Considering that hundreds of transcription factors and regulators are subject to sumoylation, we are interested in studying how cells use sumoylation to regulate gene expression. We performed a ChIP-seq analysis in budding yeast with a SUMO antibody which showed that the bulk of chromatin-associated sumoylation is found on tRNA genes and ribosomal protein genes (RPGs), which is consistent with other studies. However, we also found that 147 non-RPG protein-coding genes have a distinct SUMO peak upstream of their TSS. These SUMO peaks overlap closely with ChIP-seq peaks for TBP, the major component of TFIID, suggesting that TBP itself, or a closely associated component of the RNA polymerase II (RNAPII) pre-initiation complex (PIC) is sumoylated at these genes. Supporting this, among PIC components tested, we found that TBP, TFIIF and RNAPII are significantly sumoylated in normally growing yeast.
Eukaryotic cells coordinately modulate overall sumoylation levels with changing environmental conditions. To explore whether modulated cellular sumoylation levels affect gene expression patterns, we performed RNAPII ChIP-seq in a yeast strain that harbours significantly reduced sumoylation levels, ubc9-6. Indeed, 750 genes showed altered RNAPII occupation levels in this strain. Those with >2-fold reduction in RNAPII occupancy are largely involved in amino acid biosynthesis, whereas most with >2-fold increase in RNAPII levels are involved in translation, including most RPGs. Mutant yeast strains with low sumoylation levels, such as ubc9-6, have impaired growth at high temperatures. Consistent with this, RNAPII ChIP-seq analysis in ubc9-6 showed dramatically deregulated redistribution of RNAPII across the genome after heat shock. Together, our findings demonstrate that sumoylation regulates a subset of protein-coding genes during normal growth conditions and suggests that sumoylation can function pre-emptively to prepare yeast for the transcriptional response needed to survive high temperatures.