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Conserved and Distinct Functions of the “Stunted” (StuA)-Homolog Ust1 During Cell Differentiation in the Corn Smut Fungus Ustilago maydis

¹Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora”, Universidad de Málaga, Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Estación Experimental “La Mayora”, 29750 Algarrobo-Costa, Málaga, Spain; ²United States Department of Agriculture–Agricultural Research Service, Russell Research Center, Toxicology & Mycotoxin Research Unit, Athens, GA 30605, U.S.A.; ³Department of Cellular and Molecular Biology, Centro de Investigaciones Biológicas (CSIC), 28040 Madrid, Spain

Ustilago maydis, causal agent of corn smut, can proliferate saprobically in a yeast form but its infectious filamentous form is an obligate parasite. Previously, we showed that Ust1, the first APSES (Asm1p, Phd1p, Sok2p, Efg1p, and StuAp) transcription factor functionally characterized in the phylum Basidiomycota, controlled morphogenesis and virulence in this species. Here, we further analyzed Ust1 function using multiple experimental approaches and determined that i) Ust1 activity was able to partially reverse stuA⁻ conidiophore defects in Aspergillus nidulans; ii) in U. maydis, normal development and virulence were strongly dependent on precise induction or repression of Ust1 activity; iii) consistent with its role as a transcription factor regulating multiple processes, Ust1 accumulated in the nucleus at various stages of the life cycle; iv) however, it was undetectable at specific stages of pathogenic growth, indicating that Ust1 repression is part of normal development in planta; v) StuA response elements upstream of the ust1 open reading frame exhibited affinity for U. maydis DNA-binding proteins; vi) however, loss of regulated ust1 transcription had minor phenotypic effects; and vii) Ust1 was subject to post-translational phosphorylation but is not a target of cAMP signaling. Thus, the broad functional conservation between Ust1 and Ascomycota APSES proteins does not extend to the mechanisms regulating their activity.