The evolution of epitype

Abstract

The epitype of a single gene or entire genome is determined by cis-linked differences in chromatin structure. I explore the hypothesis that "epitype and associated phenotypes evolve by gene duplication, divergence, and subfunctionalization" parallel to models for the evolution of genotype. This hypothesis is dissected by considering the relationship between epigenetic control and phenotype, the phylogenetic evidence that epitype evolves from ancestral genes following gene duplication, and the possible evolutionary rates of change for different epitypes. Initial supporting arguments for this hypothesis are discussed based on conserved patterns of nucleosome phasing, DNA methylation, and histone variant H2AZ deposition that appear to contribute to the inheritance of epitype in plants and animals. However, patterns of histone modification in recent segmental chromosome duplications are not well conserved. A continued experimental examination of the link between gene phylogeny and epitype and the evolution of epigenetically determined phenotypes is needed to further explore this hypothesis.

Figure 1.

Nucleotide Sequence Composition Directs the Positioning of H2AZ-Enriched Nucleosomes in Saccharomyces. The frequency distribution of the combined number of AA, TT, AT, and TA dinucleotides (dashed line) or GG, CC, GC, and CG dinucleotides (solid line) at each base pair along the 147 bp of nucleosomal DNA. Repeats of G+C-rich dinucleotides are more commonly in the major groove (gray shaded areas) facing inward against the nucleosome. A+T-rich dinucleotides are generally in the major grooves facing outward from the nucleosome. The bottom axis shows the distance in base pairs from zero at the center of dyad symmetry. (Adapted by permission from Macmillan Publishers Limited: Nature, Albert et al. [2007], copyright 2007.)

Figure 2.

Cytosine Methylation Patterns Are Conserved among the Members of the Human Plasminogen Precursor Gene Family PGL, PGLA, and PGLB1/B2. In human liver, where all four genes are expressed, one of the two alleles for each gene are cytosine methylated ^5MeC (black stars) at nearly all seven CpG sites. The other allele remains unmethylated (white stars). In skeletal and heart muscle, where the genes are not expressed, both alleles for each gene are nearly all cytosine methylated at all seven sites. (Adapted from Cortese et al. [2008], with permission from Elsevier.)

Figure 3.

MADS Box Repressors of Flowering FLC, MAF4, and MAF5 Share an Uncommon Bimodal H2AZ Distribution Pattern in Arabidopsis. (A) and (C) All three MADS box transcription factor genes share in bimodal pattern of H2AZ deposition with peaks at their 5′ and 3′ ends in seedlings. (B) and (D) Maps of FLC, MAF4, and MAF5 genes and their exon structures (black boxes), and regions PCR amplified to quantify H2AZ-enriched sequences (1 to 10 for FLC and 1 to 11 for MAF4 and MAF5). (Redrawn from Deal et al. [2007].)