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

Author:

Yates Timothy B123,Feng Kai23,Zhang Jin23ORCID,Singan Vasanth4,Jawdy Sara S23,Ranjan Priya23,Abraham Paul E23,Barry Kerrie4,Lipzen Anna4,Pan Chongle5,Schmutz Jeremy46ORCID,Chen Jin-Gui123,Tuskan Gerald A23,Muchero Wellington123

Affiliation:

1. Bredesen Center for Interdisciplinary Research, University of Tennessee, Knoxville, Tennessee, USA

2. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA

3. Center for Bioenergy Innovation, Oak Ridge, Tennessee, USA

4. U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA

5. School of Computer Science and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA

6. HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, USA

Abstract

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 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.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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