Karrikin signaling regulates hypocotyl shade avoidance response by modulating auxin homeostasis in Arabidopsis

Shade affects all aspects of plant growth and development, including seed germination, hypocotyl elongation, petiole growth, leaf hyponasty, and flowering time. Here, we found that mutations in the key Arabidopsis karrikins signal perception-associated KARRIKIN INSENSITIVE 2 (KAI2) gene, encoding an alpha/beta-fold hydrolase, and the MORE AXILLARY GROWTH 2 (MAX2) gene, encoding an F-box protein, led to greater hypocotyl elongation under shade avoidance conditions. We further verified that these phenotypes were caused by perception of the endogenous KAI2-ligands (KLs), and that this phenotype is independent of strigolactone biosynthetic or signaling pathways. Upon perception of a KL, it is probable that the target protein forms a complex with the KAI2/MAX2 proteins, which are degraded through the action of the 26S proteasome. We demonstrated that SUPPRESSOR OF MAX2-1 (SMAX1) is the degradation target for the KAI2/MAX2 complex in the context of shade avoidance. KAI2 and MAX2 require SMAX1 to limit the hypocotyl growth associated with shade avoidance. Treatment with l-kynurenine, an inhibitor of auxin accumulation, partially restored elongation of kai2 mutant hypocotyls under simulated shade. Furthermore, KAI2 is involved in regulating auxin accumulation and polar auxin transport, which may contribute to the hypocotyl shade response. In addition, SMAX1 gene overexpression promoted the hypocotyl shade response. RNA-sequencing analysis revealed that SMAX1-overexpression affected the expression of many auxin homeostasis genes, especially under simulated shade. Altogether, our data support the conclusion that KL signaling regulates shade avoidance by modulating auxin homeostasis in the hypocotyl.

Automated summary

Shade has a significant impact on various aspects of plant growth and development, such as hypocotyl elongation. This study found that mutations in the KAI2 and MAX2 genes in Arabidopsis led to greater hypocotyl elongation under shade avoidance conditions. This phenotype was caused by the perception of endogenous KAI2-ligands (KLs) and independent of strigolactone biosynthetic or signaling pathways. The study also revealed the involvement of SMAX1 in limiting hypocotyl growth associated with shade avoidance. Overall, the data suggest that KL signaling regulates shade avoidance by modulating auxin homeostasis in the hypocotyl.