Mapping and dynamics of the regulatory DNA landscape in A. thaliana

This study establishes nucleotide-resolution regulatory DNA landscapes and their dynamics in response to environmental cues such as light and heat, key to shaping plant growth and development, by mapping DNase I hypersensitive site (DHSs) combined with genomic footprinting.

HFSP Long-Term Fellow Janne Lempe and colleagues
authored on Fri, 31 October 2014

Plants are sessile organisms for which the capability to respond appropriately to environmental cues is essential. Numerous studies consider responses to environmental cues at the level of gene expression. However, cis-regulatory changes controlling expression remained largely unknown. Here we used DNase I hypersensitive site mapping in Arabidopsis thaliana seedlings and genomic footprinting to delineate approximately 700,000 sites of in vivo transcription factor occupancy at nucleotide resolution and derived an extensive cis-regulatory lexicon for A. thaliana (http://plantregulome.org).

Figure by Alessandra Sullivan

Many extracted transcription factor binding motifs were novel, with many sites showing evidence of recent purifying selection, and a significant number colocalizing with single nucleotide variants associated with trait variance in genome-wide association studies. Most of the footprints reside in intergenic regions, transcriptional start sites, UTRs and Introns. Fourteen percent, however, lie within exons, in regions that are coding for both amino acids and transcription factor binding. This dual usage may have shaped codon usage patterns. Interestingly, the identity of such dual codons differed substantially between humans and A. thaliana.

We determined dynamics of DNase I hypersensitive sites in response to light and heat as major environmental cues modulating plant growth and development, clustered them into accessibility patterns and identified genes that previously were unknown to act in such pathways. Knowledge on transcription factor occupancy allowed construction of transcription factor networks and analysis of their dynamics and architectural features. The architecture of A. thaliana transcription factor networks is strikingly similar to animals despite the large phylogenetic distance. The transcription factor network response to light is characterized by a substantial rewiring between groups of transcription factors, particularly in autoregulatory feedback loops.   The response to heat shows a net loss of network edges mediating the repressive role of the heat shock response.

Reference

Mapping and Dynamics of Regulatory DNA and Transcription Factor Networks in A. thaliana. Alessandra M. Sullivan, Andrej A. Arsovski, Janne Lempe, Kerry L. Bubb, Matthew T. Weirauch, Peter J. Sabo, Richard Sandstrom, Robert E. Thurman, Shane Neph, Alex P. Reynolds, Andrew B. Stergachis, Benjamin Vernot, Audra K. Johnson, Eric Haugen, Shawn T. Sullivan, Agnieszka Thompson, Fidencio V. Neri III, Molly Weaver, Morgan Diegel, Sanie Mnaimneh, Ally Yang, Timothy R. Hughes, Jennifer L. Nemhauser, Christine Queitsch* and John A. Stamatoyannopoulos*: Cell reports 204, 8(6):205-2030.

Pubmed link