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<p>Abstract</p> <p>Background</p> <p>The plant hormone auxin directs many aspects of plant growth and development. To understand the evolution of auxin signalling, we compared the genes encoding two families of crucial transcriptional regulators, <it>AUXIN RESPONSE FACTOR </it>(<it>ARF</it>) and <it>AUXIN/INDOLE-3-ACETIC ACID </it>(<it>Aux/IAA</it>), among flowering plants and two non-seed plants, <it>Physcomitrella patens </it>and <it>Selaginella moellendorffii</it>.</p> <p>Results</p> <p>Comparative analysis of the <it>P. patens, S. moellendorffii </it>and <it>Arabidopsis thaliana </it>genomes suggests that the well-established rapid transcriptional response to auxin of flowering plants, evolved in vascular plants after their divergence from the last common ancestor shared with mosses. An N-terminally truncated ARF transcriptional activator is encoded by the genomes of <it>P. patens </it>and <it>S. moellendorffii</it>, and suggests a supplementary mechanism of nuclear auxin signalling, absent in flowering plants. Site-specific analyses of positive Darwinian selection revealed relatively high rates of synonymous substitution in the <it>A. thaliana </it>ARFs of classes IIa (and their closest orthologous genes in poplar) and Ib, suggesting that neofunctionalization in important functional regions has driven the evolution of auxin signalling in flowering plants. Primary auxin responsive gene families (GH3, SAUR, LBD) show different phylogenetic profiles in <it>P. patens</it>, <it>S. moellendorffii </it>and flowering plants, highlighting genes for further study.</p> <p>Conclusion</p> <p>The genome of <it>P. patens </it>encodes all of the basic components necessary for a rapid auxin response. The spatial separation of the Q-rich activator domain and DNA-binding domain suggests an alternative mechanism of transcriptional control in <it>P. patens </it>distinct from the mechanism seen in flowering plants. Significantly, the genome of <it>S. moellendorffii </it>is predicted to encode proteins suitable for both methods of regulation.</p>