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Title: The Ancient Salicoid Genome Duplication Event: A Platform for Reconstruction of De Novo Gene Evolution in Populus trichocarpa

Abstract

Orphan genes are characteristic genomic features that have no detectable homology to genes in any other species and represent an important attribute of genome evolution as sources of novel genetic functions. Here, we identified 445 genes specific to Populus trichocarpa. Of these, we performed deeper reconstruction of 13 orphan genes to provide evidence of de novo gene evolution. Populus and its sister genera Salix are particularly well suited for the study of orphan gene evolution because of the Salicoid whole-genome duplication event which resulted in highly syntenic sister chromosomal segments across the Salicaceae. We leveraged this genomic feature to reconstruct de novo gene evolution from intergenera, interspecies, and intragenomic perspectives by comparing the syntenic regions within the P. trichocarpa reference, then P. deltoides, and finally Salix purpurea. Furthermore, we demonstrated that 86.5% of the putative orphan genes had evidence of transcription. Additionally, we also utilized the Populus genome-wide association mapping panel, a collection of 1,084 undomesticated P. trichocarpa genotypes to further determine putative regulatory networks of orphan genes using expression quantitative trait loci (eQTL) mapping. Functional enrichment of these eQTL subnetworks identified common biological themes associated with orphan genes such as response to stress and defense response. We also identifymore » a putative cis-element for a de novo gene and leverage conserved synteny to describe evolution of a putative transcription factor binding site. Overall, 45% of orphan genes were captured in trans-eQTL networks.« less

Authors:
 [1];  [2]; ORCiD logo [2];  [3];  [2];  [2]; ORCiD logo [2];  [3];  [3];  [4]; ORCiD logo [5]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
  3. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Univ. of Oklahoma, Norman, OK (United States)
  5. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1823342
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Genome Biology and Evolution
Additional Journal Information:
Journal Volume: 13; Journal Issue: 9; Journal ID: ISSN 1759-6653
Publisher:
Society for Molecular Biology and Evolution
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; orphan genes; de novo gene evolution; genome evolution; whole-genome duplication; gene regulation; synteny

Citation Formats

Yates, Timothy, Feng, Kai, Zhang, Jin, Singan, Vasanth, Jawdy, Sara, Ranjan, Priya, Abraham, Paul, Barry, Kerrie, Lipzen, Anna, Pan, Chongle, Schmutz, Jeremy, Chen, Jay-Gui, Tuskan, Gerald A., and Muchero, Wellington. The Ancient Salicoid Genome Duplication Event: A Platform for Reconstruction of De Novo Gene Evolution in Populus trichocarpa. United States: N. p., 2021. Web. doi:10.1093/gbe/evab198.
Yates, Timothy, Feng, Kai, Zhang, Jin, Singan, Vasanth, Jawdy, Sara, Ranjan, Priya, Abraham, Paul, Barry, Kerrie, Lipzen, Anna, Pan, Chongle, Schmutz, Jeremy, Chen, Jay-Gui, Tuskan, Gerald A., & Muchero, Wellington. The Ancient Salicoid Genome Duplication Event: A Platform for Reconstruction of De Novo Gene Evolution in Populus trichocarpa. United States. https://doi.org/10.1093/gbe/evab198
Yates, Timothy, Feng, Kai, Zhang, Jin, Singan, Vasanth, Jawdy, Sara, Ranjan, Priya, Abraham, Paul, Barry, Kerrie, Lipzen, Anna, Pan, Chongle, Schmutz, Jeremy, Chen, Jay-Gui, Tuskan, Gerald A., and Muchero, Wellington. Wed . "The Ancient Salicoid Genome Duplication Event: A Platform for Reconstruction of De Novo Gene Evolution in Populus trichocarpa". United States. https://doi.org/10.1093/gbe/evab198. https://www.osti.gov/servlets/purl/1823342.
@article{osti_1823342,
title = {The Ancient Salicoid Genome Duplication Event: A Platform for Reconstruction of De Novo Gene Evolution in Populus trichocarpa},
author = {Yates, Timothy and Feng, Kai and Zhang, Jin and Singan, Vasanth and Jawdy, Sara and Ranjan, Priya and Abraham, Paul and Barry, Kerrie and Lipzen, Anna and Pan, Chongle and Schmutz, Jeremy and Chen, Jay-Gui and Tuskan, Gerald A. and Muchero, Wellington},
abstractNote = {Orphan genes are characteristic genomic features that have no detectable homology to genes in any other species and represent an important attribute of genome evolution as sources of novel genetic functions. Here, we identified 445 genes specific to Populus trichocarpa. Of these, we performed deeper reconstruction of 13 orphan genes to provide evidence of de novo gene evolution. Populus and its sister genera Salix are particularly well suited for the study of orphan gene evolution because of the Salicoid whole-genome duplication event which resulted in highly syntenic sister chromosomal segments across the Salicaceae. We leveraged this genomic feature to reconstruct de novo gene evolution from intergenera, interspecies, and intragenomic perspectives by comparing the syntenic regions within the P. trichocarpa reference, then P. deltoides, and finally Salix purpurea. Furthermore, we demonstrated that 86.5% of the putative orphan genes had evidence of transcription. Additionally, we also utilized the Populus genome-wide association mapping panel, a collection of 1,084 undomesticated P. trichocarpa genotypes to further determine putative regulatory networks of orphan genes using expression quantitative trait loci (eQTL) mapping. Functional enrichment of these eQTL subnetworks identified common biological themes associated with orphan genes such as response to stress and defense response. We also identify a putative cis-element for a de novo gene and leverage conserved synteny to describe evolution of a putative transcription factor binding site. Overall, 45% of orphan genes were captured in trans-eQTL networks.},
doi = {10.1093/gbe/evab198},
journal = {Genome Biology and Evolution},
number = 9,
volume = 13,
place = {United States},
year = {Wed Sep 01 00:00:00 EDT 2021},
month = {Wed Sep 01 00:00:00 EDT 2021}
}

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