Evolutionary Origins of Pseudogenes and Their Association with Regulatory Sequences in Plants

Pseudogenes (Psi s), nonfunctional relatives of functional genes, form by duplication or retrotransposition, and loss of gene function by disabling mutations. Evolutionary analysis provides clues to Psi origins and effects on gene regulation. However, few systematic studies of plant Psi s have been conducted, hampering comparative analyses. Here, we examined the origin, evolution, and expression patterns of Psi s and their relationships with noncoding sequences in seven angiosperm plants. We identified similar to 250,000 Psi s, most of which are more lineage specific than protein-coding genes. The distribution of Psi s on the chromosome indicates that genome recombination may contribute to Psi elimination. Most Psi s evolve rapidly in terms of sequence and expression levels, showing tissue- or stage-specific expression patterns. We found that a surprisingly large fraction of nontransposable element regulatory noncoding RNAs (microRNAs and long noncoding RNAs) originate from transcription of Psi proximal upstream regions. We also found that transcription factor binding sites preferentially occur in putative Psi proximal upstream regions compared with random intergenic regions, suggesting that Psi s have conditioned genome evolution by providing transcription factor binding sites that serve as promoters and enhancers. We therefore propose that rapid rewiring of Psi transcriptional regulatory regions is a major mechanism driving the origin of novel regulatory modules.