The karrikin signaling regulator SMAX1 controls <i>Lotus japonicus</i> root and root hair development by suppressing ethylene biosynthesis.

Abstract

An evolutionarily ancient plant hormone receptor complex comprising the α/β-fold hydrolase receptor KARRIKIN INSENSITIVE 2 (KAI2) and the F-box protein MORE AXILLARY GROWTH 2 (MAX2) mediates a range of developmental responses to smoke-derived butenolides called karrikins (KARs) and to yet elusive endogenous KAI2 ligands (KLs). Degradation of SUPPRESSOR OF MAX2 1 (SMAX1) after ligand perception is considered to be a key step in KAR/KL signaling. However, molecular events which regulate plant development downstream of SMAX1 removal have not been identified. Here we show that <i>Lotus japonicus</i> SMAX1 is specifically degraded in the presence of KAI2 and MAX2 and plays an important role in regulating root and root hair development. <i>smax1</i> mutants display very short primary roots and elongated root hairs. Their root transcriptome reveals elevated ethylene responses and expression of <i>ACC Synthase 7</i> (<i>ACS7</i>), which encodes a rate-limiting enzyme in ethylene biosynthesis. <i>smax1</i> mutants release increased amounts of ethylene and their root phenotype is rescued by treatment with ethylene biosynthesis and signaling inhibitors. KAR treatment induces <i>ACS7</i> expression in a KAI2-dependent manner and root developmental responses to KAR treatment depend on ethylene signaling. Furthermore, in <i>Arabidopsis</i>, KAR-induced root hair elongation depends on <i>ACS7</i> Thus, we reveal a connection between KAR/KL and ethylene signaling in which the KAR/KL signaling module (KAI2-MAX2-SMAX1) regulates the biosynthesis of ethylene to fine-tune root and root hair development, which are important for seedling establishment at the beginning of the plant life cycle.