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. 2020 Apr 28;10(7):2141–2157. doi: 10.1534/g3.120.401040

Table 3. Comparison of major biological and physiological processes of metamorphosis in key pathogenic dimorphic fungi.

Fungus Disease Pathogenicity and virulence Morphogenetic induction Cell-wall organization Oxidative stress Secondary metabolism Reference
Insect pathogens Metarhizium anisopliae (Ascomycota; Sordariomycetes; Hypocreales; Clavicipitaceae) Green muscardine Infective propagules are conidia and single-celled yeast-like phase (blastospores). Blastospores have been shown to be more virulent that aerial conidia toward arthropodes. Blastospores are induced during growth inside insects and in liquid media with agitation. Unknown inducing conditions (Suggested factors: high osmotic pressure and oxidative stress) Numerous enzymes involved in cell-wall synthesis and breakdown are differentially regulated between dimorphic forms. Blastospores has thinner cell walls then hyphae and it is composed by glucans and chitin. Blastospores experience oxidative stress in vitro and produces enzymes such as catalases and peroxidases. Nonribosomal peptides, Polyketides and Terpenoids are differnetially expressed between growth forms. The most well known are Destruxins and Cytochalasins. [This study, Wang and Leger 2006, Sbaraini et al. 2016 ]
Beauveria bassiana (Ascomycota; Sordariomycetes; Hypocreales; Cordycipitaceae) White muscardine Blastospores experience oxidative stress in vivo and produces catalases, intracellular polyol accumulation, activation of high osmolarity glycerol (Hog1) MAP‐kinase pathways and superoxide dismutases (SODs). Polyketides like oosporein, bassianin and tenellin, nonribosomally peptides like beauvericin, bassianolides and beauveriolides are differentially expressed between growth forms. [Bidochka et al. 1987, Tartar et al. 2005, Xiao et al. 2012, Wang et al. 2013, Ortiz-Urquiza and Keyhani (2016)]
Plant patogens Ophiostoma novo-ulmi (Ascomycota; Sordariomycetes; Ophiostomatales; Ophiostomataceae) Dutch elm disease. Spread by elm beetles from family Curculionidae. The fungus invades vascular system of trees. Both hyphae and yeast play a role in pathogenicity. Yeast-phase is induced during growth inside of the vascular system of trees. Nitrogen source, proline aminoacid, salicylic acid (cyclooxygenase inhibitor), and oxylipins induce yeast-phase in vitro. Chitin synthases and aminoglycan metabolite process are highly expressed in mycelium. Glycoside hydroxylases and glycosyltransferases are expressed differently in yeast and mycelium. Yeast phase show an increase in catalase production and increase in oxidation-reducing processes. Produces nonribosomal peptides, some polyketides produced only in mycelial phase, siderophore biosynthesis, fujikurin-like compounds produced in both yeast and mycelial phases. Jensen et al. 1992, Naruzawa and Bernier, 2014,Nigg et al. 2015, Sbaraini et al. 2017
Ustilago maydis (Basidiomycota; Ustilaginomycetes; Ustilaginales; Ustilaginaceae) Corn smut Yeast phase is saprophytic while hyphae are pathogenic induce formation of host tumors in maize. Mating interaction, nutrient starvation, Ph, pheromones β-1,6-glucan synthesis, N-glycosylation membrane proteins, hydrophobins and chitin synthase, glycosidases and others polymers are differentially expressed between filamentous and yeast phases. Hyphae experience oxidative stress during proliferation in host tissue and respond to host ROS by producing ROS‐detoxifying enzymes phospholipase and Superoxide dismutase. Many polyketides and non-ribosomal peptides, siderophores, indole pigments, ferrichrome, Pityriacitrin, and ustilagic acid are differentially expressed between growth phases. Banuett and Herskowitz, 1994, Sánchez-Martínez and Pérez-Martín, 2001, Bölker et al. 2008, García-Pedrajas et al. 2010, Robledo-Briones and Ruiz-Herrera, 2013, Kunst et al. 2016
Human pathogens Candida albicans (Ascomycota; Saccharomycetes; Saccharomycetales; Saccharomycetaceae Candidiasis Commensal fungus. Both yeast and filamentous phase are important for full virulence Temperature, Ph, nutrient deprivation, quorum sensing Differences in composition of cell walls between yeast and mycelial phase. High amount of chitin in hyphae, while the amount of glucans and mannoproteins are similar between both fungal structures. Fungus experiences oxidative stress induced by macrophages during proliferation in host tissue. Produces catalases, gluthatione peroxidases and other antioxidants in response. Produce many secondary metabolites like farnesol that inhibits transition from the yeast to hyphae. Farnesol protect Candida from oxidative stress. Sánchez-Martínez and Pérez-Martín, 2001, Albuquerque and Casadevall (2012), François et al. 2013, Ruiz-Herrera et al. 2006, Whiteway and Bachewich, 2007, Dufour and Rao, 2011, Dantas et al. 2015
Paracoccidioides brasiliensis (Ascomycota; Eurotiomycetes; Onygenales; Ajellomycetaceae) Both yeast and filamentous phase are important for virulence. Hyphae undergo thermal-induced differentiation into a yeast phase inside host lungs. Temperature Reorganization of membrane lipids and carbohydrate polymers. Increase in chitin content in yeast. α-glucan and β-glucan as main polysaccharides in the cell wall of yeast and hyphae, respectively. Hydrophobins are mycelium specific. Oxidative stress in yeast phase results in production of superoxide dismutases, catalase, and glutathione peroxidase thiol-specific antioxidant gene (TSA1) protects against ROS and RNIs. Genes encoding enzymes involved in terpenoid and melanin biosynthesis are present. Albuquerque et al. 2004, Nunes et al. 2005, Tomazett et al. 2005,
Talaromyces marneffei (Ascomycota; Eurotiomycetes; Eurotiales; Trichocomaceae) Penicilliosis Filamentous phase is saprophytic while yeast-like cells are pathogenic. Causes disease especially in immunocompromised patients. Melanins in yeast form protects from host immune system. Temperature Several enzymes involved with changes in cytoskeletal organization during morphogenesis. Cell wall composition of yeast and mycelia are different. Fungus experience oxidative stress induced by macrophages during proliferation in host tissue. It produces superoxide dismutase and catalases during macrophage infection and yeast growth. Secondary metabolism in both growth phases. Polyketides involved in biosynthesis of pigments like melanin during yeast growth and red pigments in mycelium. Cooper and Vanittanakom, 2008, Boyce et al. 2013, Tam et al. 2015