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

The birth of new genes in genomes is an important evolutionary event. Several studies reveal that new genes in animals tend to be preferentially expressed in male reproductive tissues such as testis (Betrán et al., 2002; Begun et al., 2007; Dubruille et al., 2012), and thus an "out of testis" hypothesis for the emergence of new genes has been proposed (Vinckenbosch et al., 2006; Kaessmann, 2010). However, such phenomena have not been examined in plant species. Here, by employing a phylostratigraphic method, we dated the origin of protein-coding genes in rice and Arabidopsis thaliana and observed a number of young genes in both species. These young genes tend to encode short extracellular proteins, which may be involved in rapid evolving processes, such as reproductive barriers, species specification, and anti-microbial processes. Further analysis of transcriptome age indexes across different tissues revealed that male reproductive cells express a phylogenetically younger transcriptome than other plant tissues. Compared with sporophytic tissues, the young transcriptomes of the male gametophyte displayed greater complexity and diversity, which included a higher ratio of anti-sense and inter-genic transcripts, reflecting a pervasive transcription state that facilitated the emergence of new genes. Here, we propose that pollen may act as an "innovation incubator" for the birth of de novo genes. With cases of male-biased expression of young genes reported in animals, the "new genes out of the male" model revealed a common evolutionary force that drives reproductive barriers, species specification, and the upgrading of defensive mechanisms against pathogens.