A Genome-Scale TF-DNA Interaction Network of Transcriptional Regulation of Arabidopsis Primary and Specialized Metabolism

Abstract

In single-celled microbes, transcriptional regulation by single transcription factors is sufficient to shift primary metabolism. Corresponding genome-level transcriptional regulatory maps of metabolism reveal the underlying design principles responsible for these shifts as a model in which master regulators largely coordinate specific metabolic pathways. Relative to individual microbes, plant metabolism is more complex. Primary and specialized metabolism occur within innumerable cell types, and their reactions shift depending on internal and external cues. Given the importance of plants and their metabolites in providing humanity with food, fiber and medicine, we set out to develop a genome-scale transcriptional regulatory map of Arabidopsis metabolic genes. A comprehensive set of protein-DNA interactions between Arabidopsis thaliana transcription factors and promoters of primary metabolism and specialized metabolism were mapped. To demonstrate the utility of this resource, we identified and functionally validated regulators of the TCA cycle. The resulting network suggests that plant metabolic design principles are distinct from that of microbes. Instead, metabolism appears to be transcriptionally coordinated via developmental- and stress-conditional processes that can coordinate across primary and specialized metabolism. These data represent the most comprehensive resource of interactions between TFs and metabolic genes in plants.

Chemical Imaging Reveals Diverse Functions of Tricarboxylic Acid Metabolites in Root Growth and Development

“…We found spatially distinctive distribution patterns of several classes of TCA biosynthesis genes (Fig. 3a), which match localization signatures identified in a separate study of Arabidopsis roots 8 . In particular, ACONITASE ( ACO ) and SUCCINATE-COENZYME A LIGASE ( SCL ) gene expression levels in Arabidopsis correlated with the metabolite distributions observed in maize roots, suggesting that the developmental distribution of TCA metabolites is conserved across evolutionarily divergent plants.…”

“…Between 20 to 30 small molecules were localized per each developmental zone (Supplementary Figs. [8][9][10]. We hypothesized that these enrichment patterns might predict developmental functions.…”

The trade-off function of photorespiration in a changing environment

“…Depending on the regulatory stetting, a single regulatory interaction can be beneficial or detrimental for the system stability. Further, although a vast amount of data and information is available on regulatory interplay between genes, proteins metabolites, e.g., provided by genome-scale metabolic networks (Tang et al, 2021), many regulatory and metabolic interactions can be assumed to remain elusive or unknown. Affirmatively, even in long studied and well-known biochemical reaction networks, new reactions or regulatory interactions are still being discovered.…”

Feature Importance Network reveals novel functional relationships between biological features inArabidopsis thaliana

“…Machine learning can be also used to infer gene regulatory networks. For example, a study showed that plant metabolism is transcriptionally coordinated via developmental and stress conditional processes 10 . Another approach, named EXPLICIT (Expression Prediction via Log- linear Combination of Transcription Factors), correctly predicted gene expression patterns from transcription factor information.…”