Plant F-Box Protein Evolution Is Determined by Lineage-Specific Timing of Major Gene Family Expansion Waves

Abstract

F-box proteins (FBPs) represent one of the largest and fastest evolving gene/protein families in the plant kingdom. The FBP superfamily can be divided in several subfamilies characterized by different C-terminal protein-protein interaction domains that recruit targets for proteasomal degradation. Hence, a clear picture of their phylogeny and molecular evolution is of special interest for the general understanding of evolutionary histories of multi-domain and/or large protein families in plants. In an effort to further understand the molecular evolution of F-box family proteins, we asked whether the largest subfamily in Arabidopsis thaliana, which carries a C-terminal F-box associated domain (FBA proteins) shares evolutionary patterns and signatures of selection with other FBPs. To address this question, we applied phylogenetic and molecular evolution analyses in combination with the evaluation of transcriptional profiles. Based on the 2219 FBA proteins we de novo identified in 34 completely sequenced plant genomes, we compared their evolutionary patterns to a previously analyzed large subfamily carrying C-terminal kelch repeats. We found that these two large FBP subfamilies generally tend to evolve by massive waves of duplication, followed by sequence conservation of the F-box domain and sequence diversification of the target recruiting domain. We conclude that the earlier in evolutionary time a major wave of expansion occurred, the more pronounced these selection signatures are. As a consequence, when performing cross species comparisons among FBP subfamilies, significant differences will be observed in the selective signatures of protein-protein interaction domains. Depending on the species, the investigated subfamilies comprise up to 45% of the complete superfamily, indicating that other subfamilies possibly follow similar modes of evolution.

Phylogenetic analysis of the expansion of theMATH-BTBgene family in the grasses

“…Our results thus corroborate the previous finding that the core group genes show highest degree of evolutionary conservation 5 . It was also hypothesized that conserved clades containing genes from several species display significant functional conservation and possibly regulate ancient pathways in plant development or physiology 15 , 16 . So far, the only core genes functionally analyzed are from Arabidopsis with a role in the transcriptional regulation of abscisic acid signaling and fatty acid metabolism 7 , 8 .…”

Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

“…The Poaceae age group, comprising a further 13% of genes and 9% of families, was enriched in defense response (GO:0006952) and wound response (GO:0009611) genes, including those encoding disease resistance receptors (see below) and enzyme inhibitors (Supplementary Table 36 and Supplementary Data 4). In addition, these families were enriched in genes encoding components of the ubiquitin-proteasome pathway 51 , including SKP1/BTB/ POZ and F-box proteins, the latter of which are known to undergo lineage-specific expansions and rapid evolution in plants 52 . Also enriched in Poaceae were genes encoding two classes of proteins abundant in late embryogenesis, which function in dehydration and other stress tolerance 53 .…”

Genome-wide survey and expression analysis of F-box genes in chickpea

“…This could have resulted due to an increased rate of duplication events within these subfamilies in chickpea. According to a recent study by Navarro-Quezada et al [ 58 ], the F-box subfamilies expand in waves depending on the mode as well as the timing of duplication events. It was also suggested that the F-box protein subfamilies possibly share a common evolutionary pattern which generally involves massive duplication and rapid gene birth/death during the course of evolution.…”