The Arabidopsis genome contains 10 genes belonging to the HD-Zip II family including ATHB2 and HAT2. Previous work has shown that ATHB2 is rapidly and strongly induced by light quality changes that provoke the shade avoidance response whereas HAT2 expression responds to auxin. Here, we present a genome-wide analysis of the HD-Zip II family. Phylogeny reconstruction revealed that almost all of the HD-Zip II genes can be subdivided into 4 clades (alpha-delta), each clade comprising 2-3 paralogs. Gene expression studies demonstrated that all the gamma and delta genes are regulated by light quality changes. Kinetics of induction, low R/FR/high R/FR reversibility and auxin response analyses strongly suggested that HAT1, HAT3 and ATHB4, as ATHB2, are under the control of the phytochrome system whereas HAT2 is up-regulated by low R/FR as a consequence of the induction of the auxin signaling pathway provoked by FR-rich light. Root and shoot digital in situ revealed that gamma and delta genes are also tightly regulated during plant development with both distinct and overlapping patterns. Phenotypes of gain of function and dominant negative lines demonstrated that one or more of the HD-Zip II gamma genes negatively regulate cell proliferation during leaf development in a high R/FR light environment. Finally, target gene analysis using a chimeric transcription factor (HD-Zip2-V-G), known to activate ATHB2 target genes in a glucocorticoid-dependent manner, revealed that all the 10 HD-Zip II genes can be recognized by the HD-Zip 2 domain in vivo, implying an intricate negative feedback network.

ORCID IDs: 0000-0002-8994-4838 (G.M.); 0000-0002-4974-5818 (I.R.).Shade-intolerant plants perceive the reduction in the ratio of red light (R) to far-red light (FR) as a warning of competition with neighboring vegetation and display a suite of developmental responses known as shade avoidance. In recent years, major progress has been made in understanding the molecular mechanisms underlying shade avoidance. Despite this, little is known about the dynamics of this response and the cascade of molecular events leading to plant adaptation to a low-R/FR environment. By combining genome-wide expression profiling and computational analyses, we show highly significant overlap between shade avoidance and deetiolation transcript profiles in Arabidopsis (Arabidopsis thaliana). The direction of the response was dissimilar at the early stages of shade avoidance and congruent at the late ones. This latter regulation requires LONG HYPOCOTYL IN FAR RED1/SLENDER IN CANOPY SHADE1 and phytochrome A, which function largely independently to negatively control shade avoidance. Gene network analysis highlights a subnetwork containing ELONGATED HYPOCOTYL5 (HY5), a master regulator of deetiolation, in the wild type and not in phytochrome A mutant upon prolonged low R/FR. Network analysis also highlights a direct connection between HY5 and HY5 HOMOLOG (HYH), a gene functionally implicated in the inhibition of hypocotyl elongation and known to be a direct target of the HY5 transcription factor. Kinetics analysis show that the HYH gene is indeed late induced by low R/FR and that its up-regulation depends on the action of HY5, since it does not occur in hy5 mutant. Therefore, we propose that one way plants adapt to a low-R/FR environment is by enhancing HY5 function.