Evolutionary Analysis of the MIXTA Gene Family Highlights Potential Targets for the Study of Cellular Differentiation

Abstract

Differentiated epidermal cells such as trichomes and conical cells perform numerous essential functions in plant biology and are important for our understanding of developmental patterning and cell shape regulation. Many are also commercially significant, such as cotton fibers and trichomes that secrete pharmaceutically useful or herbivore-deterring compounds. Here, we focus on the phylogeny and evolution of the subgroup 9 R2R3 MYB gene transcription factors, which include the MIXTA gene, and that are important for the specification and regulation of plant cellular differentiation. We have sequenced 49 subgroup 9 R2R3 MYB genes from key experimental taxa and combined these sequences with those identified by an exhaustive bioinformatic search, to compile a data set of 223 subgroup 9 R2R3 MYB genes. Our phylogenetic analyses demonstrate, for the first time, the complex evolutionary history of the subgroup 9 R2R3 MYB genes. A duplication event is inferred before the origin of seed plants giving rise to two major gene lineages, here termed SBG9-A and SBG9-B. The evolutionary conservation of the SBG9-B gene lineage has not been previously recognized and its role in cellular differentiation is unknown, thus an entire clade of potential candidate genes for epidermal cell regulation remains to be explored. Using a heterologous transformation bioassay, we provide functional data that implicate members of the SBG9-B lineage in the specification of epidermal projections. Furthermore, we reveal numerous putative duplication events in both SBG9-A and SBG9-B lineages, resolving uncertainty about orthology and paralogy among the subgroup 9 R2R3 MYB genes. Finally, we provide a robust framework over which to interpret existing functional data and to direct ongoing comparative genetic research into the evolution of plant cellular diversity.

A Conserved Network of Transcriptional Activators and Repressors Regulates Anthocyanin Pigmentation in Eudicots

“…Petunia and Arabidopsis represent model species from the two major groupings of dicotyledonous plants, the Asterids and Rosids, respectively. Studies of the role of the MBW complex in controlling trichome production suggest that the MYB/bHLH regulatory systems may have diverged since the evolutionary separation of these major plant groups, although the details of this are still not clear (Martin and Glover, 2007;Brockington et al, 2013).…”

The Tomato MIXTA-like Transcription Factor Coordinates Fruit Epidermis Conical Cell Development and Cuticular Lipid Biosynthesis and Assembly

“…Molecular phylogenetic analysis of the best hits revealed that the tomato genome retains seven potential orthologs to the clade containing MIXTA and MIXTA-like proteins (R2R3-MYB group 9; Supplemental Fig. S1; Stracke et al, 2001;Brockington et al, 2013). This group of MYB factors also includes MYB17 proteins, with which two of the tomato candidates (Solyc01g094360 and Solyc05g048830) group.…”

“…8B). To date, MIXTA orthologs across a variety of plant species have been reported to be involved in the regulation of epidermal cell differentiation (Brockington et al, 2013). The earliest characterized MIXTA ortholog (AmMIXTA) was shown to promote conical epidermal cell development in the petals of snapdragon (Noda et al, 1994;Brockington et al, 2013).…”

“…To date, MIXTA orthologs across a variety of plant species have been reported to be involved in the regulation of epidermal cell differentiation (Brockington et al, 2013). The earliest characterized MIXTA ortholog (AmMIXTA) was shown to promote conical epidermal cell development in the petals of snapdragon (Noda et al, 1994;Brockington et al, 2013). Subsequently, members of the MIXTA transcription factor clade from Arabidopsis, Thalictrum thalictroides, and P. hybrida were also reported to regulate conical epidermal cell development (Baumann et al, 2007;Di Stilio et al, 2009), whereas orthologs from Arabidopsis, Populus trichopoda, Mimulus guttatus, snapdragon, Medicago trunculata, and Dendrobium crumenatum have been shown to be positive regulators of trichome development (Perez-Rodriguez et al, 2005;Gilding and Marks, 2010;Plett et al, 2010;Scoville et al, 2011).…”

“…Members of the MYB protein family termed MIXTA or MIXTA-like were shown to be key regulators of epidermal cell differentiation across multiple plants species (Martin and Glover, 2007;Brockington et al, 2013). Orthologs of the MIXTA/MIXTA-like clade have been reported specifically to act as positive regulators of conical epidermal cell formation (Noda et al, 1994;Baumann et al, 2007;Di Stilio et al, 2009), trichome development (Perez-Rodriguez et al, 2005;Gilding and Marks, 2010;Plett et al, 2010), and cotton fiber development (Machado et al, 2009;Walford et al, 2011).…”