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

5 Citations (Scopus)

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

Fingerprint

Oryza
protein
gene
genes
proteins
genome
translation (genetics)
transcription (genetics)
proteomics
intergenic DNA
transcriptome
subspecies
open reading frames
RNA
sequence analysis
mass spectrometry
divergence
nucleotide sequences
DNA

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Ecology

Cite this

Zhang, L., Ren, Y., Yang, T., Li, G., Chen, J., Gschwend, A. R., ... 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

Rapid evolution of protein diversity by de novo origination in Oryza. / Zhang, Li; Ren, Yan; Yang, Tao; Li, Guangwei; Chen, Jianhai; Gschwend, Andrea R.; Yu, Yeisoo; Hou, Guixue; Zi, Jin; Zhou, Ruo; Wen, Bo; Zhang, Jianwei -; Chougule, Kapeel; Wang, Muhua; Copetti, Dario; Peng, Zhiyu; Zhang, Chengjun; Zhang, Yong; Ouyang, Yidan; Wing, Rod A; Liu, Siqi; Long, Manyuan.

In: Nature Ecology and Evolution, Vol. 3, No. 4, 01.04.2019, p. 679-690.

Research output: Contribution to journalArticle

Zhang, L, Ren, Y, Yang, T, Li, G, Chen, J, Gschwend, AR, 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, Wing, RA, Liu, S & Long, M 2019, 'Rapid evolution of protein diversity by de novo origination in Oryza', Nature Ecology and Evolution, vol. 3, no. 4, pp. 679-690. https://doi.org/10.1038/s41559-019-0822-5
Zhang, Li ; Ren, Yan ; Yang, Tao ; Li, Guangwei ; Chen, Jianhai ; Gschwend, Andrea R. ; Yu, Yeisoo ; Hou, Guixue ; Zi, Jin ; Zhou, Ruo ; Wen, Bo ; Zhang, Jianwei - ; Chougule, Kapeel ; Wang, Muhua ; Copetti, Dario ; Peng, Zhiyu ; Zhang, Chengjun ; Zhang, Yong ; Ouyang, Yidan ; Wing, Rod A ; Liu, Siqi ; Long, Manyuan. / Rapid evolution of protein diversity by de novo origination in Oryza. In: Nature Ecology and Evolution. 2019 ; Vol. 3, No. 4. pp. 679-690.
@article{c82d0ceab0b34c468ace7b9aa21b7110,
title = "Rapid evolution of protein diversity by de novo origination in Oryza",
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.",
author = "Li Zhang and Yan Ren and Tao Yang and Guangwei Li and Jianhai Chen and Gschwend, {Andrea R.} and Yeisoo Yu and Guixue Hou and Jin Zi and Ruo Zhou and Bo Wen and Zhang, {Jianwei -} and Kapeel Chougule and Muhua Wang and Dario Copetti and Zhiyu Peng and Chengjun Zhang and Yong Zhang and Yidan Ouyang and Wing, {Rod A} and Siqi Liu and Manyuan Long",
year = "2019",
month = "4",
day = "1",
doi = "10.1038/s41559-019-0822-5",
language = "English (US)",
volume = "3",
pages = "679--690",
journal = "Nature Ecology and Evolution",
issn = "2397-334X",
publisher = "Nature Publishing Group",
number = "4",

}

TY - JOUR

T1 - Rapid evolution of protein diversity by de novo origination in Oryza

AU - Zhang, Li

AU - Ren, Yan

AU - Yang, Tao

AU - Li, Guangwei

AU - Chen, Jianhai

AU - Gschwend, Andrea R.

AU - Yu, Yeisoo

AU - Hou, Guixue

AU - Zi, Jin

AU - Zhou, Ruo

AU - Wen, Bo

AU - Zhang, Jianwei -

AU - Chougule, Kapeel

AU - Wang, Muhua

AU - Copetti, Dario

AU - Peng, Zhiyu

AU - Zhang, Chengjun

AU - Zhang, Yong

AU - Ouyang, Yidan

AU - Wing, Rod A

AU - Liu, Siqi

AU - Long, Manyuan

PY - 2019/4/1

Y1 - 2019/4/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85062846033&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85062846033&partnerID=8YFLogxK

U2 - 10.1038/s41559-019-0822-5

DO - 10.1038/s41559-019-0822-5

M3 - Article

C2 - 30858588

AN - SCOPUS:85062846033

VL - 3

SP - 679

EP - 690

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

SN - 2397-334X

IS - 4

ER -