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Title: Conserved and distinct functions of the "stunted" (StuA)-Homolog Ust1 during cell differentiation in the corn smut fungus Ustilago maydis

Author
item BAEZA-MONTANEZ, LOURDES - Ihsm-Uma-csic, Estación Experimental “la Mayora”
item Gold, Scott
item ESPESO, EDUARDO - Ihsm-Uma-csic, Estación Experimental “la Mayora”
item GARCIA-PEDRAJAS, MARIA - Ihsm-Uma-csic, Estación Experimental “la Mayora”

Submitted to: Molecular Plant Microbe International Symposium
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/3/2014
Publication Date: 1/1/2015
Citation: Baeza-Montanez, L., Gold, S.E., Espeso, E.A., Garcia-Pedrajas, M.D. 2015. Conserved and distinct functions of the "stunted" (StuA)-Homolog Ust1 during cell differentiation in the corn smut fungus Ustilago maydis. Molecular Plant Microbe International Symposium. 28(1):86-102.

Interpretive Summary: Fungal plant pathogens display a number of strategies to penetrate their hosts, overcome plant defense mechanisms, and colonize plant tissue. These include morphological and metabolic changes and production of toxins and secreted proteins. Transcription factors of the APSES family, unique to fungi, have been functionally characterized in a number of species including animal and plant pathogens. They control morphogenesis, and other cellular processes relevant to disease development such as primary and secondary metabolism and the production of secreted proteins. In previous work we found that the APSES protein Ust1 is a key regulator of morphogenesis and virulence in the corn smut fungus, U. maydis. Here we provided further evidence that Ust1 functions as a transcription factor playing key roles at different stages of saprobic and parasitic growth, and we propose a model describing sequential changes in its activity required for the successful completion of the U. maydis morphogenetic program in planta. We also show that although there is broad functional conservation among APSES proteins, the mechanisms and pathways regulating Ust1 appear to be distinct. The results presented increase the potential of using the manipulation of this protein activity to molecularly analyze U. maydis features normally associated with obligate parasitism.

Technical Abstract: Ustilago maydis, causal agent of corn smut, is a model for obligate fungal plant pathogens because, although it can proliferate saprobically in its yeast form, the infectious filamentous form is absolutely dependent on the host to complete its life cycle. Maize responds to U. maydis colonization by producing tumorous structures, where the fungus produces melanized sexual teliospores. Previously we identified a regulatory protein (Ust1) encoded by gene um15042, with critical roles in morphogenesis and virulence. Ust1 is an APSES family transcription factor, and was the first protein of this class functionally characterized in the phylum Basidiomycota. Here we further analyzed Ust1 function using multiple experimental approaches and determined that: (1) Ust1 was able to regulate APSES protein StuA target genes in Aspergillus nidulans, partially reversing stuA- conidiophore defects; (2) in U. maydis, normal development and virulence were strongly dependent on precise regulation of Ust1 activity which was required for unicellular budding growth, and for distinct critical roles during pathogenic development; (3) tagging of Ust1 with mCherry revealed strong nuclear localization at various stages of the U. maydis life cycle, consistent with its role as a transcription factor regulating multiple processes; (4) however, Ust1::mCherry was undetectable at specific stages of pathogenic development, indicating that repression of this activity is part of normal development in planta; (5) StuA response elements (A/TCGCGT/ANA/C) upstream of the ust1 open reading frame exhibited affinity in vitro for U. maydis regulatory protein(s); (6) however, in contrast with well characterized APSES protein genes in Ascomycota, loss of regulated ust1 transcription had minor effects on the processes controlled by Ust1 activity; (7) Ust1 was subject to post-translational phosphorylation but unlike other APSES proteins it is not a target of cAMP signaling. Thus, although there is broad conservation of functions between Ust1 and APSES proteins from Ascomycota, there are also important differences especially regarding the mechanisms and pathways regulating their activity.