Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis

Abstract

BackgroundThe Wuschel related homeobox (WOX) family proteins are key regulators implicated in the determination of cell fate in plants by preventing cell differentiation. A recent WOX phylogeny, based on WOX homeodomains, showed that all of the Physcomitrella patens and Selaginella moellendorffii WOX proteins clustered into a single orthologous group. We hypothesized that members of this group might preferentially share a significant part of their function in phylogenetically distant organisms. Hence, we first validated the limits of the WOX13 orthologous group (WOX13 OG) using the occurrence of other clade specific signatures and conserved intron insertion sites. Secondly, a functional analysis using expression data and mutants was undertaken.ResultsThe WOX13 OG contained the most conserved plant WOX proteins including the only WOX detected in the highly proliferating basal unicellular and photosynthetic organism Ostreococcus tauri. A large expansion of the WOX family was observed after the separation of mosses from other land plants and before monocots and dicots have arisen. In Arabidopsis thaliana, AtWOX13 was dynamically expressed during primary and lateral root initiation and development, in gynoecium and during embryo development. AtWOX13 appeared to affect the floral transition. An intriguing clade, represented by the functional AtWOX14 gene inside the WOX13 OG, was only found in the Brassicaceae. Compared to AtWOX13, the gene expression profile of AtWOX14 was restricted to the early stages of lateral root formation and specific to developing anthers. A mutational insertion upstream of the AtWOX14 homeodomain sequence led to abnormal root development, a delay in the floral transition and premature anther differentiation.ConclusionOur data provide evidence in favor of the WOX13 OG as the clade containing the most conserved WOX genes and established a functional link to organ initiation and development in Arabidopsis, most likely by preventing premature differentiation. The future use of Ostreococcus tauri and Physcomitrella patens as biological models should allow us to obtain a better insight into the functional importance of WOX13 OG genes.

WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens

“…Concordantly, all WOX genes found in the Physcomitrella genome group into the WOX13 clade (Deveaux et al, 2008;van der Graaff et al, 2009;Nardmann et al, 2009). The absence of WUS-clade WOX genes in mosses raises the question of how stem cells are regulated.…”

“…Three loci containing WOX-related sequences in the Physcomitrella genome (Nardmann and Werr, 2007;Richardt et al, 2007) cluster with the Arabidopsis WOX13 clade (Deveaux et al, 2008;van der Graaff et al, 2009). Given that Arabidopsis WOX10 and WOX14 in this clade represent Brassicaceae-specific duplications of an ancestral WOX13-like gene (Deveaux et al, 2008), we named the moss homologs PpWOX13-like (PpWOX13L) genes (Fig.…”

“…Second, two members of the WOX9 clade, WOX8 and WOX9, redundantly regulate zygote development and embryo axis formation (Breuninger et al, 2008;Ueda et al, 2011) and WOX9 has an additional role in shoot meristem regulation (Wu et al, 2005). Finally, recent reports show that members of the WOX13 clade affect replum development, and dehiscence, flowering time, lateral root formation, and fertility (Deveaux et al, 2008;Romera-Branchat et al, 2012).…”

TheArabidopsisStem Cell Factor POLTERGEIST Is Membrane Localized and Phospholipid Stimulated

“…These defects result in a failure to specify the central vasculature. Interestingly, another CLE protein, CLE41, and other WOX genes have been shown to function in or are expressed in the vasculature, suggesting that other POL/PLL1-dependent CLE/WOX pathways may also exist (Haecker et al, 2004;Deveaux et al, 2008;Whitford et al, 2008). In summary, POL and PLL1 are required for at least two CLE/WOX signaling pathways that specify asymmetric cell divisions during development, including those that give rise to and maintain the shoot and root stem cell niches.…”

Gene and Protein Expression Profiles in Rice Gametes and Zygotes: A Cue for Understanding the Mechanisms of Gametic and Early Zygotic Development in Angiosperms

“…Os01g0840300 encodes a Wuschel-related homeobox (WOX) protein, the key regulator in determining cell fate in plants (Mayer et al 1998 ;Haecker et al 2004 ;Zhao et al 2009 ), and 15 WOX genes, including WUSCHEL , have been identifi ed in Arabidopsis . Interestingly, Os01g0840300 has been reported as the rice orthologue of Arabidopsis WOX2 (Deveaux et al 2008 ), whose transcripts accumulate in Arabidopsis zygotes and are restricted to the apical cell of two-celled proembryos (Haecker et al 2004 ). In addition, WOX2 has been proposed to be the predominant regulator of apical patterning (Jeong et al 2011 ), suggesting WOX proteins encoded by Os01g0840300 may have a role in determining cell fate during early embryogenesis in rice.…”