The ALOG domain defines a new family of plant-specific transcription factors acting during Arabidopsis flower development

Abstract

The ALOGs (Arabidopsis LIGHT-DEPENDENT SHORT HYPOCOTYLS 1 and Oryza G1) are Transcription Factors (TFs) from an evolutionarily conserved plant-specific family shown to play critical roles in meristem identity, inflorescence architecture and organ boundaries in diverse species from mosses to higher flowering plants. However, the DNA binding-specificity and molecular determinants of protein-DNA interactions of this family were uncharacterized. Using in vitro genome-wide studies, we identified the conserved DNA motif bound by ALOG proteins from the liverwort Marchantia polymorpha and the flowering plants Arabidopsis, tomato and rice. In order to determine the amino acids responsible for DNA-binding specificity, we solved the 2.1[A] structure of the ALOG DNA binding domain in complex with its cognate DNA. The ALOG DBD is an all-alpha helical domain with a structural zinc ribbon insertion and an N-terminal disordered NLS. The NLS sequence forms an integral part of the DNA binding domain and contributes to direct base read-out. To define the function of a group of redundant ALOG proteins in the model plant Arabidopsis thaliana, we generated a series of alog mutants and uncovered their participation in a gene regulatory network involving the other floral regulators LEAFY, BLADE-ON-PETIOLE and PUCHI, all active in defining boundary regions between reproductive meristems and repressing bracts development. Taken together, this work provides the biochemical and structural basis for DNA-binding specificity of an evolutionarily conserved TF family and reveals its role as a key player in defining organ boundaries in Arabidopsis. Significance StatementTranscription Factors (TFs) are key proteins that bind specific regions in the genome and regulate the expression of associated genes. Not all organisms possess the same set of TFs and some, like the ALOGs, are specific to the plant kingdom. These TFs have been shown to play important roles from mosses to flowering plants. However, it was not known what DNA motif they recognize and how they bind DNA. Here we identify this motif, we show it is widely conserved in evolution and we understand how this new type of DNA binding domain works at the structural level. In addition, we also show that several ALOG genes from Arabidopsis share a redundant function within the genetic network underlying correct floral meristem development.