Transcription Factor Families Have Much Higher Expansion Rates in Plants than in Animals

Abstract

(M.-C.S.) Transcription factors (TFs), which are central to the regulation of gene expression, are usually members of multigene families. In plants, they are involved in diverse processes such as developmental control and elicitation of defense and stress responses. To investigate if differences exist in the expansion patterns of TF gene families between plants and other eukaryotes, we first used Arabidopsis (Arabidopsis thaliana) TFs to identify TF DNA-binding domains. These DNA-binding domains were then used to identify related sequences in 25 other eukaryotic genomes. Interestingly, among 19 families that are shared between animals and plants, more than 14 are larger in plants than in animals. After examining the lineage-specific expansion of TF families in two plants, eight animals, and two fungi, we found that TF families shared among these organisms have undergone much more dramatic expansion in plants than in other eukaryotes. Moreover, this elevated expansion rate of plant TF is not simply due to higher duplication rates of plant genomes but also to a higher degree of expansion compared to other plant genes. Further, in many Arabidopsis-rice (Oryza sativa) TF orthologous groups, the degree of lineage-specific expansion in Arabidopsis is correlated with that in rice. This pattern of parallel expansion is much more pronounced than the wholegenome trend in rice and Arabidopsis. The high rate of expansion among plant TF genes and their propensity for parallel expansion suggest frequent adaptive responses to selection pressure common among higher plants.Regulation of gene expression is central to a myriad of biological processes at the molecular level and is to a significant extent controlled by transcription factors (TFs). Most TFs are modular proteins consisting of a DNA-binding domain that interacts with cis-regulatory elements of its target genes and a protein-protein interaction domain that facilitates oligomerization between TFs or other regulators (Wray et al., 2003). Sequence divergence in the DNA-binding domains of related TFs may lead to differences in affinities to a set of cis-regulatory elements. Together with the propensity for TFs to homodimerize and/or heterodimerize, the large TF repertoire in a eukaryote genome provides a wide range of combinatorial relationships for transcriptional regulation. TFs usually form gene families that vary considerably in size among organisms (Riechmann et al., 2000;Wray et al., 2003). The reasons behind such differences are not known, although it is suggested that organismal complexity correlates with an increase in the absolute number and the proportion of TFs in a proteome (Levine and Tjian, 2003).In Arabidopsis (Arabidopsis thaliana), at least 1,500 genes are TFs, and 45% of these TFs belong to families common to Caenorhabditis elegans, Drosophila melanogaster, and Saccharomyces cerevisiae (Riechmann et al., 2000). Some of these TF families are much larger in Arabidopsis, suggesting differential expansion. For example, the Myb family has 190 members in Ar...

Analyses of Expressed Sequence Tags from Apple

“…They estimate that these whole-genome duplication events are responsible for about 90% of the transcription factor in higher plants. Indeed, the rate of transcription factor evolution is thought to be higher in plants than in animals (Shiu et al, 2005). This contrasts with proteins involved in secondary metabolism or abiotic stress, where those derived by small segmental duplications tended to be retained, whereas those derived by whole-genome duplications were more rapidly lost (Maere et al, 2005).…”

Clustered Transcription Factor Genes Regulate Nicotine Biosynthesis in Tobacco

“…Most tandem arrays contain only two duplicated genes, and arrays with more than three members are rare (Rizzon et al, 2006). Although transcription factor families have much higher expansion rates in plants than in animals (Shiu et al, 2005), the Arabidopsis genome contains only one region with more than five duplicated transcription factor genes in tandem, whereas several such regions are present in soybean (Glycine max; Schmutz et al, 2010). Apparently, the clustering of more than seven duplicated transcription factor genes at the NIC2 locus is a rare event in the evolution of tobacco.…”

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

“…These studies have also shown that evolutionarily younger genes tend to be expressed at earlier and later stages of development, whereas the transcriptomes of the middle stages (the phylotypic stage) are dominated by ancient genes (10, 13). It remains to be investigated how the evolutionary age and the expression patterns of the different TFs shift throughout the ontogeny of these lineages and whether TF expression profiles correlate with the general transcriptome profiles.Previous studies have analyzed the evolutionary history and phylogenetic distribution of TFs in various branches of the tree of life (6,(15)(16)(17)(18)(19)(20)(21)(22). However, it is not yet clear whether the evolutionary scenarios previously proposed are robust to the incorporation of genome data from key phylogenetic taxa that were previously unavailable.…”