Transcription Factor Action Orchestrates the Complex Expression Pattern of CRABS CLAW in Arabidopsis.

Thomas Gross,Annette Becker

doi:10.3390/genes12111663

Abstract

Angiosperm flowers are the most complex organs that plants generate, and in their center, the gynoecium forms, assuring sexual reproduction. Gynoecium development requires tight regulation of developmental regulators across time and tissues. How simple on and off regulation of gene expression is achieved in plants was described previously, but molecular mechanisms generating complex expression patterns remain unclear. We use the gynoecium developmental regulator CRABS CLAW (CRC) to study factors contributing to its sophisticated expression pattern. We combine in silico promoter analyses, global TF-DNA interaction screens, and mutant analyses. We find that miRNA action, DNA methylation, and chromatin remodeling do not contribute substantially to CRC regulation. However, 119 TFs, including SEP3, ETT, CAL, FUL, NGA2, and JAG bind to the CRC promoter in yeast. These TFs finetune transcript abundance as homodimers by transcriptional activation. Interestingly, temporal–spatial aspects of expression regulation may be under the control of redundantly acting genes and require higher order complex formation at TF binding sites. Our work shows that endogenous regulation of complex expression pattern requires orchestrated transcription factor action on several conserved promotor sites covering almost 4 kb in length. Our results highlight the utility of comprehensive regulators screens directly linking transcriptional regulators with their targets.

Highlights

Transcription is a universal process in which DNA is transcribed into mRNA that is exported from the nucleus and translated into protein sequence
We find that transcription factor (TF) involved in several developmental pathways coordinate CRABS CLAW (CRC) expression via transcriptional activation, such as TFs directing flowering induction, floral organ identity and meristem regulation, and that most of them are only partially co-expressed with CRC
We were first interested in understanding the contribution of the different means of transcriptional regulation of CRC expression

Summary

Introduction

Transcription is a universal process in which DNA is transcribed into mRNA that is exported from the nucleus and translated into protein sequence. Prokaryotes tightly regulate transcription for the proper timing of cellular development and metabolic processes. The prokaryotic way to control expression is different to eukaryotes, as co-functional genes are often grouped in co-regulated polycistronic operons (reviewed in [1]). Genes involved in the same processes are distributed over the entire genome, such that every gene requires its individual regulatory sequence. The promoter regions of eukaryotic genes are longer than those of prokaryotes, and they include more transcription factor binding sites, accession points for chromatin remodelers. Distal regulatory elements such as enhancers or silencers can be many kilobases away from the transcription start site [2]

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