Evolution of F-box genes in plants: Different modes of sequence divergence and their relationships with functional diversification

Abstract

F-box proteins are substrate-recognition components of the Skp1-Rbx1-Cul1-F-box protein (SCF) ubiquitin ligases. In plants, F-box genes form one of the largest multigene superfamilies and control many important biological functions. However, it is unclear how and why plants have acquired a large number of F-box genes. Here we identified 692, 337, and 779 F-box genes in Arabidopsis, poplar and rice, respectively, and studied their phylogenetic relationships and evolutionary patterns. We found that the plant F-box superfamily can be divided into 42 families, each of which has a distinct domain organization. We also estimated the number of ancestral genes for each family and identified highly conservative versus divergent families. In conservative families, there has been little or no change in the number of genes since the divergence between eudicots and monocots Ϸ145 million years ago. In divergent families, however, the numbers have increased dramatically during the same period. In two cases, the numbers of genes in extant species are >100 times greater than that in the most recent common ancestor (MRCA) of the three species. Proteins encoded by highly conservative genes always have the same domain organization, suggesting that they interact with the same or similar substrates. In contrast, proteins of rapidly duplicating genes sometimes have quite different domain structures, mainly caused by unusually frequent shifts of exon-intron boundaries and/or frameshift mutations. Our results indicate that different F-box families, or different clusters of the same family, have experienced dramatically different modes of sequence divergence, apparently having resulted in adaptive changes in function.birth-and-death evolution ͉ F-box protein ͉ multigene family ͉ plant evolution

Novel and Recently Evolved MicroRNA Clusters Regulate Expansive F-BOX Gene Networks through Phased Small Interfering RNAs in Wild Diploid Strawberry

“…Plant FBX genes constitute a large family of genes (approximately 800 in F. vesca and approximately 690 in Arabidopsis) and can be classified into several distinct subfamilies based on domain structures (Kuroda et al, 2002;Xu et al, 2009). To investigate which specific FBX gene subfamilies are regulated by the clustered miRFBXs and deduce their potential functions, we performed phylogenetic analysis using all the FBX genes from Arabidopsis (691 genes; Xu et al, 2009) and the set of 96 F. vesca FBX genes targeted by the clustered miFBXs (Supplemental Table S6).…”

“…8G). FBX genes encode the substrate-recognition subunits of the SCF (for S-phase kinase associated protein1-Cullin-F Box) ubiquitin ligases and constitute one of the largest gene families, with 820 members in F. vesca (Xu et al, 2009;Hollender et al, 2014). FBX proteins regulate diverse biological processes and were grouped into two general types based on whether they function in conserved processes, such as embryogenesis and circadian rhythms, or relatively specialized processes, such as pollen recognition and pathogen response (Xu et al, 2009).…”

“…FBX genes encode the substrate-recognition subunits of the SCF (for S-phase kinase associated protein1-Cullin-F Box) ubiquitin ligases and constitute one of the largest gene families, with 820 members in F. vesca (Xu et al, 2009;Hollender et al, 2014). FBX proteins regulate diverse biological processes and were grouped into two general types based on whether they function in conserved processes, such as embryogenesis and circadian rhythms, or relatively specialized processes, such as pollen recognition and pathogen response (Xu et al, 2009). Xu et al (2009) noted that those with functions in conserved processes experienced little expansion in gene numbers during the evolution from the common ancestor of eudicots and monocots, while those in specialized processes experienced frequent gene duplications, in particular tandem duplications that may be critical to the evolution of specialized functions.…”

“…To investigate which specific FBX gene subfamilies are regulated by the clustered miRFBXs and deduce their potential functions, we performed phylogenetic analysis using all the FBX genes from Arabidopsis (691 genes; Xu et al, 2009) and the set of 96 F. vesca FBX genes targeted by the clustered miFBXs (Supplemental Table S6). As shown in Figure 4A, the Arabidopsis FBX genes are grouped into several distinct subfamilies, including FBA1, FBA3, LRR-FBD, Kelch repeats, and Domain Unknown Function295.…”

Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by resequencing Landsberg erecta and all four products of a single meiosis

“…Furthermore, 186 genes with exons/UTRs affected by indels (Supplemental Table 9) could have changed/disrupted expression or functions. F-box genes encode subunits of E3 ubiquitin ligases that are involved in physiological and environmental responses and differ dramatically in gene number among A. thaliana, poplar, and rice (Xu et al 2009). We found that eight F-box genes are absent from Ler (Supplemental Table 8) and 16 other F-box genes are partially affected (Supplemental Table 9), suggesting that these rapidly evolving genes are highly unstable even within the Arabidopsis species.…”