A Promiscuous Intermediate Underlies the Evolution of LEAFY DNA Binding Specificity

Abstract

Transcription factors (TFs) are key players in evolution. Changes affecting their function can yield novel life forms but may also have deleterious effects. Consequently, gene duplication events that release one gene copy from selective pressure are thought to be the common mechanism by which TFs acquire new activities. Here, we show that LEAFY, a major regulator of flower development and cell division in land plants, underwent changes to its DNA binding specificity, even though plant genomes generally contain a single copy of the LEAFY gene. We examined how these changes occurred at the structural level and identify an intermediate LEAFY form in hornworts that appears to adopt all different specificities. This promiscuous intermediate could have smoothed the evolutionary transitions, thereby allowing LEAFY to evolve new binding specificities while remaining a single-copy gene.

A Recently Evolved Isoform of the Transcription Factor BES1 Promotes Brassinosteroid Signaling and Development in Arabidopsis thaliana

“…To avoid the deleterious effects of mutation, gene duplication events occur to allow one copy of a gene to maintain its function, while another copy may diverge to acquire new functions (Sayou et al, 2014). BES1 and BZR1 belong to a small gene family encoding plant-specific transcription factors, and they may have originated from a common ancestor and then diverged (Yin et al, 2005;Lachowiec et al, 2013).…”

Molecular Evidence for Functional Divergence and Decay of a Transcription Factor Derived from Whole-Genome Duplication in Arabidopsis thaliana

“…However, the assumption that orthologous TFs do not readily undergo changes in binding site preference has been challenged by recent findings. For example, orthologous Saccharomyces cerevisiae and Candida albicans mating-type a1 TFs have highly divergent recognition sequences (Baker et al, 2011), and in plants, the TF LEAFY may have undergone changes in DNA-binding specificity during land plant evolution without the aid of duplication (Sayou et al, 2014). Thus, studies of DNA-binding preference between both paralogous and orthologous TFs are necessary to determine the contribution of binding site divergence to functional divergence.…”

Comment on “A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity”

“…Sayou et al do offer a second model of LFY evolution in this context: The promiscuous form evolved before the divergence of liverworts and was then lost twice (in liverworts and again in mosses), remaining only in the hornworts, and then lost again in land plants [ Fig. 1A, a reproduction of figure S9 in (2)]. This second model (Fig.…”

“…Applying this predominant model, most research has focused on how multiple gene copies of TFs undergo selective sub/ neo/nonfunctionalization after a duplication event. Sayou et al used the plant-specific TF LEAFY (LFY) to propose a new model for the evolution of TF binding sites, not through gene duplication but instead through a "promiscuous," gain-of-function intermediate form (2). By reconciling the phylogeny of LFY orthologs with the prevailing and widely accepted history of plant evolution, however, we argue that the evolution of LFY through gene duplications and ensuing changes in function is more consonant with the findings of Sayou et al than their proposed "promiscuous" pathway.…”