Auxin is a signaling molecule that regulates multiple processes in the growth and development of land plants. Research gathered from model species, particularly Arabidopsis thaliana, has revealed that the nuclear auxin pathway controls many of these processes through transcriptional regulation. Recently, a non-transcriptional pathway based on rapid phosphorylation mediated by kinases has been described, complementing the understanding of the complexity of auxin-regulated processes. Phylogenetic inferences of both pathways indicate that only some of the components are conserved beyond land plants. This raises fundamental questions about the evolutionary origin of auxin responses and whether algal sisters share mechanistic features with land plants. Here we explore auxin responses in the unicellular streptophyte alga Penium margaritaceum. By assessing physiological, transcriptomic and cellular responses we found that auxin triggers cell proliferation, gene regulation and acceleration of cytoplasmic streaming. Notably, all these responses are also triggered by the structurally related tryptophan. These results identify shared auxin response features among land plants and algae, and suggest that less chemically specific responses preceded the emergence of auxin-specific regulatory networks in land plants.