The dually targeted transcription factor TF1 and its role in the expression of plastid- and nuclear-encoded photosynthesis genes

Abstract

In plant cells, the distribution of genes on three spatially separated subgenomes calls for the necessity of maintaining a coordinated regulation of gene expression between these DNA-containing compartments. Especially, the translocation of nuclear-encoded gene products to plastids and mitochondria, which is crucial for the development and metabolic operation of these semi-autonomous organelles, requires continuous intercompartmental communication. This correspondence is provided by anterograde and retrograde pathways, involving nucleus-to-plastid and plastid-to-nucleus signalling, respectively. Because of their ability to target more than one DNA-containing compartment, dually targeted transcription factors have been suggested as possible participators in coordination of gene expression between subgenomes. In this study, the effect of the plastid- and nucleus-targeted AP2/EREBP transcription factor TF1 on the expression of plastid- and nuclear-encoded photosynthesis genes was investigated using run-on transcription assays and RT-qPCR, respectively. The comparison of transcription rates between a TF1 knock-down mutant (∆TF1) and wild type (WT) Arabidopsis thaliana at different points in the 24 hours day/night cycle revealed that expression of the TF1 gene is required for light-promoted transcription of the plastid-encoded photosynthesis genes psaA, psaB, psbA and rbcL. In contrast, the light-induced increase in transcription of the nuclear photosynthesis genes RBCS1A and PSBO2 was not dependent on TF1. This observation would suggest a dual role for TF1 in the light-regulated transcription of plastid-encoded photosynthesis genes and in the retrograde pathway maintaining coordinated transcription of these genes with the corresponding nuclear genes. Yeast one-hybrid assays identified two DNA sequence-motifs which were specifically bound by TF1, namely the DRE motif (TACCGACAT) and the inverted and mutated GCC box (GGAGGAT). The discovery of these DNA-motifs in the promoter regions of the TF1-regulated genes psbA and psaA/B indicated that TF1 might directly target these genes. Ultimately, the data obtained in this study, together with previously obtained information regarding this dually targeted transcription factor, lead to the proposal of a tentative model for the functional role of TF1 in the light-mediated coordination of gene expression in plastids and the nucleus, which will serve as a basis for further experiments.