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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 (Betran 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 antimicrobial 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 sporophyticThe 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 (Betran 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 antimicrobial 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.show moreshow less

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Metadaten
Author:Xiao Cui, Yang Lv, Miaolin Chen, Zoran NikoloskiORCiDGND, David Twell, Dabing Zhang
DOI:https://doi.org/10.1016/j.molp.2014.12.008
ISSN:1674-2052 (print)
ISSN:1752-9867 (online)
Pubmed Id:http://www.ncbi.nlm.nih.gov/pubmed?term=25670339
Parent Title (English):Molecular plant
Publisher:Cell Press
Place of publication:Cambridge
Document Type:Article
Language:English
Year of first Publication:2015
Year of Completion:2015
Release Date:2017/03/27
Tag:evolution; pollen; transcriptome; young genes
Volume:8
Issue:6
Pagenumber:11
First Page:935
Last Page:945
Funder:National Natural Science Foundation of China [31230051, 30971739, 31270222, 31110103915]; China Innovative Research Team, Ministry of Education; 111 Project [B14016]; National Key Basic Research Developments Program, Ministry of Science and Technology, China [2013CB126902, 2011CB100101]; 863 High-Tech Project, Ministry of Science and Technology, China [2011AA10A101, 2012AA10A302]
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
Peer Review:Referiert