Fluctuations in the supply of soil nitrogen (N) cause profound alterations in the transcriptome of plants, allowing improved N acquisition, allocation and remobilization. In Arabidopsis thaliana, N starvation-induced CEPD (C-TERMINALLY ENCODED PEPTIDE DOWNSTREAM) proteins are required for transcriptional activation of genes involved in efficient nitrate uptake by roots. CEPDs belong to a plant-specific class of glutaredoxin-like proteins (called ROXYs in A. thaliana) that interact with TGACG-binding transcription factors (TGAs). Here we show that TGA1 and TGA4 act as molecular links between CEPDs/ROXY6-9 and target promoters in roots. In the absence of CEPDs/ROXYs 6-9, TGA1/4 recruit a strong repressive complex. In wild-type plants, this repressive complex is dysfunctional and transcriptional activation upon N starvation is most likely regulated by the increased ratio of CEPDs/ROXYs 6-9 over antagonistically acting ROXYs encoding the TOPLESS-interacting ALWL motif. TGA1/4 are required for transcriptional repression on full N supply and/or for transcriptional activation under N starvation, depending on the promoter and on the exact composition of the medium. Although CEPDs/ROXY6-9 resemble glutaredoxins with glutathione-dependent oxidoreductase activity, complementation analysis with ROXY9 variants encoding mutations in the active site excludes that ROXY9 functions by altering the redox state of target proteins.