Auxin, a key plant hormone, regulates growth and development through two distinct receptor systems. The well-established transport inhibitor response 1 (TIR1)/auxin-signaling F-box protein (AFBs) pathway mediates transcriptional responses in the nucleus, whereas a distinct non-transcriptional pathway involving the plasma membrane-associated co-receptors auxin binding protein 1 (ABP1)/ABP1-like protein 1 and 2 (ABL1/2) and transmembrane kinases (TMKs) mediates rapid cellular responses. Recent breakthroughs have resolved long-standing debates regarding the apoplastic auxin signaling, highlighting the TMK kinase family and its auxin-binding co-receptors ABP1/ABL1/2 as the core components of this rapid auxin signaling system. This review explores how this signaling complex has evolved across different plant species and how it enables the perception of extracellular auxin to trigger fast cellular responses, including global phosphorylation, apoplastic acidification, and cytoskeletal changes, within seconds. By examining these interactions and their evolutionary origins, we present a unified framework for understanding how the integration of intracellular and extracellular auxin signals drives the remarkable versatility of plant development.
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