mM LiCl; 1M NaCl; 1.2M KCl. (PDF 268 KB)
Supplementary Information Fig. 4.
Stress with hydrogen peroxide to measure the sensitivity to reactive oxygen species. MM pH7 with filter papers circles impregnated with a solution of H2O2 at 30% were placed over plates grown with the wild type or mutant strains. (PDF 292 KB)
Rights and permissions
About this article
Cite this article
León-Ramírez, C.G., Sánchez-Arreguin, J.A., Cabrera-Ponce, J.L. et al. Tec1, a member of the TEA transcription factors family, is involved in virulence and basidiocarp development in Ustilago maydis. Int Microbiol 25, 17–26 (2022). https://doi.org/10.1007/s10123-021-00188-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-021-00188-8