Transcriptional regulatory sequences control when and where genes are transcribed. While plants and animals evolved the mechanisms for cell-type-specific gene expression separately, our understanding of transcription regulation in plants is mostly extrapolated from animal systems. In this work, we explore how transcription-regulatory sequences are organized in A. thaliana. We found that transcription factor binding sites and expression quantitative trait loci (eQTLs) are enriched downstream of the transcription start site (TSS). Using a massively parallel reporter assay, we directly demonstrate that sequences downstream of the TSS control transcription, and lose this ability when positioned upstream to the TSS. This position-dependent effect is unique to plants as opposed to animal enhancers, which are indifferent to relative position. Our study provide insight on the divergence of transcription-regulatory sequences between animals and plants.