Conserved Gene Expression Programs in Developing Roots from Diverse Plants

Abstract

The molecular basis for the origin and diversification of morphological adaptations is a central issue in evolutionary developmental biology. Here, we defined temporal transcript accumulation in developing roots from seven vascular plants, permitting a genome-wide comparative analysis of the molecular programs used by a single organ across diverse species. The resulting gene expression maps uncover significant similarity in the genes employed in roots and their developmental expression profiles. The detailed analysis of a subset of 133 genes known to be associated with root development in Arabidopsis thaliana indicates that most of these are used in all plant species. Strikingly, this was also true for root development in a lycophyte (Selaginella moellendorffii), which forms morphologically different roots and is thought to have evolved roots independently. Thus, despite vast differences in size and anatomy of roots from diverse plants, the basic molecular mechanisms employed during root formation appear to be conserved. This suggests that roots evolved in the two major vascular plant lineages either by parallel recruitment of largely the same developmental program or by elaboration of an existing root program in the common ancestor of vascular plants.

Tracheophytes Contain Conserved Orthologs of a Basic Helix-Loop-Helix Transcription Factor That Modulate ROOT HAIR SPECIFIC Genes

“…Our results demonstrate that the RSL4-RHE regulatory module is also conserved between a lycophyte (S. moellendorffii) and angiosperms. Thus, our study is consistent with a recent report demonstrating the similarity in overall root developmental programs between these two vascular plant groups (Huang and Schiefelbein, 2015).…”

Diversification of Root Hair Development Genes in Vascular Plants

“…Notably, the overall proportions of these nonconserved HAIR gene families is much greater than the equivalent nonconserved root-expressed gene families identified previously from these same species (controlling for family size; Fig. 7C; Huang and Schiefelbein, 2015). Thus, like the preferential divergence of AtRHMrelated genes (described above), these results suggest a relatively greater degree of diversification of HAIR genes during the evolution of these species.…”

“…To test this, we calculated the ratio of transcript accumulation in root hair cells (FPKM from COBL9::GFP) to transcript accumulation in the entire root elongation zone and differentiation zone (FPKM from published root segment RNA-seq data; Huang and Schiefelbein, 2015) for each of these genes (Supplemental Data Set S1). The distribution of these values differs significantly between the AtRHM and AtRH(-RHM) gene groups (P , 10…”

“…expression profiles). The nine expression profile types (defined by Huang and Schiefelbein [2015]) are indicated in the graphs at bottom (from left to right: meristematic, elongation, and differentiation zones). NE, No expression detected.…”

“…Because they are associated with root hair formation, AtRHM genes might be expected to exhibit relatively high transcription in the differentiation zone of the root, where root hairs emerge and grow (Grierson et al, 2014). To examine this, we compared each gene's transcript accumulation in the three major longitudinal root zones (meristematic zone, elongation zone, and differentiation zone) using transcriptome data reported previously from these Arabidopsis root segments (Huang and Schiefelbein, 2015). We found that a majority of the AtRHM genes (79%), but not the AtRH(-RHM) genes (30%), exhibit temporal expression profiles associated with relatively high transcript accumulation in the differentiation zone (expression profile types 6-9; Supplemental Data Set S1), a statistically significant enrichment (P , 0.01 for each of these four profile types, x 2 test; Fig.…”