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New Insights Into LEAFY Structure and Function

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New Insights Into LEAFY Structure and Function doi:10.1093/jxb/erx092 New insights into LEAFY structure and function Frank Wellmer Smurfit Institute of Genetics, Trinity College Dublin, Ireland [email protected] The plant-specific transcription factor LEAFY (LFY) is a master regulator of early flower development (Weigel et al., 1992). It orchestrates the onset of flowering and is involved in activating the expression of floral organ identity genes (Busch et al., 1999; Parcy et al., 1998), which specify the different types of floral organs. Because of LFY’s central role in reproductive development, its function and molecular evolution have been studied in detail over the past 25 years using a multitude of different experimental approaches. In fact, there are arguably few plant transcriptional regulators that have been studied as extensively as LFY. However, the protein structure of LFY remained unknown for many years, precluding detailed insights in the molecular mechanism underlying its activity. This knowledge gap was partially closed in 2008, when the structure of the highly conserved carboxy-terminal DNA binding domain was resolved through X-ray crystallography (Hamès et al., 2008). This work showed that the DNA binding domain is composed of a helix-turn-helix motif and binds DNA as a dimer (Fig. 1). In contrast, the function of the amino-terminal half of LFY, which Fig. 1. A LEAFY dimer bound contains another conserved domain, remained unknown. to DNA. The N-terminal SAM Using LFY from the gymnosperm Gingko biloba, Sayou et al. (2016) recently and C-terminal DNA binding succeeded in crystallizing the N-terminal domain and resolved its structure at domains are shown. (Image kindly provided by François 2.3 Å resolution. They found that the domain resembles a Sterile Alpha Motif Parcy). (SAM) and is composed of five α-helices that are connected by four loops. SAM domains are common structural motifs in eukaryotes mediating the interaction with nucleic acids, lipids and other proteins. Some SAM domains have also been shown to trigger protein oligomerization. The SAM domain in LFY appears to belong to this latter group as indicated by the formation of LFY-SAM domain polymer chains in a crystal, where monomers contact each other in a head-to-tail arrangement. What is the functional relevance of this oligomerization event and is it required for LFY activity? To investigate this, Sayou and colleagues first identified the amino acid residues that are essential for oligomerization. To this end, they used the structural information they had obtained as well as data from the analysis of other SAM domain-containing proteins. They then carried out a series of experiments with modified LFY proteins in which these essential amino acid residues had been substituted, leading to the suppression of oligomerization. They found that the expression of the mutated form of LFY in plants resulted in a much reduced activity when compared to wild-type LFY protein, thus implying that oligomerization is required for proper LFY function. Additional tests showed that the SAM domain prevents LFY from binding to DNA as a monomer and hence promotes dimer formation. Furthermore, the results of genome-wide localization studies showed that the mutated form of LFY exhibited a substantial decrease in its overall ability to bind to DNA. In addition to regulating the binding properties of LFY, the SAM domain also appears to be involved in binding site selection. Specifically, Sayouet al . showed that the SAM domain mediates cooperative binding of LFY protein oligomers to multiple binding sites and facilitates binding to sites with low affinity for LFY. Thus, the SAM domain plays a central role in regulating the DNA binding activity of the LFY transcription factor. Another interesting observation reported by Sayou et al. is that the SAM domain appears to promote binding of LFY to regions of chromatin with low accessibility. Since it has been shown previously that LFY can interact with chromatin remodeling factors, it is possible that LFY acts as a ‘pioneer transcription factor’, and recruits these proteins to regions of closed chromatin to bring about changes in chromatin conformation and gene expression. Notably, it has been suggested that some of the floral organ identity factors, which mediate floral organ specification, also function as pioneer factors (Pajoro et al., 2014). These include the MADS-domain protein APETELA1, which controls early flower development together with LFY. Thus, pioneer factor activity may be at the core of the mechanism that regulates the onset of flower formation, possibly explaining the massive changes in gene expression observed during this developmental stage. In summary, the detailed insights into LFY structure and function obtained by Sayou et al. represent a major breakthrough in the analysis of this master regulator of flower development. They will undoubtedly open up new avenues for experimentation that will lead to an even deeper mechanistic understanding of the activities of LFY during plant reproduction. References Busch MA, Bomblies K, Weigel D. 1999. Activation of a floral homeotic gene in Arabidopsis. Science 285, 585–587. Hamès C, Ptchelkine D, Grimm C, et al. 2008. Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. The EMBO Journal 27, 2628–2637. Pajoro A, Madrigal P, Muiño JM, et al. 2014. Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biology 15, R41. Parcy F, Nilsson O, Busch MA, Lee I, Weigel D. 1998. A genetic framework for floral patterning. Nature 395, 561–566. Sayou C, Nanao MH, Jamin M, et al. 2016. A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor. Nature Communications 7, 11222. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM. 1992. LEAFY controls floral meristem identity in Arabidopsis. Cell69, 843–859..
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