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

Abstract

Duplications allow for gene functional diversification and accelerate genome evolution. Occasionally, the transposon amplification machinery reverse transcribes the mRNA of a gene, integrates it into the genome, and forms an RNA-duplicated copy: the retrogene. Although retrogenes have been found in plants, their biology and evolution are poorly understood. Here, we identified 251 (216 novel) retrogenes in Arabidopsis thaliana, corresponding to 1% of protein-coding genes. Arabidopsis retrogenes are derived from ubiquitously transcribed parents and reside in gene-rich chromosomal regions. Approximately 25% of retrogenes are cotranscribed with their parents and 3% with head-to-head oriented neighbors. This suggests transcription by novel promoters for 72% of Arabidopsis retrogenes. Many retrogenes reach their transcription maximum in pollen, the tissue analogous to animal spermatocytes, where upregulation of retrogenes has been found previously. This implies an evolutionarily conserved mechanism leading to this transcription pattern of RNA-duplicated genes. During transcriptional repression, retrogenes are depleted of permissive chromatin marks without an obvious enrichment for repressive modifications. However, this pattern is common to many other pollen-transcribed genes independent of their evolutionary origin. Hence, retroposition plays a role in plant genome evolution, and the developmental transcription pattern of retrogenes suggests an analogous regulation of RNA-duplicated genes in plants and animals.

Young Genes out of the Male: An Insight from Evolutionary Age Analysis of the Pollen Transcriptome

“…TE movements bring sequence changes to open chromatin regions, which may also aid the birth of de novo genes. Abdelsamad and Pecinka (2014) reported pollen-specific activation of 216 novel retrogenes in Arabidopsis, which supports the hypothesis of special chromatin states favoring the creation of new genes.…”

“…; see Supplemental Table 5 for a complete list). Since it is known that retrogenes are upregulated in pollen (Abdelsamad and Pecinka, 2014), to rule out the possible bias caused by retrogenes, we removed 95 reported rice retrogenes (Sakai et al, 2011) and 241 reported Arabidopsis retrogenes (Abdelsamad and Pecinka, 2014) from the phylostrata rank data sets in the TAI computation.…”

First proteome study of sporadic flowering in bamboo species (Bambusa vulgaris and Dendrocalamus manipureanus) reveal the boom is associated with stress and mobile genetic elements

“…This is important because genes identified in transcriptome data are not often translated into functional proteins. Some important passenger's genes are retrogenes whose mobility allows them to reach their transcriptional maximum in pollens (Abdelsamad and Pecinka, 2014). Sporadic flowering is an active process that could deplete the vital energy required for survival and hence prompt death of bamboo clumps.…”

“…Previously, it was shown that small interfering RNAs originating from genome transposable elements renders the FLOWERING LOCUS C (FLC)-Ler subject to repressive chromatin modifications with implications in the natural flowering behaviour in Arabidopsis(Liu et al, 2004). These studies(Liu et al, 2004;Abdelsamad and Pecinka, 2014; Tamaki et al, 2014) highlight the importance of mobile genetic elements in flowering. A previous study on in vitro chemical induction of flowering boom in Bambusa oldhamii identified transposable elements, stress related proteins and proteins with unknown functions(Lin et al, 2010) akin to the present study.…”

PlantRGDB: A Database of Plant Retrocopied Genes

“…A few studies have demonstrated that retrogenes may also be functional in plants. Retrogenes are up-regulated and play a role in pollen development in Arabidopsis (Abdelsamad and Pecinka 2014). Rice retrogenes have persisted longer than would be expected for nonfunctional elements and are under selection (Wang et al 2006).…”