The Transcription Factors Tec1 and Ste12 Interact with Coregulators Msa1 and Msa2 To Activate Adhesion and Multicellular Development

Abstract

In Saccharomyces cerevisiae and related yeast species, the TEA transcription factor Tec1, together with a second transcription factor, Ste12, controls development, including cell adhesion and filament formation. Tec1-Ste12 complexes control target genes through Tec1 binding sites (TEA consensus sequences [TCSs]) that can be further combined with Ste12 binding sites (pheromone response elements [PREs]) for cooperative DNA binding. The activity of Tec1-Ste12 complexes is known to be under negative control of the Dig1 and Dig2 (Dig1/2) transcriptional corepressors that confer regulation by upstream signaling pathways. Here, we found that Tec1 and Ste12 can associate with the transcriptional coregulators Msa1 and Msa2 (Msa1/2), which were previously found to associate with the cell cycle transcription factor complexes SBF (Swi4/Swi6 cell cycle box binding factor) and MBF (Mbp1/Swi6 cell cycle box binding factor) to control G₁-specific transcription. We further show that Tec1-Ste12-Msa1/2 complexes (i) do not contain Swi4 or Mbp1, (ii) assemble at single TCSs or combined TCS-PREs in vitro, and (iii) coregulate genes involved in adhesive and filamentous growth by direct promoter binding in vivo. Finally, we found that, in contrast to Dig proteins, Msa1/2 seem to act as coactivators that enhance the transcriptional activity of Tec1-Ste12. Taken together, our findings add an additional layer of complexity to our understanding of the control mechanisms exerted by the evolutionarily conserved TEA domain and Ste12-like transcription factors.

SUPPLEMENTAL MATERIAL

Supplemental material for this article may be found at http://dx.doi.org/10.1128/MCB.01599-13.

ACKNOWLEDGMENTS

We thank Michael Knop and Florian Bauer for generous gifts of plasmids. We are grateful to Konstanze Bandmann, Patrick Berndt, Raphael Birke, and Christof Taxis for help with some of the experiments and Diana Kruhl for technical assistance.

This work was supported by grants from the Deutsche Forschungsgemeinschaft (GRK 1216; SFB 987) and by the Marburg Center for Synthetic Microbiology (SYNMIKRO).