Evolutionary characteristics of intergenic transcribed regions indicate rare novel genes and widespread noisy transcription in the Poaceae

Lloyd, John P.; Bowman, Megan J.; Azodi, Christina B.; Sowers, Rosalie P.; Moghe, Gaurav D.; Childs, Kevin L.; Shiu, Shin-Han

doi:10.1038/s41598-019-47797-y

Evolutionary characteristics of intergenic transcribed regions indicate rare novel genes and widespread noisy transcription in the Poaceae

Journal Article · Tue Aug 20 00:00:00 EDT 2019 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-019-47797-y· OSTI ID:1619548

; ; ; Sowers, Rosalie P.; Moghe, Gaurav D.; Childs, Kevin L.;

Abstract

Extensive transcriptional activity occurring in intergenic regions of genomes has raised the question whether intergenic transcription represents the activity of novel genes or noisy expression. To address this, we evaluated cross-species and post-duplication sequence and expression conservation of intergenic transcribed regions (ITRs) in four Poaceae species. Among 43,301 ITRs across the four species, 34,460 (80%) are species-specific. ITRs found across species tend to be more divergent in expression and have more recent duplicates compared to annotated genes. To assess if ITRs are functional (under selection), machine learning models were established in Oryza sativa (rice) that could accurately distinguish between phenotype genes and pseudogenes (area under curve-receiver operating characteristic = 0.94). Based on the models, 584 (8%) and 4391 (61%) rice ITRs are classified as likely functional and nonfunctional with high confidence, respectively. ITRs with conserved expression and ancient retained duplicates, features that were not part of the model, are frequently classified as likely-functional, suggesting these characteristics could serve as pragmatic rules of thumb for identifying candidate sequences likely to be under selection. This study also provides a framework to identify novel genes using comparative transcriptomic data to improve genome annotation that is fundamental for connecting genotype to phenotype in crop and model systems.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States). Great Lakes Bioenergy Research Center

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0018409

OSTI ID:: 1619548

Alternate ID(s):: OSTI ID: 1579362

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 9; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (59)

Genome Annotation and Curation Using MAKER and MAKER‐P Campbell, Michael S.; Holt, Carson; Moore, Barry Current Protocols in Bioinformatics, Vol. 48, Issue 1 https://doi.org/10.1002/0471250953.bi0411s48	journal	December 2014
Spatial Clustering for Identification of ChIP-Enriched Regions (SICER) to Map Regions of Histone Methylation Patterns in Embryonic Stem Cells Xu, Shiliyang; Grullon, Sean; Ge, Kai Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-0512-6_5	book	January 2014
Function without purpose: The uses of causal role function in evolutionary biology Amundson, Ron; Lauder, George V. Biology & Philosophy, Vol. 9, Issue 4 https://doi.org/10.1007/BF00850375	journal	October 1994
Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function Pang, Ken C.; Frith, Martin C.; Mattick, John S. Trends in Genetics, Vol. 22, Issue 1 https://doi.org/10.1016/j.tig.2005.10.003	journal	January 2006
New technologies accelerate the exploration of non-coding RNAs in horticultural plants Liu, Degao; Mewalal, Ritesh; Hu, Rongbin Horticulture Research, Vol. 4, Issue 1 https://doi.org/10.1038/hortres.2017.31	journal	July 2017
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
An integrated encyclopedia of DNA elements in the human genome No authors listed Nature, Vol. 489, Issue 7414, p. 57-74 https://doi.org/10.1038/nature11247	journal	September 2012
Diversity and dynamics of the Drosophila transcriptome Brown, James B.; Boley, Nathan; Eisman, Robert Nature, Vol. 512, Issue 7515 https://doi.org/10.1038/nature12962	journal	March 2014
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Trapnell, Cole; Williams, Brian A.; Pertea, Geo Nature Biotechnology, Vol. 28, Issue 5 https://doi.org/10.1038/nbt.1621	journal	May 2010
An expression atlas of rice mRNAs and small RNAs Nobuta, Kan; Venu, R. C.; Lu, Cheng Nature Biotechnology, Vol. 25, Issue 4 https://doi.org/10.1038/nbt1291	journal	March 2007
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis Haas, Brian J.; Papanicolaou, Alexie; Yassour, Moran Nature Protocols, Vol. 8, Issue 8 https://doi.org/10.1038/nprot.2013.084	journal	July 2013
Cis-acting noncoding RNAs: friends and foes Guil, Sònia; Esteller, Manel Nature Structural & Molecular Biology, Vol. 19, Issue 11 https://doi.org/10.1038/nsmb.2428	journal	November 2012
Transcriptional noise and the fidelity of initiation by RNA polymerase II Struhl, Kevin Nature Structural & Molecular Biology, Vol. 14, Issue 2 https://doi.org/10.1038/nsmb0207-103	journal	February 2007
Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics Paterson, A. H.; Bowers, J. E.; Chapman, B. A. Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0307901101	journal	May 2004
Angiosperm genome comparisons reveal early polyploidy in the monocot lineage Tang, H.; Bowers, J. E.; Wang, X. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0908007107	journal	December 2009
Small open reading frames associated with morphogenesis are hidden in plant genomes Hanada, K.; Higuchi-Takeuchi, M.; Okamoto, M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 6 https://doi.org/10.1073/pnas.1213958110	journal	January 2013
Defining functional DNA elements in the human genome Kellis, M.; Wold, B.; Snyder, M. P. Proceedings of the National Academy of Sciences, Vol. 111, Issue 17 https://doi.org/10.1073/pnas.1318948111	journal	April 2014
PHAST and RPHAST: phylogenetic analysis with space/time models Hubisz, M. J.; Pollard, K. S.; Siepel, A. Briefings in Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1093/bib/bbq072	journal	December 2010
The uniqueome: a mappability resource for short-tag sequencing Koehler, Ryan; Issac, Hadar; Cloonan, Nicole Bioinformatics, Vol. 27, Issue 2 https://doi.org/10.1093/bioinformatics/btq640	journal	November 2010
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
On the Immortality of Television Sets: "Function" in the Human Genome According to the Evolution-Free Gospel of ENCODE Graur, D.; Zheng, Y.; Price, N. Genome Biology and Evolution, Vol. 5, Issue 3 https://doi.org/10.1093/gbe/evt028	journal	January 2013
Distinguishing between "Function" and "Effect" in Genome Biology Doolittle, W. F.; Brunet, T. D. P.; Linquist, S. Genome Biology and Evolution, Vol. 6, Issue 5 https://doi.org/10.1093/gbe/evu098	journal	May 2014
PAML 4: Phylogenetic Analysis by Maximum Likelihood Yang, Z. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm088	journal	April 2007
Gene Space Dynamics During the Evolution of Aegilops tauschii, Brachypodium distachyon, Oryza sativa, and Sorghum bicolor Genomes Massa, A. N.; Wanjugi, H.; Deal, K. R. Molecular Biology and Evolution, Vol. 28, Issue 9 https://doi.org/10.1093/molbev/msr080	journal	April 2011
Conservation and Functional Element Discovery in 20 Angiosperm Plant Genomes Hupalo, D.; Kern, A. D. Molecular Biology and Evolution, Vol. 30, Issue 7 https://doi.org/10.1093/molbev/mst082	journal	May 2013
Defining Functional Genic Regions in the Human Genome through Integration of Biochemical, Evolutionary, and Genetic Evidence Tsai, Zing Tsung-Yeh; Lloyd, John P.; Shiu, Shin-Han Molecular Biology and Evolution, Vol. 34, Issue 7 https://doi.org/10.1093/molbev/msx101	journal	April 2017
A Model-Based Approach for Identifying Functional Intergenic Transcribed Regions and Noncoding RNAs Lloyd, John P.; Tsai, Zing Tsung-Yeh; Sowers, Rosalie P. Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy035	journal	March 2018
Regulated functional alternative splicing in Drosophila Venables, J. P.; Tazi, J.; Juge, F. Nucleic Acids Research, Vol. 40, Issue 1 https://doi.org/10.1093/nar/gkr648	journal	September 2011
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
miRBase: annotating high confidence microRNAs using deep sequencing data Kozomara, Ana; Griffiths-Jones, Sam Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1181	journal	November 2013
Rfam 12.0: updates to the RNA families database Nawrocki, Eric P.; Burge, Sarah W.; Bateman, Alex Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1063	journal	November 2014
Araport: the Arabidopsis Information Portal Krishnakumar, Vivek; Hanlon, Matthew R.; Contrino, Sergio Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1200	journal	November 2014
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Extensive microRNA-mediated crosstalk between lncRNAs and mRNAs in mouse embryonic stem cells Tan, Jennifer Y.; Sirey, Tamara; Honti, Frantisek Genome Research, Vol. 25, Issue 5 https://doi.org/10.1101/gr.181974.114	journal	March 2015
Determinants of nucleosome positioning and their influence on plant gene expression Liu, Ming-Jung; Seddon, Alexander E.; Tsai, Zing Tsung-Yeh Genome Research, Vol. 25, Issue 8 https://doi.org/10.1101/gr.188680.114	journal	June 2015
Aligning Multiple Genomic Sequences With the Threaded Blockset Aligner Blanchette, M. Genome Research, Vol. 14, Issue 4 https://doi.org/10.1101/gr.1933104	journal	April 2004
The time-resolved transcriptome of C. elegans Boeck, Max E.; Huynh, Chau; Gevirtzman, Lou Genome Research, Vol. 26, Issue 10 https://doi.org/10.1101/gr.202663.115	journal	August 2016
Close Split of Sorghum and Maize Genome Progenitors Swigonova, Z. Genome Research, Vol. 14, Issue 10a https://doi.org/10.1101/gr.2332504	journal	September 2004
Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes Siepel, A. Genome Research, Vol. 15, Issue 8 https://doi.org/10.1101/gr.3715005	journal	August 2005
MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes Cantarel, B. L.; Korf, I.; Robb, S. M. C. Genome Research, Vol. 18, Issue 1 https://doi.org/10.1101/gr.6743907	journal	November 2007
Evolutionary and Expression Signatures of Pseudogenes in Arabidopsis and Rice Zou, Cheng; Lehti-Shiu, Melissa D.; Thibaud-Nissen, Françoise Plant Physiology, Vol. 151, Issue 1 https://doi.org/10.1104/pp.109.140632	journal	July 2009
Characteristics and Significance of Intergenic Polyadenylated RNA Transcription in Arabidopsis Moghe, Gaurav D.; Lehti-Shiu, Melissa D.; Seddon, Alex E. Plant Physiology, Vol. 161, Issue 1 https://doi.org/10.1104/pp.112.205245	journal	November 2012
MAKER-P: A Tool Kit for the Rapid Creation, Management, and Quality Control of Plant Genome Annotations Campbell, Michael S.; Law, MeiYee; Holt, Carson Plant Physiology, Vol. 164, Issue 2 https://doi.org/10.1104/pp.113.230144	journal	December 2013
Automated Update, Revision, and Quality Control of the Maize Genome Annotations Using MAKER-P Improves the B73 RefGen_v3 Gene Models and Identifies New Genes Law, MeiYee; Childs, Kevin L.; Campbell, Michael S. Plant Physiology, Vol. 167, Issue 1 https://doi.org/10.1104/pp.114.245027	journal	November 2014
Seventy Million Years of Concerted Evolution of a Homoeologous Chromosome Pair, in Parallel, in Major Poaceae Lineages Wang, Xiyin; Tang, Haibao; Paterson, Andrew H. The Plant Cell, Vol. 23, Issue 1 https://doi.org/10.1105/tpc.110.080622	journal	January 2011
Characteristics of Plant Essential Genes Allow for within- and between-Species Prediction of Lethal Mutant Phenotypes Lloyd, John P.; Seddon, Alexander E.; Moghe, Gaurav D. The Plant Cell, Vol. 27, Issue 8 https://doi.org/10.1105/tpc.15.00051	journal	August 2015
Empirical Analysis of Transcriptional Activity in the Arabidopsis Genome Yamada, K. Science, Vol. 302, Issue 5646 https://doi.org/10.1126/science.1088305	journal	October 2003
Global Identification of Human Transcribed Sequences with Genome Tiling Arrays Bertone, P. Science, Vol. 306, Issue 5705 https://doi.org/10.1126/science.1103388	journal	December 2004
The Transcriptional Landscape of the Yeast Genome Defined by RNA Sequencing Nagalakshmi, U.; Wang, Z.; Waern, K. Science, Vol. 320, Issue 5881 https://doi.org/10.1126/science.1158441	journal	June 2008
The GENCODE pseudogene resource Pei, Baikang; Sisu, Cristina; Frankish, Adam Genome Biology, Vol. 13, Issue 9 https://doi.org/10.1186/gb-2012-13-9-r51	journal	January 2012
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Genome Biology, Vol. 14, Issue 4 https://doi.org/10.1186/gb-2013-14-4-r36	journal	January 2013
Biological function in the twilight zone of sequence conservation Ponting, Chris P. BMC Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12915-017-0411-5	journal	August 2017
An ontology approach to comparative phenomics in plants Oellrich, Anika; Walls, Ramona L.; Cannon, Ethalinda Plant Methods, Vol. 11, Issue 1 https://doi.org/10.1186/s13007-015-0053-y	journal	January 2015
Most “Dark Matter” Transcripts Are Associated With Known Genes van Bakel, Harm; Nislow, Corey; Blencowe, Benjamin J. PLoS Biology, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pbio.1000371	journal	May 2010
Genome-Wide Nucleosome Positioning Is Orchestrated by Genomic Regions Associated with DNase I Hypersensitivity in Rice Wu, Yufeng; Zhang, Wenli; Jiang, Jiming PLoS Genetics, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pgen.1004378	journal	May 2014
Infrageneric Phylogeny and Temporal Divergence of Sorghum (Andropogoneae, Poaceae) Based on Low-Copy Nuclear and Plastid Sequences Liu, Qing; Liu, Huan; Wen, Jun PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0104933	journal	August 2014
Regularization Paths for Generalized Linear Models via Coordinate Descent Friedman, Jerome; Hastie, Trevor; Tibshirani, Robert Journal of Statistical Software, Vol. 33, Issue 1 https://doi.org/10.18637/jss.v033.i01	journal	January 2010
mice : Multivariate Imputation by Chained Equations in R Buuren, Stef van; Groothuis-Oudshoorn, Karin Journal of Statistical Software, Vol. 45, Issue 3 https://doi.org/10.18637/jss.v045.i03	journal	January 2011
Utility of RNA Sequencing for Analysis of Maize Reproductive Transcriptomes Davidson, Rebecca M.; Hansey, Candice N.; Gowda, Malali The Plant Genome Journal, Vol. 4, Issue 3, p. 191-203 https://doi.org/10.3835/plantgenome2011.05.0015	journal	August 2011

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