Decarboxylation of indoleacetic acid illuminates its evolution into a plant hormone

The evolution of indoleacetic acid (IAA) into the plant hormone auxin remains unclear. Here, we compared IAA response and metabolism in land plants and their closest living relatives, the streptophyte algae, using chemical treatments, phytohormone profiling, and targeted and untargeted metabolomics. Streptophyte algae showed neither plant-like auxin responses nor canonical IAA metabolism. Here, we demonstrate IAA side-chain decarboxylation as a novel pathway of cellular IAA metabolism, operating in streptophyte algae and land plants alike. Decarboxylation also underpinned IAA’s innate photolability and yielded cytotoxic intermediates, which also accumulated endogenously under simulated sunlight. Together, these findings establish IAA decarboxylation as a major, conserved metabolic pathway, and suggest that the metabolic constraints arising from IAA’s instability and indirect cytotoxicity contributed to its adoption as a plant hormone.