Integrated Regulation of Apical Hook Development by Transcriptional Coupling of EIN3/EIL1 and PIFs in Arabidopsis

Abstract

The apical hook protects the meristems of dicot seedlings as they protrude through the soil; multiple factors, including phytohormones and light, mediate apical hook development. HOOKLESS1 (HLS1) plays an indispensable role, as HLS1 mutations cause a hookless phenotype. The ETHYLENE INSENSITIVE3 (EIN3) and EIN3-LIKE1 (EIL1) transcription factors integrate multiple signals (ethylene, gibberellins, and jasmonate) and activate HLS1 expression to enhance hook development. Here, we found that Arabidopsis thaliana PHYTOCHROME INTERACTING FACTOR (PIF) transcription factors act in parallel with EIN3/EIL1 and promote hook curvature by activating HLS1 transcription at a distinct binding motif. EIN3/EIL1 and PIFs can promote hook formation in the absence of the other. Jasmonate represses PIF function to inhibit hook development. Like EIN3 and EIL1, MYC2 interacts with PIF4 and hampers its activity. Acting together, EIN3/EIL1 and PIFs alleviate the negative effects of jasmonate/light and facilitate the positive effects of ethylene/gibberellins. Mutating EIN3/EIL1 and PIFs causes a complete hookless phenotype, marginal HLS1 expression, and insensitivity to upstream signals. Transcriptome profiling revealed that EIN3/EIL1 and PIFs additively and distinctly regulate a wide array of processes, including apical hook development. Together, our findings identify an integrated framework underlying the regulation of apical hook development and show that EIN3/EIL1 and PIFs fine-tune adaptive growth in response to hormone and light signals.