Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat-stress responses

Abstract The post-translational protein modification known as SUMOylation has conserved roles in heat-stress responses in various species. The functional connection between the global regulation of gene expression and chromatin-associated SUMOylation in plant cells is unknown. Here we uncovered a genome-wide relationship between chromatin-associated SUMOylation and transcriptional switches in Arabidopsis thaliana grown at room temperature, after heat stress, and after heat stress followed by recovery. The small ubiquitin-like modifier (SUMO)-associated chromatin sites, as characterized by whole-genome ChIP-seq, were generally associated with active chromatin markers. In response to heat stress, chromatin-associated SUMO signals increased at promoter-transcriptional start site regions and decreased in gene bodies. RNA-seq analysis supported the role of chromatin-associated SUMOylation in transcriptional activation during rapid responses to high temperature. Changes in SUMO signals on chromatin were associated with the upregulation of heat-responsive genes and the downregulation of growth-related genes. Disrupting the SUMO ligase gene SIZ1 abolished SUMO signals on chromatin and attenuated rapid transcriptional responses to heat stress. The SUMO signal peaks were enriched in DNA elements recognized by distinct groups of transcription factors under different temperature conditions. These observations provide evidence that chromatin-associated SUMOylation regulates the transcriptional switch between development and heat-stress responses in plant cells.