Evolution of the Class IV HD-Zip Gene Family in Streptophytes

Abstract

Class IV homeodomain leucine zipper (C4HDZ) genes are plant-specific transcription factors that, based on phenotypes in Arabidopsis thaliana, play an important role in epidermal development. In this study, we sampled all major extant lineages and their closest algal relatives for C4HDZ homologs and phylogenetic analyses result in a gene tree that mirrors land plant evolution with evidence for gene duplications in many lineages, but minimal evidence for gene losses. Our analysis suggests an ancestral C4HDZ gene originated in an algal ancestor of land plants and a single ancestral gene was present in the last common ancestor of land plants. Independent gene duplications are evident within several lineages including mosses, lycophytes, euphyllophytes, seed plants, and, most notably, angiosperms. In recently evolved angiosperm paralogs, we find evidence of pseudogenization via mutations in both coding and regulatory sequences. The increasing complexity of the C4HDZ gene family through the diversification of land plants correlates to increasing complexity in epidermal characters.

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

“…Yang et al (2011) proposed that promoter disablement may be a largely unrecognized first step in pseudogenization, and the consequent relaxation of selection may be followed by the disablement of coding regions. Consistent with this hypothesis, among class IV homeodomain-Zip TF duplicate genes derived from the a WGD, one duplicate often has a higher rate of evolution and a more limited expression pattern than its paralog, suggesting possible pseudogenization through the disablement of regulatory regions (Zalewski et al, 2013). AtDDF2 also shows evidence of promoter disablement, such as reduced expression, fewer predicted cis-elements compared with DDF1, and a methylated repetitive element found in close proximity to the TSS.…”

DEFECTIVE KERNEL 1 promotes and maintains plant epidermal differentiation

“…Here we show that defects in DEK1 perturb epidermal cell differentiation via a mechanism affecting the transcription of genes encoding HD-ZIP IV family TFs. The ancestral HD-ZIP IV protein, like DEK1, is thought to have arisen in the common algal ancestor of land plants, where it might have been crucial in the evolution of a specialised outer cell layer with the characteristics necessary for life on land, such as cuticle formation and stomatal development (Zalewski et al, 2013). Apoplastic signalling mediated by ACR4, like DEK1 function, is necessary for the maintenance of HD-ZIP IV gene expression (San-Bento et al, 2014).…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…The origin of two major groups of HD-ZIP proteins (class III and class IV) has been traced back to charophyte algae (Floyd et al 2006;Zalewski et al 2013). Although HD-ZIP proteins are also found in bryophytes, their function in lower plants is not well characterized (Sakakibara et al 2001;Prigge and Clark 2006).…”