Investigating the Smuts: Common Cues, Signaling Pathways, and the Role of MAT in Dimorphic Switching and Pathogenesis
Abstract
:1. Introduction
2. Physiological Aspect of Fungal Dimorphism
2.1. External Factors Affecting Fungal Dimorphism
Lineages/Species | Life Strategy | Environmental Cues * | References |
---|---|---|---|
ASCOMYCOTA Saccharomycotina Saccharomyces cerevisiae | Saprobe | Nutrient limitation (carbon, nitrogen) | [14] |
Candida albicans | Opportunistic human pathogen | Temperature, serum, CO2, pH, farnesol, GlcNAc | [16] |
Holleya sinecauda | Plant pathogen | Media solidity | [34] |
Yarrowia lipolytica | Saprobe | Nitrogen source, GlcNAc, serum, citrate, pH, anaerobic | [21,24,29] |
Taphrinomycotina Taphrina deformans | Plant pathogen | Unknown cue from host leaves | [36,37] |
Schizosaccharomyces pombe | Saprobe | Nitrogen starvation | [15] |
Eurotiomycetes Blastomyces dermatidis | Human pathogen | Temperature, GlcNAc | [6,30] |
Coccidioides immitis | Human pathogen | Temperature | [6] |
Talaromyces marneffii | Human pathogen | Temperature | [6] |
Histoplasma capsulatum | Human pathogen | Temperature, GlcNAc | [6,30,38] |
Sordariomycetes Sporothrix schenckii | Human pathogen | Temperature | [6] |
Ophiostoma ulmi & O. novo-ulmi | Plant pathogen | Nitrogen source, inoculum density, quorum-sensing, linoleic acid | [23,39,40,41] |
Verticillium albo-atrum | Plant pathogen | Culture agitation, inoculum density | [35] |
Metarhizium rileyi | Insect pathogen | Host hemolymph, quorum-sensing | [42] |
Dothideomycetes Zymoseptoria tritici | Plant pathogen | Nitrogen starvation | [19] |
Aureobasidium pullulans | Saprobe | Nitrogen source, quorum-sensing, Zn2+ | [22,33] |
Hortaea werneckii ** | Saprobe, opportunistic human pathogen | Temperature, CO2, cysteine, inoculum size, agitation | [43,44] |
BASIDIOMYCOTA Ustilaginomycotina Ustilago maydis | Plant pathogen | Mating, lipid, hydrophobicity, acidic pH, nitrogen starvation | [18,31,45,46] |
Malassezia spp. | Opportunistic human pathogen | L-DOPA, lipid on mammal skin, high CO2 tension | [47,48,49] |
Pucciniomycotina Microbotryum lychnidis-dioicae | Plant pathogen | Unknown | [50] |
Agaricomycotina Cryptococcus neoformans | Human pathogen | Mating, nitrogen starvation, temperature, CO2 | [17] |
Trichosporon cutaneum | Saprobe | Nitrogen source, pH, temperature | [20] |
Tremella spp. | Saprobe, mycoparasite | Mating, ploidy status, carbon sources, nitrogen sources | [25,26] |
MUCOROMYCOTA Mucor spp. | Saprobe, opportunistic human pathogen | Carbon source, CO2 | [27] |
2.2. Comparative Physiological Studies in Ustilaginomycotina
3. Mating and Fungal Dimorphism
3.1. Cellular Communication in Dimorphic Fungi
3.2. Mating (MAT) Loci in U. maydis
3.3. Comparative MAT Loci Analyses in Ustilaginomycotina
4. Molecular Mechanism Related to Fungal Dimorphism
4.1. cAMP-PKA Pathway
4.2. MAPK Pathway
4.3. Alternative Pathways
4.4. Upstream and Downstream Molecular Players
4.5. Comparative Genomics of Fungal Dimorphism Genes in Ustilaginomycotina
5. Benefits of Fungal Dimorphism
6. Conclusions and Perspectives
7. Materials and Methods
7.1. Physiological Study
7.2. MAT Loci Studies
7.3. Comparative Genomic Studies
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Zhao, Y.; Lin, J.; Fan, Y.; Lin, X. Life cycle of Cryptococcus neoformans. Annu. Rev. Microbiol. 2019, 73, 17–42. [Google Scholar] [CrossRef] [PubMed]
- Riquelme, M.; Aguirre, J.; Bartnicki-García, S.; Braus, G.H.; Feldbrügge, M.; Fleig, U.; Hansberg, W.; Herrera-Estrella, A.; Kämper, J.; Kück, U.; et al. Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures. Microbiol. Mol. Biol. Rev. 2018, 82, 1–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kurtzman, C.P.; Sugiyama, J. Saccharomycotina and Taphrinomycotina: The Yeasts and Yeast-like Fungi of the Ascomycota. In The Mycota VII Systematics and Evolution Part B; McLaughlin, D.J., Spatafora, J.W., Eds.; Springer: Berlin/Heidelberg, Germany; New York, NY, USA, 2015; pp. 3–34. [Google Scholar]
- Berkeley, M.J. On a confervoid state of Mucor clavatus, Lk. Mag. Zool. Bot. 1838, 2, 340–343. [Google Scholar]
- Naranjo-Ortiz, M.A.; Gabaldón, T. Fungal evolution: Major ecological adaptations and evolutionary transitions. Biol. Rev. 2019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sil, A.; Andrianopoulos, A. Thermally dimorphic human fungal pathogens—Polyphyletic pathogens with a convergent pathogenicity trait. Cold Spring Harb. Perspect. Med. 2015, 5, 1–17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Begerow, D.; Schaffer, A.M.; Kellner, R.; Youkov, A.; Kemler, M.; Oberwinkler, F.; Bauer, R. Ustilaginomycotina. In Mycota VII Systematics and Evolution Part A; McLaughlin, D.J., Spatafora, J.W., Eds.; Springer: Berlin/Heidelberg, Germany; New York, NY, USA, 2014; pp. 295–329. [Google Scholar]
- Weiss, M.; Bauer, R.; Sampaio, J.P.; Oberwinkler, F. Tremellomycetes and Related Groups. In Mycota VII Systematics and Evolution Part A; McLaughlin, D.J., Spatafora, J.W., Eds.; Springer: Berlin/Heidelberg, Germany; New York, NY, USA, 2014; pp. 331–355. [Google Scholar]
- Oberwinkler, F. Yeasts in Pucciniomycotina. Mycol. Prog. 2017, 16, 831–856. [Google Scholar] [CrossRef]
- Vollmeister, E.; Schipper, K.; Baumann, S.; Haag, C.; Pohlmann, T.; Stock, J.; Feldbrügge, M. Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol. Rev. 2012, 36, 59–77. [Google Scholar] [CrossRef] [Green Version]
- Hibbett, D.S.; Stajich, J.E.; Spatafora, J.W. Toward genome-enabled mycology. Mycologia 2013, 105, 1339–1349. [Google Scholar] [CrossRef] [Green Version]
- Kijpornyongpan, T. Comparative Studies of Fungal Dimorphism in Dikarya; Purdue University: West Lafayette, IN, USA, 2019. [Google Scholar]
- Kijpornyongpan, T.; Mondo, S.J.; Barry, K.; Sandor, L.; Lee, J.; Lipzen, A.; Pangilinan, J.; LaButti, K.; Hainaut, M.; Henrissat, B.; et al. Broad Genomic Sampling Reveals a Smut Pathogenic Ancestry of the Fungal Clade Ustilaginomycotina. Mol. Biol. Evol. 2018, 35, 1840–1854. [Google Scholar] [CrossRef] [Green Version]
- Cullen, P.J.; Sprague, G.F. The regulation of filamentous growth in yeast. Genetics 2012, 190, 23–49. [Google Scholar] [CrossRef]
- Amoah-Buahin, E.; Bone, N.; Armstrong, J. Hyphal Growth in the Fission Yeast. Microbiology 2005, 4, 1287–1297. [Google Scholar] [CrossRef]
- Sudbery, P.E. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 2011, 9, 737–748. [Google Scholar] [CrossRef] [PubMed]
- Lin, X. Cryptococcus neoformans: Morphogenesis, infection, and evolution. Infect. Genet. Evol. 2009, 9, 401–416. [Google Scholar] [CrossRef]
- Paul, J.A.; Barati, M.T.; Cooper, M.; Perlin, H. Physical and Genetic Interaction between Ammonium Transporters and the Signaling Protein Rho1 in the Plant Pathogen Ustilago maydis. Eukaryot. Cell 2014, 13, 1328–1336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yemelin, A.; Brauchler, A.; Jacob, S.; Laufer, J.; Heck, L.; Foster, A.J.; Antelo, L.; Andresen, K.; Thines, E. Identification of factors involved in dimorphism and pathogenicity of Zymoseptoria tritici. PLoS ONE 2017, 12, e0183065. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, L.B.; Wang, Y.; Zhang, Z.B.; Yang, H.L.; Yan, R.M.; Zhu, D. Influence of environmental and nutritional conditions on yeast—Mycelial dimorphic transition in Trichosporon cutaneum. Biotechnol. Biotechnol. Equip. 2017, 2818. [Google Scholar] [CrossRef] [Green Version]
- Szabo, R. Dimorphism in Yarrowia lipolytica: Filament formation is suppressed by nitrogen starvation and inhibition of respiration. Folia Microbiol. (Praha) 1999, 44, 19–24. [Google Scholar] [CrossRef]
- Park, D. Population density and yeast mycelial dimorphism in Aureobasidium pullulans. Trans. Br. Mycol. Soc. 1984, 82, 39–44. [Google Scholar] [CrossRef]
- Kulkarni, R.K.; Nickerson, K.W. Nutritional control of dimorphism in Ceratocystis ulmi. Exp. Mycol. 1981, 5, 148–154. [Google Scholar] [CrossRef]
- Ruiz-Herrera, J.; Sentandreu, R. Different effectors of dimorphism in Yarrowia lipolytica. Arch. Microbiol. 2002, 178, 477–483. [Google Scholar] [CrossRef]
- Hou, L.; Chen, Y.; Ma, C.; Liu, J.; Chen, L.; Ma, A. Effects of environmental factors on dimorphic transition of the jelly mushroom Tremella fuciformis. Cryptogam. Mycol. 2011, 32, 421–428. [Google Scholar] [CrossRef]
- Pippola, E.; Kyroviita, M.-M. Growth and dimorphism of the mycoparasite Tremella encephala as affected by different nitrogen and carbon sources and the host presence. Cryptogamie 2009, 30, 3. [Google Scholar]
- Orlowski, M. Mucor Dimorphism. Microbiol. Rev. 1991, 55, 234–258. [Google Scholar] [CrossRef] [PubMed]
- Cullen, P.J.; Sprague, G.F. Glucose depletion causes haploid invasive growth in yeast. Proc. Natl. Acad. Sci. USA 2000, 97, 13619–13624. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.; Cheon, S.A.; Park, S.; Song, Y.; Kim, J.Y. Serum-induced hypha formation in the dimorphic yeast Yarrowia lipolytica. FEMS Microbiol. Lett. 2000, 190, 9–12. [Google Scholar] [CrossRef]
- Gilmore, S.A.; Naseem, S.; Konopka, J.B.; Sil, A. N-acetylglucosamine (GlcNAc) Triggers a Rapid, Temperature-Responsive Morphogenetic Program in Thermally Dimorphic Fungi. PLoS Genet. 2013, 9. [Google Scholar] [CrossRef] [Green Version]
- Ruiz-Herrera, J.; Guevara-Olvera, C.G.L.L.; Cdrabez-Trejo, A. Yeast-mycelial dimorphism of haploid and diploid strains of Ustiago maydis. Microbiology 1995, 695–703. [Google Scholar] [CrossRef] [Green Version]
- Buffo, J.; Herman, M.A.; Soll, D.R. A characterization of pH-regulated dimorphism in Candida albicans. Mycopathologia 1984, 85, 21–30. [Google Scholar] [CrossRef]
- Reeslev, M.; Jorgensen, B.B.; Jorgensen, O.B. Influence of Zn2+ on yeast-mycelium dimorphism and exopolysaccharide production by the fungus Aureobasidium pullulans grown in a defined medium in continuous culture. J. Gen. Microbiol. 1993, 139, 3065–3070. [Google Scholar] [CrossRef] [Green Version]
- Schade, D.; Walther, A.; Wendland, J. The development of a transformation system for the dimorphic plant pathogen Holleya sinecauda based on Ashbya gossypii DNA elements. Fungal Genet. Biol. 2003, 40, 65–71. [Google Scholar] [CrossRef]
- Keen, N.T.; Wang, M.C.; Long, M.; Erwin, D.C. Dimorphism in Verticillium albo-atrum as affected by initial spore concentration and antisporulant chemicals. Phytopathology 1971, 61, 1266–1269. [Google Scholar] [CrossRef]
- Rodrigues, M.G.; Fonseca, A. Molecular systematics of the dimorphic ascomycete genus Taphrina. Int. J. Syst. Evol. Microbiol. 2003, 53, 607–616. [Google Scholar] [CrossRef] [PubMed]
- Svetaz, L.A.; Bustamante, C.A.; Goldy, C.; Rivero, N.; Müller, G.L.; Valentini, G.H.; Fernie, A.R.; Drincovich, M.F.; Lara, M.V. Unravelling early events in the Taphrina deformans–Prunus persica interaction: An insight into the differential responses in resistant and susceptible genotypes. Plant Cell Environ. 2017, 40, 1456–1473. [Google Scholar] [CrossRef] [PubMed]
- Maresca, B.; Lambowitz, A.M.; Kumar, V.B.; Grant, G.A.; Kobayashi, G.S.; Medoff, G. Role of cysteine in regulating morphogenesis and mitochondrial activity in the dimorphic fungus Histoplasma capsulatum. Proc. Natl. Acad. Sci. USA 1981, 78, 4596–4600. [Google Scholar] [CrossRef] [Green Version]
- Hornby, J.M.; Jacobitz-Kizzier, S.M.; McNeel, D.J.; Jensen, E.C.; Treves, D.S.; Nickerson, K.W. Inoculum size effect in dimorphic fungi: Extracellular control of yeast-mycelium dimorphism in Ceratocystis ulmi. Appl. Environ. Microbiol. 2004, 70, 1356–1359. [Google Scholar] [CrossRef] [Green Version]
- Naruzawa, E.S.; Bernier, L. Control of yeast-mycelium dimorphism invitro in Dutch elm disease fungi by manipulation of specific external stimuli. Fungal Biol. 2014, 118, 872–884. [Google Scholar] [CrossRef]
- Naruzawa, E.S.; Malagnac, F.; Bernier, L. Effect of linoleic acid on reproduction and yeast-mycelium dimorphism in the Dutch elm disease pathogens. Botany 2016, 96, 31–39. [Google Scholar] [CrossRef] [Green Version]
- Boucias, D.; Liu, S.; Meagher, R.; Baniszewski, J. Fungal dimorphism in the entomopathogenic fungus Metarhizium rileyi: Detection of an in vivo quorum-sensing system. J. Invertebr. Pathol. 2016, 136, 100–108. [Google Scholar] [CrossRef]
- Hardcastle, R.V.; Szaniszlo, P.J. Characterization of dimorphism in Cladosporium werneckii. J. Bacteriol. 1974, 119, 294–302. [Google Scholar] [CrossRef] [Green Version]
- Houston, M.R.; Meyer, K.H.; Thomas, N.; Wolf, F.T. Dimorphism in Cladosporium werneckii. Sabouraudia J. Med. Vet. Mycol. 1969, 7, 195–198. [Google Scholar] [CrossRef]
- Brefort, T.; Doehlemann, G.; Mendoza-mendoza, A.; Reissmann, S.; Djamei, A.; Kahmann, R. Ustilago maydis as a Pathogen. Annu. Rev. Phytopathol. 2009, 47, 423–445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mendoza-Mendoza, A.; Berndt, P.; Djamei, A.; Weise, C.; Linne, U.; Marahiel, M.; Vraneš, M.; Kämper, J.; Kahmann, R. Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol. Microbiol. 2009, 71, 895–911. [Google Scholar] [CrossRef] [PubMed]
- Youngchim, S.; Nosanchuk, J.D.; Pornsuwan, S.; Kajiwara, S.; Vanittanakom, N. The role of L-DOPA on melanization and mycelial production in Malassezia furfur. PLoS ONE 2013, 8, e63764. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Faergemann, J.; Bernander, S. Micro-aerophilic and anaerobic growth of Pityrosporum species. Med. Mycol. 1981, 19, 117–121. [Google Scholar] [CrossRef]
- Faergemann, J. A new model for growth and filament production of Pityrosporum ovale (orbiculare) on human stratum corneum in vitro. J. Investig. Dermatol. 1989, 92, 117–119. [Google Scholar] [CrossRef] [Green Version]
- Schäfer, A.M.; Kemler, M.; Bauer, R.; Begerow, D. The illustrated life cycle of Microbotryum on the host plant Silene latifolia. Botany 2010, 88, 875–885. [Google Scholar] [CrossRef]
- Morrow, C.A.; Fraser, J.A. Sexual reproduction and dimorphism in the pathogenic basidiomycetes. FEMS Yeast Res. 2009, 9, 161–177. [Google Scholar] [CrossRef] [Green Version]
- Lanver, D.; Mendoza-Mendoza, A.; Brachmann, A.; Kahmann, R. Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 2010, 22, 2085–2101. [Google Scholar] [CrossRef] [Green Version]
- Domínguez, E.; Cuartero, J.; Heredia, A. An overview on plant cuticle biomechanics. Plant Sci. 2011, 181, 77–84. [Google Scholar] [CrossRef]
- Klose, J.; De Sá, M.M.; Kronstad, J.W. Lipid-induced filamentous growth in Ustilago maydis. Mol. Microbiol. 2004, 52, 823–835. [Google Scholar] [CrossRef]
- Rush, T.A.; Aime, M.C. The genus Meira: Phylogenetic placement and description of a new species. Antonie Van Leeuwenhoek 2013, 103, 1097–1106. [Google Scholar] [CrossRef] [PubMed]
- Kijpornyongpan, T.; Aime, M.C. Taxonomic revisions in the Microstromatales: Two new yeast species, two new genera, and validation of Jaminaea and two Sympodiomycopsis species. Mycol. Prog. 2017, 16, 495–505. [Google Scholar] [CrossRef]
- Albu, S.; Toome, M.; Aime, M.C. Violaceomyces palustris gen. et sp. nov. and a new monotypic lineage, Violaceomycetales ord. nov. in Ustilaginomycetes. Mycologia 2015, 107, 1193–1204. [Google Scholar] [CrossRef] [PubMed]
- Boekhout, T.; Gildemacher, P.; Theelen, B.; Müller, W.H.; Heijne, B.; Lutz, M. Extensive colonization of apples by smut anamorphs causes a new postharvest disorder. FEMS Yeast Res. 2006, 6, 63–76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, W.; Zhou, X.; Li, G.; Li, L.; Kong, L.; Wang, C.; Zhang, H.; Xu, J.R. Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog. 2011, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zabka, V.; Stangl, M.; Bringmann, G.; Vogg, G.; Riederer, M.; Hildebrandt, U. Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol. 2008, 177, 251–263. [Google Scholar] [CrossRef]
- Borges-Walmsley, M.I.; Walmsley, A.R. cAMP signalling in pathogenic fungi: Control of dimorphic switching and pathogenicity. Trends Microbiol. 2000, 8, 133–141. [Google Scholar] [CrossRef]
- Wongsuk, T.; Pumeesat, P.; Luplertlop, N. Fungal quorum sensing molecules: Role in fungal morphogenesis and pathogenicity. J. Basic Microbiol. 2016, 56, 440–447. [Google Scholar] [CrossRef]
- Boekhout, T.; Fonseca, A.; Sampaio, J.P.; Bandoni, R.J.; Fell, J.W.; Kwon-Chung, K.J. Discussion of Teleomorphic and Anamorphic Basidiomycetous Yeasts. In The Yeasts, a Taxonomic Study Volume 3; Kurtzman, C.P., Fell, J.W., Boekhout, T., Eds.; Elseiver: Burlington, MA, USA, 2011; pp. 1339–1371. [Google Scholar]
- Spellig, T.; Bölker, M.; Lottspeich, F.; Frank, R.W.; Kahmann, R. Pheromones trigger filamentous growth in Ustilago maydis. EMBO J. 1994, 13, 1620–1627. [Google Scholar] [CrossRef]
- Bölker, M.; Urban, M.; Kahmann, R. The a mating type locus of U. maydis specifies cell signaling components. Cell 1992, 68, 441–450. [Google Scholar] [CrossRef] [Green Version]
- Hartmann, H.A.; Kahmann, R.; Bolker, M. The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. Embo J. 1996, 15, 1632–1641. [Google Scholar] [CrossRef]
- Schirawski, J.; Heinze, B.; Wagenknecht, M.; Kahmann, R. Mating type loci of Sporisorium reilianum: Novel pattern with three a and multiple b specificities. Eukaryot. Cell 2005, 4, 1317–1327. [Google Scholar] [CrossRef] [Green Version]
- Yan, M.; Zhu, G.; Lin, S.; ** reveals stage-specific display of surface carbohydrates in in vitro and haemolymph- derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology 2009, 155, 3121–3133. [Google Scholar] [CrossRef] [Green Version]
- Manning, M.; Mitchell, T.G. Strain variation and morphogenesis of yeast- and mycelial-phase Candida albicans in low-sulfate, synthetic medium. J. Bacteriol. 1980, 142, 714–719. [Google Scholar] [CrossRef] [Green Version]
- Henninger, W.; Windisch, S. A New Yeast of Sterigmatomyces, S. aphidis sp. nov. Arch. Microbiol. 1975, 105, 49–50. [Google Scholar] [CrossRef]
- Boekhout, T. Pseudozyma Bandoni emend. for yeast-like anamorphs of Ustilaginales. J. Gen. Appl. Microbiol. 1995, 41, 359–366. [Google Scholar] [CrossRef]
- Doiphode, N.; Joshi, C.; Ghormade, V.; Deshpande, M. V Biotechnological Applications of Dimorphic Yeasts. In Yeast Biotechnology: Diversity and Applications; Satyanarayana, T., Kunze, G., Eds.; Springer: Berlin/Heidelberg, Germany, 2009; pp. 635–650. [Google Scholar]
- Ceccato-antonini, S.R.; Sudbery, P.E. Filamentous Growth in Saccharomyces cerevisiae. Braz. J. Microbiol. 2004, 35, 173–181. [Google Scholar] [CrossRef] [Green Version]
- Ruiz-herrera, J.; Campos-Góngora, E. An Introduction to Fungal Dimorphism. In Dimorphic Fungi: Their Importance as Models for Differentiation and Fungal Pathogenesis; Ruiz-herrera, J., Ed.; Bentham Science: Sharjah, UAE, 2012; pp. 3–15. [Google Scholar]
- Doëhlemann, G. Exobasidium vaccinii MPITM Genome sequencing. unpublished.
- Wickham, H. ggplot2: Elegant Graphics for Data Analysis; Springer: Berlin/Heidelberg, Germany, 2016; ISBN 3319242776. [Google Scholar]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- Emms, D.M.; Kelly, S. OrthoFinder: Solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015, 16, 157. [Google Scholar] [CrossRef] [Green Version]
Gene Name | Ustma GeneID | Acain | Cergu | Exova | Jamro | Malgl | Meimi | Moeap | Psean | Psehu | Psegl | Spore | Tescy | Tilan | Tilwa | Ustma | Viopa |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Msb2 | UMAG_00480 | ||||||||||||||||
Pra1 | UMAG_02383 | ||||||||||||||||
Sho1 | UMAG_03156 | ||||||||||||||||
Ump2 | UMAG_05889 | ||||||||||||||||
Adr1 | UMAG_04456 | ||||||||||||||||
Bpp1 | UMAG_00703 | ||||||||||||||||
Gpa3 | UMAG_04474 | ||||||||||||||||
Uac1 | UMAG_05232 | ||||||||||||||||
Ubc1 | UMAG_00525 | ||||||||||||||||
Ucn1 | UMAG_00936 | ||||||||||||||||
Uka1 | UMAG_11860 | ||||||||||||||||
Umpde1 | UMAG_02531 | ||||||||||||||||
Umpde2 | UMAG_10895 | ||||||||||||||||
Crk1 | UMAG_11410 | ||||||||||||||||
Fuz7/Ubc5 | UMAG_01514 | ||||||||||||||||
Kpp2/Ubc3 | UMAG_03305 | ||||||||||||||||
Kpp4/Ubc4 | UMAG_04258 | ||||||||||||||||
Kpp6 | UMAG_02331 | ||||||||||||||||
Rok1 | UMAG_03701 | ||||||||||||||||
Ubc2 | UMAG_05261 | ||||||||||||||||
Cla4 | UMAG_10145 | ||||||||||||||||
Pdc1 | UMAG_01366 | ||||||||||||||||
Ras1 | UMAG_01643 | ||||||||||||||||
Ras2 | UMAG_03172 | ||||||||||||||||
Rho1 | UMAG_05734 | ||||||||||||||||
Sql2 | UMAG_10803 | ||||||||||||||||
Biz1 | UMAG_02549 | ||||||||||||||||
Chs5 | UMAG_10277 | ||||||||||||||||
Chs7 | UMAG_05480 | ||||||||||||||||
Cib1 | UMAG_11782 | ||||||||||||||||
Clb2 | UMAG_10279 | ||||||||||||||||
Clp1 | UMAG_02438 | ||||||||||||||||
Gcn5 | UMAG_10190 | ||||||||||||||||
Hap2 | UMAG_01597 | ||||||||||||||||
Hgl1 | UMAG_11450 | ||||||||||||||||
Hos2 | UMAG_11828 | ||||||||||||||||
Khd4 | UMAG_03837 | ||||||||||||||||
Kin1 | UMAG_04218 | ||||||||||||||||
Kin3 | UMAG_06251 | ||||||||||||||||
Mcs1 | UMAG_03204 | ||||||||||||||||
Med1 | UMAG_03588 | ||||||||||||||||
Myo5 | UMAG_04555 | ||||||||||||||||
Nit2 | UMAG_10417 | ||||||||||||||||
Pac2 | UMAG_15096 | ||||||||||||||||
Prf1 | UMAG_02713 | ||||||||||||||||
Rac1 | UMAG_00774 | ||||||||||||||||
Rak1 | UMAG_10146 | ||||||||||||||||
Rbf1 | UMAG_03167 | ||||||||||||||||
Rop1 | UMAG_12033 | ||||||||||||||||
Ros1 | UMAG_05853 | ||||||||||||||||
Rrm4 | UMAG_03494 | ||||||||||||||||
Sep3 | UMAG_03449 | ||||||||||||||||
Tea1 | UMAG_15019 | ||||||||||||||||
Tea4 | UMAG_01012 | ||||||||||||||||
Tup1 | UMAG_03280 | ||||||||||||||||
Yup1 | UMAG_05406 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kijpornyongpan, T.; Aime, M.C. Investigating the Smuts: Common Cues, Signaling Pathways, and the Role of MAT in Dimorphic Switching and Pathogenesis. J. Fungi 2020, 6, 368. https://doi.org/10.3390/jof6040368
Kijpornyongpan T, Aime MC. Investigating the Smuts: Common Cues, Signaling Pathways, and the Role of MAT in Dimorphic Switching and Pathogenesis. Journal of Fungi. 2020; 6(4):368. https://doi.org/10.3390/jof6040368
Chicago/Turabian StyleKijpornyongpan, Teeratas, and M. Catherine Aime. 2020. "Investigating the Smuts: Common Cues, Signaling Pathways, and the Role of MAT in Dimorphic Switching and Pathogenesis" Journal of Fungi 6, no. 4: 368. https://doi.org/10.3390/jof6040368