The plant hormone auxin triggers a wide range of developmental and growth responses throughout a plant’s life. Most well-known auxin responses involve changes in gene expression that are mediated by a short pathway involving an auxin-receptor/ubiquitin-ligase, DNA-binding auxin response factor (ARF) transcription factors and their interacting auxin/indole-3-acetic acid (Aux/IAA) transcriptional inhibitors. Auxin promotes the degradation of Aux/IAA proteins through the auxin receptor and hence releases the inhibition of ARF transcription factors. Although this generic mechanism is now well understood, it is still unclear how developmental specificity is generated and how individual gene family members of response components contribute to local auxin responses. We have established a collection of transcriptional reporters for the ARF gene family and used these to generate a map of expression during embryogenesis and in the primary root meristem. Our results demonstrate that transcriptional regulation of ARF genes generates a complex pattern of overlapping activities. Genetic analysis shows that functions of co-expressed ARFs converge on the same biological processes, but can act either antagonistically or synergistically. Importantly, the existence of an ‘ARF pre-pattern’ could explain how cell-type-specific auxin responses are generated. Furthermore, this resource can now be used to probe the functions of ARF in other auxin-dependent processes.