Purifying selection and birth-and-death evolution in the ubiquitin gene family

Abstract

Ubiquitin is a highly conserved protein that is encoded by a multigene family. It is generally believed that this gene family is subject to concerted evolution, which homogenizes the member genes of the family. However, protein homogeneity can be attained also by strong purifying selection. We therefore studied the proportion (p(S)) of synonymous nucleotide differences between members of the ubiquitin gene family from 28 species of fungi, plants, and animals. The results have shown that p(S) is generally very high and is often close to the saturation level, although the protein sequence is virtually identical for all ubiquitins from fungi, plants, and animals. A small proportion of species showed a low level of p(S) values, but these values appeared to be caused by recent gene duplication. It was also found that the number of repeat copies of the gene family varies considerably with species, and some species harbor pseudogenes. These observations suggest that the members of this gene family evolve almost independently by silent nucleotide substitution and are subjected to birth-and-death evolution at the DNA level.

Figure 1

Ubiquitin polymeric (poly-u) loci in humans and C. elegans. A poly-u locus consists of a number of ubiquitin genes that are concatenated with no intervening sequences. A monomeric locus is composed of a ubiquitin gene and a ribosomal protein gene with either 52 or 80 codons. The proteins encoded by polymeric and monomeric genes are identical. Poly-u ψ is a pseudogene locus.

Figure 2

A scenario of the evolution history of poly-u loci A and B in sunflower. O represents the common ancestral poly-u locus of UbA and UbB, whereas A′, B′, etc., stand for more recent ancestors. a, b, c, etc., represent ancestral ubiquitin genes. The X mark indicates gene deletion. In the ancestral poly-u locus, B′, genes c and e are inverted. The present-day ubiquitin genes are indicated by numbers.

Figure 3

A scenario of the evolutionary history of poly-u loci A, B, C, D, and E in Arabidopsis. The notations O, A′, B′, etc., and a, b, c, etc., are the same as those in Fig. 2. The present-day ubiquitin genes are indicated by numbers. The p_S values for the five poly-u loci are presented in Table 8 (see supplementary material at www.pnas.org).

Figure 4

Poly-u pseudogenes from humans, Arabidopsis, and Chinese hamster.