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

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

doi:10.1093/gbe/evab198

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

Journal Article · Wed Sep 01 00:00:00 EDT 2021 · Genome Biology and Evolution

DOI:https://doi.org/10.1093/gbe/evab198· OSTI ID:1823342

Yates, Timothy ^[1]; Feng, Kai ^[2]; ^[2]; Singan, Vasanth ^[3]; Jawdy, Sara ^[2]; Ranjan, Priya ^[2]; ^[2]; Barry, Kerrie ^[3]; Lipzen, Anna ^[3]; Pan, Chongle ^[4]; ^[5]; ^[1]; ^[2]; ^[1]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of Oklahoma, Norman, OK (United States)
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)

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.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1823342

Journal Information:: Genome Biology and Evolution, Journal Name: Genome Biology and Evolution Journal Issue: 9 Vol. 13; ISSN 1759-6653

Publisher:: Society for Molecular Biology and EvolutionCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

Young Genes out of the Male: An Insight from Evolutionary Age Analysis of the Pollen Transcriptome Cui, Xiao; Lv, Yang; Chen, Miaolin Molecular Plant, Vol. 8, Issue 6 https://doi.org/10.1016/j.molp.2014.12.008	journal	June 2015
Coming of age: orphan genes in plants Arendsee, Zebulun W.; Li, Ling; Wurtele, Eve Syrkin Trends in Plant Science, Vol. 19, Issue 11 https://doi.org/10.1016/j.tplants.2014.07.003	journal	November 2014
Crux: Rapid Open Source Protein Tandem Mass Spectrometry Analysis McIlwain, Sean; Tamura, Kaipo; Kertesz-Farkas, Attila Journal of Proteome Research, Vol. 13, Issue 10 https://doi.org/10.1021/pr500741y	journal	September 2014
The willow genome and divergent evolution from poplar after the common genome duplication Dai, Xiaogang; Hu, Quanjun; Cai, Qingle Cell Research, Vol. 24, Issue 10 https://doi.org/10.1038/cr.2014.83	journal	July 2014
Proto-genes and de novo gene birth Carvunis, Anne-Ruxandra; Rolland, Thomas; Wapinski, Ilan Nature, Vol. 487, Issue 7407 https://doi.org/10.1038/nature11184	journal	June 2012
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli Nature Genetics, Vol. 46, Issue 10 https://doi.org/10.1038/ng.3075	journal	August 2014
Variance component model to account for sample structure in genome-wide association studies Kang, Hyun Min; Sul, Jae Hoon; Service, Susan K. Nature Genetics, Vol. 42, Issue 4 https://doi.org/10.1038/ng.548	journal	March 2010
moFF: a robust and automated approach to extract peptide ion intensities Argentini, Andrea; Goeminne, Ludger J. E.; Verheggen, Kenneth Nature Methods, Vol. 13, Issue 12 https://doi.org/10.1038/nmeth.4075	journal	November 2016
The evolutionary origin of orphan genes Tautz, Diethard; Domazet-Lošo, Tomislav Nature Reviews Genetics, Vol. 12, Issue 10 https://doi.org/10.1038/nrg3053	journal	August 2011
Uncovering de novo gene birth in yeast using deep transcriptomics Blevins, William R.; Ruiz-Orera, Jorge; Messeguer, Xavier Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-20911-3	journal	January 2021
Rapid evolution of protein diversity by de novo origination in Oryza Zhang, Li; Ren, Yan; Yang, Tao Nature Ecology & Evolution, Vol. 3, Issue 4 https://doi.org/10.1038/s41559-019-0822-5	journal	March 2019
Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza Stein, Joshua C.; Yu, Yeisoo; Copetti, Dario Nature Genetics, Vol. 50, Issue 2 https://doi.org/10.1038/s41588-018-0040-0	journal	January 2018
Characterisation and functional predictions of canine long non-coding RNAs Le Béguec, Céline; Wucher, Valentin; Lagoutte, Lætitia Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-31770-2	journal	September 2018
Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression Levine, M. T.; Jones, C. D.; Kern, A. D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 26 https://doi.org/10.1073/pnas.0509809103	journal	June 2006
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe The American Journal of Human Genetics, Vol. 81, Issue 3 https://doi.org/10.1086/519795	journal	September 2007
clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters Yu, Guangchuang; Wang, Li-Gen; Han, Yanyan OMICS: A Journal of Integrative Biology, Vol. 16, Issue 5 https://doi.org/10.1089/omi.2011.0118	journal	May 2012
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
FIMO: scanning for occurrences of a given motif Grant, Charles E.; Bailey, Timothy L.; Noble, William Stafford Bioinformatics, Vol. 27, Issue 7 https://doi.org/10.1093/bioinformatics/btr064	journal	February 2011
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
genBlastG: using BLAST searches to build homologous gene models She, Rong; Chu, Jeffrey Shih-Chieh; Uyar, Bora Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr342	journal	June 2011
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data Li, H. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr509	journal	September 2011
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features Liao, Y.; Smyth, G. K.; Shi, W. Bioinformatics, Vol. 30, Issue 7 https://doi.org/10.1093/bioinformatics/btt656	journal	November 2013
On the Origin of De Novo Genes in Arabidopsis thaliana Populations Li, Zi-Wen; Chen, Xi; Wu, Qiong Genome Biology and Evolution, Vol. 8, Issue 7 https://doi.org/10.1093/gbe/evw164	journal	July 2016
Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity Lim, P. O.; Lee, I. C.; Kim, J. Journal of Experimental Botany, Vol. 61, Issue 5 https://doi.org/10.1093/jxb/erq010	journal	February 2010
Origin of Primate Orphan Genes: A Comparative Genomics Approach Toll-Riera, M.; Bosch, N.; Bellora, N. Molecular Biology and Evolution, Vol. 26, Issue 3 https://doi.org/10.1093/molbev/msn281	journal	December 2008
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Enhancers Facilitate the Birth of De Novo Genes and Gene Integration into Regulatory Networks Majic, Paco; Payne, Joshua L. Molecular Biology and Evolution, Vol. 37, Issue 4 https://doi.org/10.1093/molbev/msz300	journal	December 2019
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Wang, Y.; Tang, H.; DeBarry, J. D. Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1293	journal	January 2012
CDD: NCBI's conserved domain database Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1221	journal	November 2014
PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants Chow, Chi-Nga; Lee, Tzong-Yi; Hung, Yu-Cheng Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1081	journal	November 2018
Recent de novo origin of human protein-coding genes Knowles, D. G.; McLysaght, A. Genome Research, Vol. 19, Issue 10 https://doi.org/10.1101/gr.095026.109	journal	September 2009
Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation Werner, Michael S.; Sieriebriennikov, Bogdan; Prabh, Neel Genome Research, Vol. 28, Issue 11 https://doi.org/10.1101/gr.234872.118	journal	September 2018
Genome-wide association studies and expression-based quantitative trait loci analyses reveal roles of HCT2 in caffeoylquinic acid biosynthesis and its regulation by defense-responsive transcription factors in Populus Zhang, Jin; Yang, Yongil; Zheng, Kaijie New Phytologist, Vol. 220, Issue 2 https://doi.org/10.1111/nph.15297	journal	July 2018
QQS orphan gene and its interactor NF ‐ YC 4 reduce susceptibility to pathogens and pests Qi, Mingsheng; Zheng, Wenguang; Zhao, Xuefeng Plant Biotechnology Journal, Vol. 17, Issue 1 https://doi.org/10.1111/pbi.12961	journal	July 2018
The Arabidopsis ceramidase At ACER functions in disease resistance and salt tolerance Wu, Jian-Xin; Li, Jian; Liu, Zhe The Plant Journal, Vol. 81, Issue 5 https://doi.org/10.1111/tpj.12769	journal	February 2015
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Tuskan, G. A.; DiFazio, S.; Jansson, S. Science, Vol. 313, Issue 5793, p. 1596-1604 https://doi.org/10.1126/science.1128691	journal	September 2006
Synteny and Collinearity in Plant Genomes Tang, H.; Bowers, J. E.; Wang, X. Science, Vol. 320, Issue 5875 https://doi.org/10.1126/science.1153917	journal	April 2008
Origin and Spread of de Novo Genes in Drosophila melanogaster Populations Zhao, L.; Saelao, P.; Jones, C. D. Science, Vol. 343, Issue 6172 https://doi.org/10.1126/science.1248286	journal	January 2014
Evolution and tinkering Jacob, F. Science, Vol. 196, Issue 4295 https://doi.org/10.1126/science.860134	journal	June 1977
Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: two essential mechanisms of Fusarium head blight resistance in wheat? Gottwald, Sven; Samans, Birgit; Lück, Stefanie BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-369	journal	January 2012
A Human-Specific De Novo Protein-Coding Gene Associated with Human Brain Functions Li, Chuan-Yun; Zhang, Yong; Wang, Zhanbo PLoS Computational Biology, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pcbi.1000734	journal	March 2010
MUMmer4: A fast and versatile genome alignment system Marçais, Guillaume; Delcher, Arthur L.; Phillippy, Adam M. PLOS Computational Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pcbi.1005944	journal	January 2018
A Rice Gene of De Novo Origin Negatively Regulates Pathogen-Induced Defense Response Xiao, Wenfei; Liu, Hongbo; Li, Yu PLoS ONE, Vol. 4, Issue 2 https://doi.org/10.1371/journal.pone.0004603	journal	February 2009
Evidence for de Novo Evolution of Testis-Expressed Genes in the Drosophila yakuba / Drosophila erecta Clade Begun, David J.; Lindfors, Heather A.; Kern, Andrew D. Genetics, Vol. 176, Issue 2 https://doi.org/10.1534/genetics.106.069245	journal	April 2007
The Enormous Diversity in Genome Sizes of Fish as a Reflection of Nature's Extensive Experiments with Gene Duplication Ohno, Susumu Transactions of the American Fisheries Society, Vol. 99, Issue 1 https://doi.org/10.1577/1548-8659(1970)99<120:TEDIGS>2.0.CO;2	journal	January 1970
Are Antisense Proteins in Prokaryotes Functional? Ardern, Zachary; Neuhaus, Klaus; Scherer, Siegfried Frontiers in Molecular Biosciences, Vol. 7 https://doi.org/10.3389/fmolb.2020.00187	journal	August 2020
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w Cingolani, Pablo; Platts, Adrian; Wang, Le Lily Fly, Vol. 6, Issue 2 https://doi.org/10.4161/fly.19695	journal	April 2012

Similar Records

Characterization of a large sex determination region in Salix purpurea L. (Salicaceae)

Journal Article · Wed Jul 18 00:00:00 EDT 2018 · Molecular Genetics and Genomics · OSTI ID:1494877

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
de novo gene evolution
gene regulation
genome evolution
orphan genes
synteny
whole-genome duplication

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

Citation Formats

References (50)

Similar Records

Related Subjects