Arabidopsis HOOKLESS1 acts as a histone acetyltransferase to promote cotyledon greening during seedling de-etiolation.

Abstract

Greening immediately after etiolated-seedling's emergence from the soil is critical for plants to initiate their autotrophic life cycle through photosynthesis. The greening process relies on a complex transcriptional network that fine-tunes the biosynthesis of chlorophyll and prevents premature development of chloroplasts. In this study, we identified the Arabidopsis HOOKLESS1 (HLS1) as a key regulator of light-induced cotyledon greening. Our results demonstrated that HLS1 is essential for the proper expression of greening-related genes controlling chlorophyll biosynthesis and chloroplast development. Loss of HLS1 severely disrupts the Pchlide-to-Chlide transition and impairs reactive oxygen species (ROS) scavenging in etiolated seedlings upon light exposure, leading to catastrophic ROS burst and even photobleaching. Biochemical assays revealed that HLS1 is a histone acetyltransferase mediating the deposition of H3K9ac and H3K27ac marks at multiple greening-related genes, thereby promoting their transcriptional activation. Genetic analysis further confirmed that HLS1's promotive effect on the greening process is fully dependent on its histone acetyltransferase activity. Moreover, the loss of HLS1 also interrupts the promotive effect of ethylene signaling on the greening process by reducing the binding of ETHYLENE-INSENSITIVE 3 to the promoter region of POR genes, thus inhibiting the activation effect of ethylene signaling on the expression of PORs. Collectively, our study reveals that HLS1 acetylates histones to activate greening-related genes, optimizing chlorophyll biosynthesis and chloroplast development during dark-to-light transition in seedlings.