Rapid evolution of protein diversity by de novo origination in Oryza

Li Zhang, Yan Ren, Tao Yang, Guangwei Li, Jianhai Chen, Andrea R. Gschwend, Yeisoo Yu, Guixue Hou, Jin Zi, Ruo Zhou, Bo Wen, Jianwei Zhang, Kapeel Chougule, Muhua Wang, Dario Copetti, Zhiyu Peng, Chengjun Zhang, Yong Zhang, Yidan Ouyang, Rod A. WingSiqi Liu, Manyuan Long

Research output: Contribution to journalArticle

20 Scopus citations

Abstract

New protein-coding genes that arise de novo from non-coding DNA sequences contribute to protein diversity. However, de novo gene origination is challenging to study as it requires high-quality reference genomes for closely related species, evidence for ancestral non-coding sequences, and transcription and translation of the new genes. High-quality genomes of 13 closely related Oryza species provide unprecedented opportunities to understand de novo origination events. Here, we identify a large number of young de novo genes with discernible recent ancestral non-coding sequences and evidence of translation. Using pipelines examining the synteny relationship between genomes and reciprocal-best whole-genome alignments, we detected at least 175 de novo open reading frames in the focal species O. sativa subspecies japonica, which were all detected in RNA sequencing-based transcriptomes. Mass spectrometry-based targeted proteomics and ribosomal profiling show translational evidence for 57% of the de novo genes. In recent divergence of Oryza, an average of 51.5 de novo genes per million years were generated and retained. We observed evolutionary patterns in which excess indels and early transcription were favoured in origination with a stepwise formation of gene structure. These data reveal that de novo genes contribute to the rapid evolution of protein diversity under positive selection.

Original languageEnglish (US)
Pages (from-to)679-690
Number of pages12
JournalNature Ecology and Evolution
Volume3
Issue number4
DOIs
StatePublished - Apr 1 2019

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Ecology

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    Zhang, L., Ren, Y., Yang, T., Li, G., Chen, J., Gschwend, A. R., Yu, Y., Hou, G., Zi, J., Zhou, R., Wen, B., Zhang, J., Chougule, K., Wang, M., Copetti, D., Peng, Z., Zhang, C., Zhang, Y., Ouyang, Y., ... Long, M. (2019). Rapid evolution of protein diversity by de novo origination in Oryza. Nature Ecology and Evolution, 3(4), 679-690. https://doi.org/10.1038/s41559-019-0822-5