Acid pH Strategy Adaptation through NRG1 in Ustilago maydis
Abstract
:1. Introduction
2. Material and Methods
2.1. Strains, Media and Culture Conditions
2.2. Oxidative Stress
2.3. Identification of NRG1 Gene of U. maydis
2.4. Determination of Virulence
2.5. DNA Extraction
2.6. Mutation of U. maydis NRG1 Gene
2.7. Analysis of the Phenotypic Characteristics of nrg1 Mutant Strains of U. maydis
2.8. RNA Extraction
2.9. RNA-Seq Library Sequencing
2.10. Analysis of the RNA-Seq Data
2.11. Differential Gene Expression (DGE) and GSEA Analysis
2.12. Validation of Expression (RT-qPCR)
2.13. Statistics
2.14. Promoter Analyses
2.15. Glycolipids Detection
2.16. Nucleus and Cell Wall Staining
3. Results
3.1. In Silico Identification of the Gene NRG1 Based on Sequence Similarity
3.2. Mutation and Phenotypic Characterization of the nrg1 Mutant Growth and Wall State under Different Conditions
3.3. Altered Resistance of ∆nrg1 Mutant Cells to Oxidative, Toxic Ionic and General Stress
3.4. Mannosyl Erythritol Lipids (MELs) Synthesis Pathway and Light Voltage Response Genes Are Affected in the ∆nrg1 Mutant Strain
3.5. Cellular Functions of U. maydis NRG1-Regulated Genes
3.6. Validation of the RNA-Seq Data by RT-qPCR
3.7. Functional Enrichment and Network Analysis of Differentially Expressed Genes
3.8. The NRG1 Gene Is Required for U. maydis Pathogenesis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Cervantes-Chávez, J.A.; Ortiz-Castellanos, L.; Tejeda-Sartorius, M.; Gold, S.; Ruiz-Herrera, J. Functional analysis of the pH responsive pathway Pal/Rim in the basidiomycete Ustilago maydis. Fungal Genet. Biol. 2010, 47, 446–457. [Google Scholar]
- Sartorel, E.; Perez-Martin, J. The distinct interaction between cell cycle regulation and the widely conserved morphogenesis-related (MOR) pathways in the fungus Ustilago maydis determines morphology. J. Cell Sci. 2012, 125, 4597–4608. [Google Scholar] [CrossRef] [Green Version]
- Cervantes-Montelongo, J.A.; Aréchiga-Carvajal, E.T.; Ruiz-Herrera, J. Adaptation of Ustilago maydis to extreme values: A transcriptomic analysis. J. Basic Microbiol. 2017, 56, 1222–1233. [Google Scholar] [CrossRef]
- Vyas, A.; Berkey, C.D.; Miyao, T.; Carlson, M. Repressors Nrg1 and Nrg2 regulate a set of stress-responsive genes in Sacharomyces cerevisiae. Eukaryot. Cell 2005, 4, 1882–1891. [Google Scholar] [CrossRef] [Green Version]
- Park, S.H.; Koh, S.S.; Chun, J.H.; Hwang, H.J.; Kang, H.S. Nrg1 is a transcriptional repressor for glucose repression of STA1 gene expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19, 2044–2050. [Google Scholar] [CrossRef] [Green Version]
- Braun, B.R.; Kadosh, D.; Johnson, A.D. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 2001, 20, 4753–4761. [Google Scholar] [CrossRef]
- Murad, A.M.; d’Enfert, C.; Gaillardin, C.; Tournu, H.; Tekaia, F.; Talibi, D.; Marechal, D.; Marchais, V.; Cottin, J.; Brown, A.J. Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1. Mol. Microbiol. 2001, 42, 981–983. [Google Scholar] [CrossRef] [Green Version]
- Rocha, C.R.; Schroppel, K.; Harcus, D.; Marcil, A.; Dignard, D.; Taylor, B.N.; Thomas, D.Y.; Whiteway, M.; Leberer, E. Signaling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans. Mol. Biol. Cell 2001, 12, 3631–3643. [Google Scholar] [CrossRef] [Green Version]
- Bockmühl, D.P.; Krishnamurthy, S.; Gerads, M.; Sonneborn, A.; Ernst, J.F. Distinct and redundant roles of the two protein kinase A isoforms Tpk1p and Tpk2p in morphogenesis and growth of Candida albicans. Mol. Microbiol. 2001, 42, 1243–1257. [Google Scholar] [CrossRef]
- Lu, Y.; Su, C.; Wang, A.; Liu, H. Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for formation and maintenance. PLoS Biol. 2011, 9, e1001105. [Google Scholar] [CrossRef]
- Lu, Y.; Su, C.; Liu, H. Candida albicans hyphal initiation and elongation. Trends Microbiol. 2014, 22, 707–714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cramer, K.L.; Gerrald, Q.D.; Nichols, C.B.; Price, M.S.; Alspaugh, J.A. Transcription factor Nrg1 mediates capsule formation, stress response, and pathogenesis in Cryptococcus neoformans. Eukaryot. Cell 2006, 5, 1147–1156. [Google Scholar] [CrossRef] [Green Version]
- Kämper, J.; Kahmann, R.; Bölker, M.; Ma, L.; Brefort, T.; Saville, B.J.; Banuett, F.; Kronstad, J.W.; Gold, S.E.; Müller, O.; et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444, 97–101. [Google Scholar] [CrossRef]
- Franco-Frías, E.; Ruiz-Herrera, J.; Aréchiga-Carvajal, E.T. Transcriptomic analysis of the role of Rim101/PacC in the adaptation of Ustilago maydis to an alkaline environment. Microbiology 2014, 160, 1985–1998. [Google Scholar] [CrossRef] [Green Version]
- Ruiz-Herrera, J.; León-Ramírez, C.G.; Guevara-Olvera, L.; Cárabez-Trejo, A. Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis. Microbiology 1995, 141, 695–703. [Google Scholar] [CrossRef] [Green Version]
- Davis, D.A. How human pathogenic fungi sense and adapt to pH: The link to virulence. Curr. Opin. Microbiol. 2009, 12, 365–370. [Google Scholar] [CrossRef]
- Martínez-Espinoza, A.D.; Ruiz-Herrera, J.; León-Ramírez, C.G.; Gold, S.E. MAP kinase and cAMP signaling pathways modulate the pH-induced yeast-to-mycelium dimorphic transition in the corn smut fungus Ustilago maydis. Curr. Microbiol. 2004, 49, 274–281. [Google Scholar] [CrossRef]
- Peñalva, M.A.; Arst, H.N., Jr. Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeast. Annu. Rev. Microbiol. 2004, 58, 425–451. [Google Scholar] [CrossRef]
- Aréchiga-Carvajal, E.T.; Ruiz-Herrera, J. The RIM101/PacC homologue from the basidiomycete Ustilago maydis is functional in multiple pH-sensitive phenomena. Eukaryot. Cell 2005, 4, 999–1008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Banuett, F.; Herskowitz, J. Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl. Acad. Sci. USA 1989, 86, 5878–5882. [Google Scholar] [CrossRef] [Green Version]
- Holliday, R. Ustilago maydis. In Handbook of Genetics; King, R.C., Ed.; Plenum Press: New York, NY, USA, 1974; pp. 575–595. [Google Scholar]
- García-Pedrajas, M.D.; Nadal, M.; Kapa, L.B.; Perlin, M.H.; Andrews, D.L.; Gold, S.E. DelsGate, a robust and rapid gene deletion construction method. Fungal Genet. Biol. 2008, 45, 379–388. [Google Scholar] [CrossRef] [PubMed]
- Chavez-Ontiveros, J.; Martinez-Espinoza, A.; Ruiz-Herrera, J. Double chitin synthetase mutants from the corn smut fungus Ustilago maydis. New Phytol. 2000, 146, 335–341. [Google Scholar] [CrossRef]
- Hoffman, C.S.; Wriston, F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 1987, 57, 267–272. [Google Scholar] [CrossRef]
- Yu, J.H.; Hamari, Z.; Han, K.H.; Seo, J.A.; Reyes-Dominguez, Y.; Scazzocchio, C. Double-joint PCR: A PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 2004, 41, 973–981. [Google Scholar] [CrossRef]
- Tsukuda, T.; Carleton, S.; Fotheringham, S.; Holloman, W.K. Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol. Cell. Biol. 1988, 8, 3703–3709. [Google Scholar] [CrossRef] [Green Version]
- Sambrook, J.; Russell, J.W. Molecular Cloning: A Laboratory Manual; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 2001. [Google Scholar]
- Edgar, R.; Domrachev, M.; Lash, A.E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleis Acids Res. 2002, 30, 207–210. [Google Scholar] [CrossRef] [Green Version]
- Huber, W.; Carey, V.J.; Gentleman, R.; Anders, S.; Carlson, M.; Carvalho, B.S.; Bravo, H.C.; Davis, S.; Gatto, L.; Girke, T.; et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat. Methods 2015, 12, 115–121. [Google Scholar] [CrossRef]
- Götz, S.; Garcia-Gómez, J.M.; Terol, J.; Willians, T.D.; Nagaraj, S.H.; Nueda, M.J.; Robles, M.; Talón, M.; Dopazo, J.; Conesa, A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36, 3420–3435. [Google Scholar] [CrossRef]
- Gaidatzis, D.; Lerch, A.; Hahne, F.; Stadler, M.B. QuasR: Quantification and annotation of short reads in R. Bioinformatics 2015, 31, 1130–1132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Langmead, B.; Trapnell, C.; Pop, M.; Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10, R25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Au, K.F.; Jiang, H.; Lin, L.; Xing, Y.; Wong, W.H. Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res. 2010, 38, 4570–4578. [Google Scholar] [CrossRef] [PubMed]
- Szklarczyk, D.; Gable, A.L.; Lyon, D.; Junge, A.; Wyder, S.; Huerta-Cepas, J.; Simonovic, M.; Doncheva, N.T.; Morris, J.H.; Bork, P.; et al. STRING v11: Protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019, 47, D607–D613. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- León-Ramírez, C.G.; Cabrera-Ponce, J.L.; Martínez-Soto, D.; Sánchez-Arreguin, J.A.; Aréchiga-Carvajal, E.T.; Ruiz-Herrera, J. Transcriptomic analysis of basidiocarp development in Ustilago maydis (DC) Cda. Fungal Genet. Biol. 2017, 101, 34–45. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2013. [Google Scholar]
- Monteiro, P.T.; Mendes, N.D.; Teixeira, M.C.; d’Orey, S.; Tenreiro, S.; Mira, N.P.; Pais, H.; Francisco, A.P.; Carvalho, A.M.; Lourenço, A.B.; et al. YEASTRAC-DISCOVERER: New tools improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res. 2008, 36, D132–D136. [Google Scholar] [CrossRef] [Green Version]
- Teixera, M.C.; Monteiro, P.T.; Palma, M.; Costa, C.; Godinho, C.P.; Pais, P.; Cavalheiro, M.; Antunes, M.; Lemos, A.; Pedreira, T.; et al. YEASTRACT: An upgraded database for the analysis of transcription regulatory networks in Saccharomyces cerevisiae. Nucleic Acids Res. 2018, 46, D348–D353. [Google Scholar] [CrossRef] [Green Version]
- Hewald, S.; Josephs, K.; Bölker, M. Genetic analysis of biosurfactant production in Ustilago maydis. Appl. Environ. Microbiol. 2005, 71, 3033–3040. [Google Scholar] [CrossRef] [Green Version]
- Nern, A.; Arkowitz, R.A. A GTP-exchange factor required for cell orientation. Nature 2002, 391, 195–198. [Google Scholar] [CrossRef]
- Wedlich-Soldner, R.; Wai, S.C.; Schmidt, T.; Li, R. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J. Cell Biol. 2004, 166, 889–900. [Google Scholar] [CrossRef]
- Castresana, J.; Sarastre, M. Does Vav bind to F-actin through a CH domain? FEBS Lett. 1995, 374, 149–151. [Google Scholar] [CrossRef] [Green Version]
- Vancompernolle, K.; Gimona, M.; Herzog, M.; Damme, J.; Vandekerckhove, J.; Small, V. Isolation and sequence of a tropomyosin-binding fragment of turkey gizzard calponin. FEBS Lett. 1990, 274, 146–150. [Google Scholar]
- Kolakowski, J.; Makuch, R.; Stepkowski, D.; Dabrowska, R. Interaction of calponin with actin its functional implications. Biochem. J. 1995, 306, 199–204. [Google Scholar] [CrossRef] [PubMed]
- Bassiliana, M.; Hopkins, J.; Arkowitz, R.A. Regulation of the Cdc42/Cdc24 GTPase module during Candida albicans hyphal growth. Eukaryot. Cell 2005, 4, 588–603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brombacher, K.; Fisher, B.B.; Rüfenacht, K.; Eggen, R.I. The role of Yap1p and Skn7p-mediated oxidative stress response in the defense of Saccharomyces cerevisiae against singlet oxygen. Yeast 2006, 23, 741–750. [Google Scholar] [CrossRef]
- Hewald, S.; Linne, U.; Sherer, M.; Marahiel, M.A.; Kämper, J.; Bölker, M. Identification of a gene cluster for Biosynthesis of mannosylerythritol lipids in the Basidiomycetous fungus Ustilago maydis. Appl. Environ. Microbiol. 2006, 72, 5469–5477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ruepp, A.; Zollner, A.; Maier, D.; Alberman, K.; Hani, J.; Mokrejs, M.; Tetko, I.; Güldener, U.; Mannhaupt, G.; Münsterkö, M.; et al. The Funcat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004, 32, 5539–5545. [Google Scholar] [CrossRef] [PubMed]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2∆∆CT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
- Selvig, K.; Aspaugh, J.A. pH response pathways in fungi: Adapting to host-derived and environmental signals. Microbiology 2011, 39, 249–256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, C.; Yu, J.; Lu, Y. Hyphal development in Candida albicans from different cell states. Curr. Genet. 2018, 64, 1239–1243. [Google Scholar] [CrossRef]
- Zhao, Y.; Du, J.; Xiong, B.; Xu, H.; Jiang, L. ESCRT components regulate the expression of the ER/Golgi calcium pump gene PMR1 through the Rim101/Nrg1 pathway in budding yeast. J. Mol. Cell Biol. 2013, 5, 336–344. [Google Scholar] [CrossRef] [Green Version]
- Cotter, P.D.; Hill, C. Surviving the acid test: Responses of gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev. 2003, 67, 429–453. [Google Scholar] [CrossRef] [Green Version]
- Brych, A.; Mascarenhas, J.; Jaeger, E.; Charkiewicz, E.; Pokorny, R.; Bölker, M.; Doehlemann, G.; Batschauer, A. White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis. Microbiologyopen 2016, 5, 224–243. [Google Scholar] [CrossRef] [PubMed]
- Bilsland, E.; Molin, C.; Swaminathan, S.; Ramne, A.; Sunnerhagen, P. Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol. Microbiol. 2004, 53, 1743–1756. [Google Scholar] [CrossRef] [PubMed]
- Smith, D.A.; Morgan, B.A.; Quinn, J. Stress signaling to fungal stress-activated protein kinase pathways. FEMS Microbiol. Lett. 2010, 306, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Reverberi, M.; Gazzetti, K.; Punelli, F.; Scarpari, M.; Zjalic, S.; Ricelli, A.; Fabbri, A.A.; Fanelli, C. Aoyap1 regulates OTA synthesis by controlling cell redox balance in Aspergillus ochraceus. Appl. Microbiol. Biotechnol. 2012, 95, 1293–1304. [Google Scholar] [CrossRef]
- Toledano, M.B.; Delaunay, A.; Monceau, L.; Tacnet, F. Microbial H2O2 sensors as archetypical redox signaling modules. Trends Biochem. Sci. 2004, 29, 351–357. [Google Scholar] [CrossRef]
- Yin, W.B.; Amaike, S.; Wohlbach, D.J.; Gash, A.P.; Chiang, Y.M.; Wang, C.C.; Bok, J.W.; Rohlfs, M.; Keller, N.P. An Aspergillus nidulans bZIP response pathway hardwired for defensive secondary metabolism operates through aflR. Mol. Microbiol. 2012, 83, 1024–1034. [Google Scholar] [CrossRef] [Green Version]
- Bayram, O.; Biesemann, C.; Krappmann, S.; Galland, O.; Braus, G.H. More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development. Mol. Biol. Cell 2008, 19, 3254–3262. [Google Scholar] [CrossRef] [Green Version]
- García-Esquivel, M.; Esquivel-Naranjo, E.U.; Hernández-Oñate, M.A.; Ibarra-Laclette, E.; Herrera-Estrella, A. The Trichoderma atroviride cryptochrome/photolyase genes regulate the expression of blr1-independent genes both in red and blue light. Fungal Biol. 2016, 120, 500–512. [Google Scholar] [CrossRef]
- Kurz, M.; Eder, C.; Isert, D.; Li, Z.; Paulus, E.F.; Schiell, M.; Toti, L.; Vértesy, L.; Wink, J.; Seibert, G. Ustilipids, acylated β-d-mannopynanosyl d-erythritols from Ustilago maydis and Geotrichum candidum. J. Antibiot. 2003, 56, 91–101. [Google Scholar] [CrossRef] [Green Version]
- Lemieux, R.U. Biochemistry of the ustilaginales: VIII. the structures and configurations of the ustilic acids. Can. J. Chem. 1953, 31, 396–417. [Google Scholar] [CrossRef]
- Fluharty, A.L.; O’Brien, J.S. A mannose- and erythritol-containing glycolipid from Ustilago maydis. Biochemistry 1969, 8, 2627–2632. [Google Scholar] [CrossRef] [PubMed]
- Spoeckner, S.; Wray, V.; Nimtz, M.; Lang, S. Glycolipids of the smut fungus Ustilago maydis from cultivation on renewable resources. Appl. Microbiol. Biotechnol. 1999, 51, 33–39. [Google Scholar] [CrossRef]
- Ron, E.Z.; Rosenberg, E. Natural roles of biosurfactants. Environ. Microbiol. 2001, 3, 229–236. [Google Scholar] [CrossRef] [PubMed]
- Wood, J.M. Bacterial osmoregulation: A paradigm for the study of cellular homeostasis. Annu. Rev. Microbiol. 2011, 65, 215–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rzechonek, D.A.; Day, A.M.; Quinn, J.; Mironczuk, A.M. Influence of ylHog1 MAPK kinase on Yarrowia lipolytica stress response and erythritol production. Sci. Rep. 2018, 8, 14735. [Google Scholar] [CrossRef] [PubMed]
- Reddy, V.S.; Shlykov, M.A.; Castillo, R.; Sun, E.I.; Saier, M.H. The major facilitator superfamily (MFS) revisited. FEBS J. 2012, 279, 2022–2035. [Google Scholar] [CrossRef]
- Yin, W.B.; Reinke, A.W.; Szilágil, M.; Emri, T.; Chiang, Y.M.; Keating, A.E.; Pócsi, I.; Wang, C.C.; Keller, N.P. bZIP transcription factors affecting secondary metabolism, sexual development and stress responses in Aspergillus nidulans. Microbiology 2013, 157, 77–88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hérivaux, A.; So, Y.S.; Gastebois, A.; Latgé, J.P.; Bouchara, J.P.; Bahn, Y.S.; Papon, N. Major sensing proteins in pathogenic fungi: The hybrid histidine kinase family. PLoS Pathog. 2016, 12, e1005683. [Google Scholar] [CrossRef] [Green Version]
- Kabbara, S.; Hérivaux, A.; Dugé de Bernonville, T.; Courdavault, V.; Clastre, M.; Gastebois, A.; Osman, M.; Hamze, M.; Cock, J.M.; Schaap, P.; et al. Diversity and evolution of sensor histidine kinases in eukaryotes. Genome Biol. Evol. 2018, 11, 86–108. [Google Scholar] [CrossRef]
- Purschwitz, J.; Müller, S.; Fischer, R. Mapping the interaction sites of Aspergillus nidulans phytochrome FphA with the global regulator VeA and the White collar proteins LreB. Mol. Genet. Genom. 2009, 281, 35–42. [Google Scholar] [CrossRef]
- Sánchez-Arreguin, J.A.; Cabrera-Ponce, J.L.; León-Ramírez, C.G.; Camargo-Escalante, M.O.; Ruiz-Herrera, J. Analysis of the photoreceptors involved on light-depending basidiocarp formation in Ustilago maydis. Arch. Microbiol. 2020, 202, 93–103. [Google Scholar] [CrossRef] [PubMed]
- Briggs, W.R.; Spudich, J.L. Handbook of Photosensory Receptors; Wiley VCH: Weinheim, Germany, 2005; pp. 277–304. [Google Scholar]
- Baker, C.L.; Loros, L.L.; Dunlap, J.C. The circadian clock of Neurospora crassa. FEMS Microbiol. Rev. 2012, 36, 95–110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Sánchez-Arreguin, J.A.; Ruiz-Herrera, J.; Mares-Rodriguez, F.d.J.; León-Ramírez, C.G.; Sánchez-Segura, L.; Zapata-Morín, P.A.; Coronado-Gallegos, J.; Aréchiga-Carvajal, E.T. Acid pH Strategy Adaptation through NRG1 in Ustilago maydis. J. Fungi 2021, 7, 91. https://doi.org/10.3390/jof7020091
Sánchez-Arreguin JA, Ruiz-Herrera J, Mares-Rodriguez FdJ, León-Ramírez CG, Sánchez-Segura L, Zapata-Morín PA, Coronado-Gallegos J, Aréchiga-Carvajal ET. Acid pH Strategy Adaptation through NRG1 in Ustilago maydis. Journal of Fungi. 2021; 7(2):91. https://doi.org/10.3390/jof7020091
Chicago/Turabian StyleSánchez-Arreguin, José Alejandro, José Ruiz-Herrera, F. de Jesus Mares-Rodriguez, Claudia Geraldine León-Ramírez, Lino Sánchez-Segura, Patricio Adrián Zapata-Morín, Jordan Coronado-Gallegos, and Elva Teresa Aréchiga-Carvajal. 2021. "Acid pH Strategy Adaptation through NRG1 in Ustilago maydis" Journal of Fungi 7, no. 2: 91. https://doi.org/10.3390/jof7020091