Retrogenes in Rice (Oryza sativa L. ssp. japonica) Exhibit Correlated Expression with Their Source Genes

Abstract

Gene duplication occurs by either DNA- or RNA-based processes; the latter duplicates single genes via retroposition of messenger RNA. The expression of a retroposed gene copy (retrocopy) is expected to be uncorrelated with its source gene because upstream promoter regions are usually not part of the retroposition process. In contrast, DNA-based duplication often encompasses both the coding and the intergenic (promoter) regions; hence, expression is often correlated, at least initially, between DNA-based duplicates. In this study, we identified 150 retrocopies in rice (Oryza sativa L. ssp japonica), most of which represent ancient retroposition events. We measured their expression from high-throughput RNA sequencing (RNAseq) data generated from seven tissues. At least 66% of the retrocopies were expressed but at lower levels than their source genes. However, the tissue specificity of retrogenes was similar to their source genes, and expression between retrocopies and source genes was correlated across tissues. The level of correlation was similar between RNA- and DNA-based duplicates, and they decreased over time at statistically indistinguishable rates. We extended these observations to previously identified retrocopies in Arabidopsis thaliana, suggesting they may be general features of the process of retention of plant retrogenes.

Pollen-Specific Activation of Arabidopsis Retrogenes Is Associated with Global Transcriptional Reprogramming

“…A recent study in rice suggested frequent cotranscription between retrogenes and parents in plants (Sakai et al, 2011). Our retrogene identification criteria and the nature of the Arabidopsis retrogenes (e.g., an absence of retrogenes residing in the introns of other genes) allowed testing three possible mechanisms of retrogene cis-regulatory element origin: (1) carryover of parental promoters, (2) the use of bidirectional promoters, and (3) an acquisition of novel cis-regulatory elements.…”

“…Duplicated genes are generated by several DNA-and RNA-based mechanisms (Innan and Kondrashov, 2010;Sakai et al, 2011). Whole-genome DNA-based duplication (WGD) by polyploidization has occurred in the evolutionary history of all land plants and many animals (Dehal and Boore, 2005;De Smet et al, 2013).…”

“…In RNA-based duplication (retroposition), the mature mRNA of a protein-coding gene is reverse transcribed and integrated at an ectopic position in the genome using retroviral or retrotransposon machinery (Kaessmann et al, 2009). Therefore, retroposition has a high potential to generate evolutionary innovations (e.g., by expressing genes in a new developmental context, generating chimeric genes with new functional domain combinations, or interspecific horizontal gene transfer) (Wang et al, 2006;Yoshida et al, 2010;Sakai et al, 2011). Relatively few studies have searched for retrogenes at the genome-wide scale in plants (Zhang et al, 2005;Wang et al, 2006;Zhu et al, 2009;Sakai et al, 2011).…”

“…Therefore, retroposition has a high potential to generate evolutionary innovations (e.g., by expressing genes in a new developmental context, generating chimeric genes with new functional domain combinations, or interspecific horizontal gene transfer) (Wang et al, 2006;Yoshida et al, 2010;Sakai et al, 2011). Relatively few studies have searched for retrogenes at the genome-wide scale in plants (Zhang et al, 2005;Wang et al, 2006;Zhu et al, 2009;Sakai et al, 2011). These studies have identified at most 0.38% of protein-coding genes as retrogenes, except for a study in maize (Zea mays) where low-stringency selection criteria were applied (Wang et al, 2006).…”

“…Therefore, 3.4% of all human genes are retrocopies producing putatively functional proteins (Marques et al, 2005;Pennisi, 2012). In rice (Oryza sativa subsp japonica), transcription was observed for two-thirds of retrogenes, indirectly suggesting that there may be a higher proportion of functional retrogenes in plants (Sakai et al, 2011).…”