Abstract
Pseudogenes are significant components of eukaryotic genomes, and some have acquired novel regulatory roles. To date, no study has characterized rice pseudogenes systematically or addressed their impact on the structure and function of the rice genome. In this genome-wide study, we have identified 11,956 non-transposon-related rice pseudogenes, most of which are from gene duplications. About 12% of the rice protein-coding genes, half of which are in singleton families, have a pseudogene paralog. Interestingly, we found that 145 of these pseudogenes potentially gave rise to antisense small RNAs after examining ∼1.5 million small RNAs from developing rice grains. The majority (>50%) of these antisense RNAs are 24-nucleotides long, a feature often seen in plant repeat-associated small interfering RNAs (siRNAs) produced by RNA-dependent RNA polymerase (RDR2) and Dicer-like protein 3 (DCL3), suggesting that some pseudogene-derived siRNAs may be implicated in repressing pseudogene transcription (i.e., cis-acting). Multiple lines of evidence, however, indicate that small RNAs from rice pseudogenes might also function as natural antisense siRNAs either by interacting with the complementary sense RNAs from functional parental genes (38 cases) or by forming double-strand RNAs with transcripts of adjacent paralogous pseudogenes (2 cases) (i.e., trans-acting). Further examinations of five additional small RNA libraries revealed that pseudogene-derived antisense siRNAs could be produced in specific rice developmental stages or physiological growth conditions, suggesting their potentially important roles in normal rice development. In summary, our results show that pseudogenes derived from protein-coding genes are prevalent in the rice genome, and a subset of them are strong candidates for producing small RNAs with novel regulatory roles. Our findings suggest that pseudogenes of exapted functions may be a phenomenon ubiquitous in eukaryotic organisms.
Highlights
Pseudogenes are genomic sequences derived from functional genes, but are often considered non-functional due to the accumulation of various deleterious mutations over their evolutionary history [1,2,3,4,5,6]
Recent important studies have discovered that a subset of them have unforeseen roles as sources of non-coding RNA transcripts that can regulate the expression of functional coding genes. We have explored this perspective by studying to what extent rice pseudogenes can encode small RNAs, especially the antisense type
After crossexamining thousands of rice pseudogenes and several millions of small RNA sequences, we found that pseudogene-derived small RNAs are abundant in rice, and many of them may function as natural antisense RNAs by interacting complementarily with sense RNAs from either parental genes or other pseudogenes
Summary
Pseudogenes are genomic sequences derived from functional genes, but are often considered non-functional due to the accumulation of various deleterious mutations over their evolutionary history [1,2,3,4,5,6]. Compared with its parental gene (more precisely, the direct descendent of the ancestral gene that gave rise to the pseudogene), a pseudogene generally contains sequence features such as premature stop codon or frameshift mutations, due to relaxation of or entirely lack of functional constraints. Processed pseudogenes arose from retrotransposition events, i.e., the insertions of DNA materials into a genome via RNA intermediates. As a result, duplicated pseudogenes often retain the exon-intron structures of their parent genes, a characteristic absent in processed pseudogenes [1,2,4,6]
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