Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum

VanBuren, Robert; Bryant, Doug; Edger, Patrick P.; Tang, Haibao; Burgess, Diane; Challabathula, Dinakar; Spittle, Kristi; Hall, Richard; Gu, Jenny; Lyons, Eric; Freeling, Michael; Bartels, Dorothea; Ten Hallers, Boudewijn; Hastie, Alex; Michael, Todd P.; Mockler, Todd C.

doi:10.1038/nature15714

Title: Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum

Journal Article · Wed Nov 11 00:00:00 EST 2015 · Nature (London)

DOI:https://doi.org/10.1038/nature15714· OSTI ID:1436509

VanBuren, Robert ^[1]; Bryant, Doug ^[1]; Edger, Patrick P. ^[2]; Tang, Haibao ^[3]; Burgess, Diane ^[4]; Challabathula, Dinakar ^[5]; Spittle, Kristi ^[6]; Hall, Richard ^[6]; Gu, Jenny ^[6]; Lyons, Eric ^[7]; Freeling, Michael ^[4]; Bartels, Dorothea ^[8]; Ten Hallers, Boudewijn ^[9]; Hastie, Alex ^[9]; Michael, Todd P. ^[10]; Mockler, Todd C. ^[1]

Donal Danforth Plant Science Center, St. Louis, MO (United States)
Univ. of California, Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States)
Univ. of Arizona, Tucson, AZ (United States); Fujan Agriculture and Forestry Univ., Fuzhou (China)
Univ. of California, Berkeley, CA (United States)
Univ. of Bonn, Bonn (Germany); Central Univ. of Tamil Nadu, Thiruvarur (India)
Pacific Biosciences, Menlo Park, CA (United States)
Univ. of Arizona, Tucson, AZ (United States)
Univ. of Bonn, Bonn (Germany)
BioNano Genomics, San Diego, CA (United States)
Ibis Biosciences, Carlsbad, CA (United States)

Plant genomes, and eukaryotic genomes in general, are typically repetitive, polyploid and heterozygous, which complicates genome assembly1. The short read lengths of early Sanger and current next-generation sequencing platforms hinder assembly through complex repeat regions, and many draft and reference genomes are fragmented, lacking skewed GC and repetitive intergenic sequences, which are gaining importance due to projects like the Encyclopedia of DNA Elements (ENCODE). Here we report the whole-genome sequencing and assembly of the desiccation-tolerant grass Oropetium thomaeum. Using only single-molecule real-time sequencing, which generates long (>16 kilobases) reads with random errors, we assembled 99% (244 megabases) of the Oropetium genome into 625 contigs with an N50 length of 2.4 megabases. Oropetium is an example of a ‘near-complete’ draft genome which includes gapless coverage over gene space as well as intergenic sequences such as centromeres, telomeres, transposable elements and rRNA clusters that are typically unassembled in draft genomes. Oropetium has 28,466 protein-coding genes and 43% repeat sequences, yet with 30% more compact euchromatic regions it is the smallest known grass genome. As a result, the Oropetium genome demonstrates the utility of single-molecule real-time sequencing for assembling high-quality plant and other eukaryotic genomes, and serves as a valuable resource for the plant comparative genomics community.

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Research Organization:: Donald Danforth Plant Science Center, St. Louis, MO (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0012639

OSTI ID:: 1436509

Journal Information:: Nature (London), Vol. 527, Issue 7579; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 209 works

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How Single Molecule Real-Time Sequencing and Haplotype Phasing Have Enabled Reference-Grade Diploid Genome Assembly of Wine Grapes Minio, Andrea; Lin, Jerry; Gaut, Brandon S. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00826	journal	May 2017
The Sequenced Angiosperm Genomes and Genome Databases Chen, Fei; Dong, Wei; Zhang, Jiawei Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00418	journal	April 2018
Improving the Yield and Nutritional Quality of Forage Crops Capstaff, Nicola M.; Miller, Anthony J. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00535	journal	April 2018
Hardwood Tree Genomics: Unlocking Woody Plant Biology Tuskan, Gerald A.; Groover, Andrew T.; Schmutz, Jeremy Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01799	journal	December 2018
The Dynamic Responses of Cell Walls in Resurrection Plants During Dehydration and Rehydration Chen, Peilei; Jung, Niklas Udo; Giarola, Valentino Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01698	journal	January 2020
Advances in Integrating Genomics and Bioinformatics in the Plant Breeding Pipeline Hu, Haifei; Scheben, Armin; Edwards, David Agriculture, Vol. 8, Issue 6 https://doi.org/10.3390/agriculture8060075	journal	May 2018
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Genome Sequencing and Assembly by Long Reads in Plants Li, Changsheng; Lin, Feng; An, Dong Genes, Vol. 9, Issue 1 https://doi.org/10.3390/genes9010006	journal	December 2017
Full-Length Transcriptome Analysis of the ABCB, PIN/PIN-LIKES, and AUX/LAX Families Involved in Somatic Embryogenesis of Lilium pumilum DC. Fisch. Song, Shengli; Wang, Zhiping; Ren, Yamin International Journal of Molecular Sciences, Vol. 21, Issue 2 https://doi.org/10.3390/ijms21020453	journal	January 2020
The Complete Chloroplast Genome Sequence of the Medicinal Plant Swertia mussotii Using the PacBio RS II Platform Xiang, Beibei; Li, Xiaoxue; Qian, Jun Molecules, Vol. 21, Issue 8 https://doi.org/10.3390/molecules21081029	journal	August 2016
De novo assembly of a Chinese soybean genome Shen, Yanting; Liu, Jing; Geng, Haiying Science China Life Sciences, Vol. 61, Issue 8 https://doi.org/10.1007/s11427-018-9360-0	journal	July 2018
Improved maize reference genome with single-molecule technologies Jiao, Yinping; Peluso, Paul; Shi, Jinghua Nature, Vol. 546, Issue 7659 https://doi.org/10.1038/nature22971	journal	June 2017
Rapid genotype imputation from sequence without reference panels Davies, Robert W.; Flint, Jonathan; Myers, Simon Nature Genetics, Vol. 48, Issue 8 https://doi.org/10.1038/ng.3594	journal	July 2016
Developing naturally stress-resistant crops for a sustainable agriculture Zhang, Heng; Li, Yuanyuan; Zhu, Jian-Kang Nature Plants, Vol. 4, Issue 12 https://doi.org/10.1038/s41477-018-0309-4	journal	November 2018
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Comprehensive evaluation of non-hybrid genome assembly tools for third-generation PacBio long-read sequence data Jayakumar, Vasanthan; Sakakibara, Yasubumi Briefings in Bioinformatics, Vol. 20, Issue 3 https://doi.org/10.1093/bib/bbx147	journal	November 2017
Vegetative desiccation tolerance in the resurrection plant Xerophyta humilis has not evolved through reactivation of the seed canonical LAFL regulatory network Lyall, Rafe; Schlebusch, Stephen A.; Proctor, Jessica The Plant Journal, Vol. 101, Issue 6 https://doi.org/10.1111/tpj.14596	journal	December 2019
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A De Novo Genome Sequence Assembly of the Arabidopsis thaliana Accession Niederzenz-1 Displays Presence/Absence Variation and Strong Synteny Pucker, Boas; Holtgräwe, Daniela; Rosleff Sörensen, Thomas PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0164321	journal	October 2016
Molecular Mechanisms of Acclimatization to Phosphorus Starvation and Recovery Underlying Full-Length Transcriptome Profiling in Barley (Hordeum vulgare L.) Ren, Panrong; Meng, Yaxiong; Li, Baochun Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00500	journal	April 2018
A Partially Phase-Separated Genome Sequence Assembly of the Vitis Rootstock ‘Börner’ (Vitis riparia × Vitis cinerea) and Its Exploitation for Marker Development and Targeted Mapping Holtgräwe, Daniela; Rosleff Soerensen, Thomas; Hausmann, Ludger Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00156	journal	March 2020
Genome-Wide Analysis of ROS Antioxidant Genes in Resurrection Species Suggest an Involvement of Distinct ROS Detoxification Systems during Desiccation Gupta, Saurabh; Dong, Yanni; Dijkwel, Paul P. Zenodo https://doi.org/10.5281/zenodo.3692494	text	January 2019
Sequencing and de novo assembly of a near complete indica rice genome Du, Huilong; Yu, Ying; Ma, Yanfei Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15324	journal	May 2017
Long-read sequencing data analysis for yeasts Yue, Jia-Xing; Liti, Gianni Nature Protocols, Vol. 13, Issue 6 https://doi.org/10.1038/nprot.2018.025	journal	May 2018
Genome-Guided Phylo-Transcriptomic Methods and the Nuclear Phylogenetic Tree of the Paniceae Grasses Washburn, Jacob D.; Schnable, James C.; Conant, Gavin C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-13236-z	journal	October 2017
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Computational aspects underlying genome to phenome analysis in plants Bolger, Anthony M.; Poorter, Hendrik; Dumschott, Kathryn RWTH Aachen University https://doi.org/10.18154/rwth-2019-01486	text	January 2019
Genome-Wide Analysis of ROS Antioxidant Genes in Resurrection Species Suggest an Involvement of Distinct ROS Detoxification Systems during Desiccation Gupta, Saurabh; Dong, Yanni; Dijkwel, Paul P. Universität Potsdam https://doi.org/10.25932/publishup-43729	text	January 2019
plantiSMASH: automated identification, annotation and expression analysis of plant biosynthetic gene clusters Kautsar, Satria A.; Suarez Duran, Hernando G.; Blin, Kai Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx305	journal	April 2017
Recompleting the Caenorhabditis elegans genome Yoshimura, Jun; Ichikawa, Kazuki; Shoura, Massa J. Genome Research, Vol. 29, Issue 6 https://doi.org/10.1101/gr.244830.118	journal	May 2019
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Haplotype-resolved genomes of geminivirus-resistant and geminivirus-susceptible African cassava cultivars Kuon, Joel‑Elias; Qi, Weihong; Schläpfer, Pascal ETH Zurich https://doi.org/10.3929/ethz-b-000366924	text	January 2019
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Characterization, correction and de novo assembly of an Oxford Nanopore genomic dataset from Agrobacterium tumefaciens Deschamps, Stéphane; Mudge, Joann; Cameron, Connor Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28625	journal	June 2016
The nuclear genome of Rhazya stricta and the evolution of alkaloid diversity in a medically relevant clade of Apocynaceae Sabir, Jamal S. M.; Jansen, Robert K.; Arasappan, Dhivya Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33782	journal	September 2016
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Enhancing the GABI-KatArabidopsis thalianaT-DNA Insertion Mutant Database by Incorporating Araport11 Annotation Kleinboelting, Nils; Huep, Gunnar; Weisshaar, Bernd Plant and Cell Physiology https://doi.org/10.1093/pcp/pcw205	journal	December 2016
Contrasting genome dynamics between domesticated and wild yeasts Yue, Jia-Xing; Li, Jing; Aigrain, Louise Nature Genetics https://doi.org/10.1101/076562	journal	September 2016
LTR_retriever: a highly accurate and sensitive program for identification of LTR retrotransposons Ou, Shujun; Jiang, Ning Plant Physiology https://doi.org/10.1101/137141	journal	August 2017
LRSDAY: Long-read Sequencing Data Analysis for Yeasts Yue, Jia-Xing; Liti, Gianni Nature Protocols https://doi.org/10.1101/184572	journal	September 2017
Comparison of the two up-to-date sequencing technologies for genome assembly: HiFi reads of Pacbio Sequel II system and ultralong reads of Oxford Nanopore Lang, Dandan; Zhang, Shilai; Ren, Pingping GigaScience https://doi.org/10.1101/2020.02.13.948489	journal	February 2020
Integrating Genomic Data Sets for Knowledge Discovery: An Informed Approach to Management of Captive Endangered Species Irizarry, Kristopher J. L.; Bryant, Doug; Kalish, Jordan International Journal of Genomics, Vol. 2016 https://doi.org/10.1155/2016/2374610	journal	January 2016
Perspectives on Structural, Physiological, Cellular, and Molecular Responses to Desiccation in Resurrection Plants Neeragunda Shivaraj, Yathisha; Barbara, Plancot; Gugi, Bruno Scientifica, Vol. 2018 https://doi.org/10.1155/2018/9464592	journal	June 2018
Whole Genome Mapping with Feature Sets from High-Throughput Sequencing Data Pan, Yonglong; Wang, Xiaoming; Liu, Lin PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0161583	journal	September 2016
MASQC: Next Generation Sequencing Assists Third Generation Sequencing for Quality Control in N6-Methyladenine DNA Identification Yang, Siqian; Wang, Yaoxin; Chen, Ying Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.00269	journal	March 2020
Quality Control of the Traditional Patent Medicine Yimu Wan Based on SMRT Sequencing and DNA Barcoding Jia, Jing; Xu, Zhichao; Xin, Tianyi Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00926	journal	May 2017
Domestication and Improvement in the Model C4 Grass, Setaria Hu, Hao; Mauro-Herrera, Margarita; Doust, Andrew N. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00719	journal	May 2018
Enzymes and Metabolites in Carbohydrate Metabolism of Desiccation Tolerant Plants Zhang, Qingwei; Song, Xiaomin; Bartels, Dorothea Proteomes, Vol. 4, Issue 4 https://doi.org/10.3390/proteomes4040040	journal	December 2016

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