IAA3-mediated repression of PIF proteins coordinates light and auxin signaling in Arabidopsis

The exogenous light signal and endogenous auxin are two critical factors that antagonistically regulate hypocotyl growth. However, the regulatory mechanisms integrating light and auxin signaling pathways need further investigation. In this study, we identified a direct link between the light and auxin signaling pathways mediated by the auxin transcriptional repressor IAA3 and light-controlled PIF transcription factors in Arabidopsis. The gain-of-function mutation in IAA3 caused hyposensitivity to light, whereas disruption of IAA3 led to an elongated hypocotyl under different light intensity conditions, indicating that IAA3 is required in light regulated hypocotyl growth. Genetic studies showed that the function of IAA3 in hypocotyl elongation is dependent on PIFs. Our data further demonstrated that IAA3 interacts with PIFs in vitro and in vivo, and it attenuates the DNA binding activities of PIFs to the target genes. Moreover, IAA3 negatively regulates the expression of PIFs-dependent genes. Collectively, our study reveals an interplay mechanism of light and auxin on the regulation of hypocotyl growth, coordinated by the IAA3 and PIFs transcriptional regulatory module.
Author summary Sessile plants integrate environmental and endogenous signals to optimize their growth and development. Hypocotyl growth is a crucial developmental process tightly affected by light and auxin, but the underlying mechanism is still not well understood. Here, we demonstrate that the IAA3, a suppressor in auxin signaling, negatively regulates the light signaling regulator PIF protein activities. The IAA3 gain-of-function mutant displays reduced responses to light, while disruption of IAA3 results in elongated hypocotyl under various light intensity conditions. Genetic studies showed that IAA3 functions through PIFs to regulate hypocotyl growth. IAA3 physically interacts with PIFs through its C-terminal region and inhibits PIFs binding to target genes. Furthermore, IAA3 and PIFs coregulated a subset of downstream genes. The IAA3-PIFs interaction represents a novel layer of the regulatory mechanism by which light and auxin signals are integrated to affect hypocotyl growth.