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Title: A survey of the sorghum transcriptome using single-molecule long reads

Abstract

Alternative splicing and alternative polyadenylation (APA) of pre-mRNAs greatly contribute to transcriptome diversity, coding capacity of a genome and gene regulatory mechanisms in eukaryotes. Second-generation sequencing technologies have been extensively used to analyse transcriptomes. However, a major limitation of short-read data is that it is difficult to accurately predict full-length splice isoforms. Here we sequenced the sorghum transcriptome using Pacific Biosciences single-molecule real-time long-read isoform sequencing and developed a pipeline called TAPIS (Transcriptome Analysis Pipeline for Isoform Sequencing) to identify full-length splice isoforms and APA sites. Our analysis reveals transcriptome-wide full-length isoforms at an unprecedented scale with over 11,000 novel splice isoforms. Additionally, we uncover APA ofB11,000 expressed genes and more than 2,100 novel genes. Lastly, these results greatly enhance sorghum gene annotations and aid in studying gene regulation in this important bioenergy crop. The TAPIS pipeline will serve as a useful tool to analyse Iso-Seq data from any organism.

Authors:
; ; ; ; ; ; ;
Publication Date:
Research Org.:
Colorado State Univ., Fort Collins, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1306471
Grant/Contract Number:  
SC0010733
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Abdel-Ghany, Salah E., Hamilton, Michael, Jacobi, Jennifer L., Ngam, Peter, Devitt, Nicholas, Schilkey, Faye, Ben-Hur, Asa, and Reddy, Anireddy S. N. A survey of the sorghum transcriptome using single-molecule long reads. United States: N. p., 2016. Web. doi:10.1038/ncomms11706.
Abdel-Ghany, Salah E., Hamilton, Michael, Jacobi, Jennifer L., Ngam, Peter, Devitt, Nicholas, Schilkey, Faye, Ben-Hur, Asa, & Reddy, Anireddy S. N. A survey of the sorghum transcriptome using single-molecule long reads. United States. doi:10.1038/ncomms11706.
Abdel-Ghany, Salah E., Hamilton, Michael, Jacobi, Jennifer L., Ngam, Peter, Devitt, Nicholas, Schilkey, Faye, Ben-Hur, Asa, and Reddy, Anireddy S. N. Fri . "A survey of the sorghum transcriptome using single-molecule long reads". United States. doi:10.1038/ncomms11706. https://www.osti.gov/servlets/purl/1306471.
@article{osti_1306471,
title = {A survey of the sorghum transcriptome using single-molecule long reads},
author = {Abdel-Ghany, Salah E. and Hamilton, Michael and Jacobi, Jennifer L. and Ngam, Peter and Devitt, Nicholas and Schilkey, Faye and Ben-Hur, Asa and Reddy, Anireddy S. N.},
abstractNote = {Alternative splicing and alternative polyadenylation (APA) of pre-mRNAs greatly contribute to transcriptome diversity, coding capacity of a genome and gene regulatory mechanisms in eukaryotes. Second-generation sequencing technologies have been extensively used to analyse transcriptomes. However, a major limitation of short-read data is that it is difficult to accurately predict full-length splice isoforms. Here we sequenced the sorghum transcriptome using Pacific Biosciences single-molecule real-time long-read isoform sequencing and developed a pipeline called TAPIS (Transcriptome Analysis Pipeline for Isoform Sequencing) to identify full-length splice isoforms and APA sites. Our analysis reveals transcriptome-wide full-length isoforms at an unprecedented scale with over 11,000 novel splice isoforms. Additionally, we uncover APA ofB11,000 expressed genes and more than 2,100 novel genes. Lastly, these results greatly enhance sorghum gene annotations and aid in studying gene regulation in this important bioenergy crop. The TAPIS pipeline will serve as a useful tool to analyse Iso-Seq data from any organism.},
doi = {10.1038/ncomms11706},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {6}
}

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Cited by: 27 works
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Works referenced in this record:

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journal, April 2008

  • Shen, Yingjia; Ji, Guoli; Haas, Brian J.
  • Nucleic Acids Research, Vol. 36, Issue 9
  • DOI: 10.1093/nar/gkn158

FY Is an RNA 3′ End-Processing Factor that Interacts with FCA to Control the Arabidopsis Floral Transition
journal, June 2003


Targeted 3' Processing of Antisense Transcripts Triggers Arabidopsis FLC Chromatin Silencing
journal, December 2009


Poly(A)-tail profiling reveals an embryonic switch in translational control
journal, January 2014

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journal, November 2006

  • Kertész, Sándor; Kerényi, Zoltán; Mérai, Zsuzsanna
  • Nucleic Acids Research, Vol. 34, Issue 21
  • DOI: 10.1093/nar/gkl737

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Compilation of mRNA Polyadenylation Signals in Arabidopsis Revealed a New Signal Element and Potential Secondary Structures
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Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis
journal, January 2014


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journal, February 2005


Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid
journal, October 2011


SpliceGrapher: detecting patterns of alternative splicing from RNA-Seq data in the context of gene models and EST data
journal, January 2012


A Survey Of The Sorghum Transcriptome Using Single-Molecule Long Reads
dataset, January 2016


    Works referencing / citing this record:

    Comparative transcriptome and coexpression network analysis of carpel quantitative variation in Paeonia rockii
    journal, August 2019


    Genome-wide profiling of the alternative splicing provides insights into development in Plutella xylostella
    journal, June 2019


    Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis
    journal, January 2017


    Bridging the gap between reference and real transcriptomes
    journal, June 2019


    Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis
    journal, January 2017


    Bio-Fuel Crops Research for Energy Security and Rural Development in Developing Countries
    journal, October 2008


    Genome-wide survey of Alternative Splicing in Sorghum Bicolor
    journal, June 2014

    • Panahi, Bahman; Abbaszadeh, Bahram; Taghizadeghan, Mehdi
    • Physiology and Molecular Biology of Plants, Vol. 20, Issue 3
    • DOI: 10.1007/s12298-014-0245-3

    Sweet sorghum as a model system for bioenergy crops
    journal, June 2012


    Long non-coding RNAs and their functions in plants
    journal, October 2015


    FY Is an RNA 3′ End-Processing Factor that Interacts with FCA to Control the Arabidopsis Floral Transition
    journal, June 2003


    The Sorghum bicolor genome and the diversification of grasses
    journal, January 2009

    • Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy
    • Nature, Vol. 457, Issue 7229
    • DOI: 10.1038/nature07723

    Poly(A)-tail profiling reveals an embryonic switch in translational control
    journal, January 2014

    • Subtelny, Alexander O.; Eichhorn, Stephen W.; Chen, Grace R.
    • Nature, Vol. 508, Issue 7494
    • DOI: 10.1038/nature13007

    A single-molecule long-read survey of the human transcriptome
    journal, October 2013

    • Sharon, Donald; Tilgner, Hagen; Grubert, Fabian
    • Nature Biotechnology, Vol. 31, Issue 11
    • DOI: 10.1038/nbt.2705

    Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum
    journal, August 2013

    • Mace, Emma S.; Tai, Shuaishuai; Gilding, Edward K.
    • Nature Communications, Vol. 4, Issue 1
    • DOI: 10.1038/ncomms3320

    Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing
    journal, November 2008

    • Pan, Qun; Shai, Ofer; Lee, Leo J.
    • Nature Genetics, Vol. 40, Issue 12
    • DOI: 10.1038/ng.259

    Assessment of transcript reconstruction methods for RNA-seq
    journal, November 2013

    • Steijger, Tamara; Abril, Josep F.; Engström, Pär G.
    • Nature Methods, Vol. 10, Issue 12
    • DOI: 10.1038/nmeth.2714

    Functional consequences of developmentally regulated alternative splicing
    journal, September 2011

    • Kalsotra, Auinash; Cooper, Thomas A.
    • Nature Reviews Genetics, Vol. 12, Issue 10
    • DOI: 10.1038/nrg3052

    Alternative cleavage and polyadenylation: extent, regulation and function
    journal, June 2013

    • Elkon, Ran; Ugalde, Alejandro P.; Agami, Reuven
    • Nature Reviews Genetics, Vol. 14, Issue 7
    • DOI: 10.1038/nrg3482

    Coupling mRNA processing with transcription in time and space
    journal, February 2014

    • Bentley, David L.
    • Nature Reviews Genetics, Vol. 15, Issue 3
    • DOI: 10.1038/nrg3662

    Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation
    journal, July 2012

    • Sherstnev, Alexander; Duc, Céline; Cole, Christian
    • Nature Structural & Molecular Biology, Vol. 19, Issue 8
    • DOI: 10.1038/nsmb.2345

    Transcriptome profiling for floral development in reblooming cultivar ‘High Noon’ of Paeonia suffruticosa
    journal, October 2019


    A transcriptome atlas of rabbit revealed by PacBio single-molecule long-read sequencing
    journal, August 2017


    A near complete snapshot of the Zea mays seedling transcriptome revealed from ultra-deep sequencing
    journal, March 2014

    • Martin, Jeffrey A.; Johnson, Nicole V.; Gross, Stephen M.
    • Scientific Reports, Vol. 4, Issue 1
    • DOI: 10.1038/srep04519

    Genomewide comparative analysis of alternative splicing in plants
    journal, April 2006

    • Wang, B. -B.; Brendel, V.
    • Proceedings of the National Academy of Sciences, Vol. 103, Issue 18
    • DOI: 10.1073/pnas.0602039103

    Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation
    journal, July 2011

    • Wu, X.; Liu, M.; Downie, B.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
    • DOI: 10.1073/pnas.1019732108

    Characterization of the human ESC transcriptome by hybrid sequencing
    journal, November 2013

    • Au, K. F.; Sebastiano, V.; Afshar, P. T.
    • Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
    • DOI: 10.1073/pnas.1320101110

    Ectopic Expression of atRSZ33 Reveals Its Function in Splicing and Causes Pleiotropic Changes in Development
    journal, September 2003

    • Kalyna, Maria; Lopato, Sergiy; Barta, Andrea
    • Molecular Biology of the Cell, Vol. 14, Issue 9
    • DOI: 10.1091/mbc.e03-02-0109

    GMAP: a genomic mapping and alignment program for mRNA and EST sequences
    journal, February 2005


    GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data
    journal, August 2012


    proovread : large-scale high-accuracy PacBio correction through iterative short read consensus
    journal, July 2014


    LoRDEC: accurate and efficient long read error correction
    journal, August 2014


    rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data
    journal, September 2019


    Discovery and Expression Analysis of Alternative Splicing Events Conserved among Plant SR Proteins
    journal, December 2013

    • Rauch, Hypaitia B.; Patrick, Tara L.; Klusman, Katarina M.
    • Molecular Biology and Evolution, Vol. 31, Issue 3
    • DOI: 10.1093/molbev/mst238

    miRBase: microRNA sequences, targets and gene nomenclature
    journal, January 2006

    • Griffiths-Jones, S.
    • Nucleic Acids Research, Vol. 34, Issue 90001
    • DOI: 10.1093/nar/gkj112

    Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins
    journal, August 2006

    • Kalyna, Maria; Lopato, Sergiy; Voronin, Viktor
    • Nucleic Acids Research, Vol. 34, Issue 16
    • DOI: 10.1093/nar/gkl570

    Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants
    journal, November 2006

    • Kertész, Sándor; Kerényi, Zoltán; Mérai, Zsuzsanna
    • Nucleic Acids Research, Vol. 34, Issue 21
    • DOI: 10.1093/nar/gkl737

    miRBase: tools for microRNA genomics
    journal, December 2007

    • Griffiths-Jones, S.; Saini, H. K.; van Dongen, S.
    • Nucleic Acids Research, Vol. 36, Issue Database
    • DOI: 10.1093/nar/gkm952

    Genome level analysis of rice mRNA 3′-end processing signals and alternative polyadenylation
    journal, April 2008

    • Shen, Yingjia; Ji, Guoli; Haas, Brian J.
    • Nucleic Acids Research, Vol. 36, Issue 9
    • DOI: 10.1093/nar/gkn158

    MEME SUITE: tools for motif discovery and searching
    journal, May 2009

    • Bailey, T. L.; Boden, M.; Buske, F. A.
    • Nucleic Acids Research, Vol. 37, Issue Web Server
    • DOI: 10.1093/nar/gkp335

    miRBase: integrating microRNA annotation and deep-sequencing data
    journal, October 2010

    • Kozomara, A.; Griffiths-Jones, S.
    • Nucleic Acids Research, Vol. 39, Issue Database
    • DOI: 10.1093/nar/gkq1027

    miRBase: annotating high confidence microRNAs using deep sequencing data
    journal, November 2013

    • Kozomara, Ana; Griffiths-Jones, Sam
    • Nucleic Acids Research, Vol. 42, Issue D1
    • DOI: 10.1093/nar/gkt1181

    atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes
    journal, April 1999

    • Lopato, S.; Kalyna, M.; Dorner, S.
    • Genes & Development, Vol. 13, Issue 8
    • DOI: 10.1101/gad.13.8.987

    Genome-wide mapping of alternative splicing in Arabidopsis thaliana
    journal, October 2009

    • Filichkin, S. A.; Priest, H. D.; Givan, S. A.
    • Genome Research, Vol. 20, Issue 1
    • DOI: 10.1101/gr.093302.109

    Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis
    journal, March 2012

    • Marquez, Yamile; Brown, John W. S.; Simpson, Craig
    • Genome Research, Vol. 22, Issue 6
    • DOI: 10.1101/gr.134106.111

    Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis
    journal, January 2014


    Compilation of mRNA Polyadenylation Signals in Arabidopsis Revealed a New Signal Element and Potential Secondary Structures
    journal, June 2005

    • Loke, Johnny C.; Stahlberg, Eric A.; Strenski, David G.
    • Plant Physiology, Vol. 138, Issue 3
    • DOI: 10.1104/pp.105.060541

    Complexity of the Alternative Splicing Landscape in Plants
    journal, October 2013

    • Reddy, Anireddy S. N.; Marquez, Yamile; Kalyna, Maria
    • The Plant Cell, Vol. 25, Issue 10
    • DOI: 10.1105/tpc.113.117523

    Genome-Wide Analysis of Alternative Splicing in Zea mays: Landscape and Genetic Regulation
    journal, September 2014


    Genome-Wide Analysis of Alternative Splicing Landscapes Modulated during Plant-Virus Interactions in Brachypodium distachyon
    journal, January 2015


    A global survey of alternative splicing in allopolyploid cotton: landscape, complexity and regulation
    journal, September 2017

    • Wang, Maojun; Wang, Pengcheng; Liang, Fan
    • New Phytologist, Vol. 217, Issue 1
    • DOI: 10.1111/nph.14762

    Identification of an intronic splicing regulatory element involved in auto-regulation of alternative splicing of SCL33 pre-mRNA
    journal, October 2012

    • Thomas, Julie; Palusa, Saiprasad G.; Prasad, Kasavajhala V. S. K.
    • The Plant Journal, Vol. 72, Issue 6
    • DOI: 10.1111/tpj.12004

    The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization
    journal, December 2017

    • McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash
    • The Plant Journal, Vol. 93, Issue 2
    • DOI: 10.1111/tpj.13781

    Targeted 3' Processing of Antisense Transcripts Triggers Arabidopsis FLC Chromatin Silencing
    journal, December 2009


    Regulation of mRNA Translation and Stability by microRNAs
    journal, June 2010


    Regulation of Alternative Splicing Through Coupling with Transcription and Chromatin Structure
    journal, June 2015


    Alternative Splicing of Pre-Messenger RNAs in Plants in the Genomic Era
    journal, June 2007


    Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid
    journal, October 2011


    SpliceGrapher: detecting patterns of alternative splicing from RNA-Seq data in the context of gene models and EST data
    journal, January 2012


    Single-molecule real-time transcript sequencing identified flowering regulatory genes in Crocus sativus
    journal, November 2019


    Candidate genes for grape white rot resistance based on SMRT and Illumina sequencing
    journal, November 2019


    Exploiting single-molecule transcript sequencing for eukaryotic gene prediction
    journal, September 2015


    ReorientExpress: reference-free orientation of nanopore cDNA reads with deep learning
    journal, November 2019


    Deciphering highly similar multigene family transcripts from Iso-Seq data with IsoCon
    journal, November 2018

    • Sahlin, Kristoffer; Tomaszkiewicz, Marta; Makova, Kateryna D.
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-06910-x

    Transcriptome profiling for floral development in reblooming cultivar ‘High Noon’ of Paeonia suffruticosa
    journal, October 2019


    A transcriptome atlas of rabbit revealed by PacBio single-molecule long-read sequencing
    journal, August 2017


    rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data
    journal, September 2019


    Detecting alternatively spliced transcript isoforms from single-molecule long-read sequences without a reference genome
    journal, June 2017

    • Liu, Xiaoxian; Mei, Wenbin; Soltis, Pamela S.
    • Molecular Ecology Resources, Vol. 17, Issue 6
    • DOI: 10.1111/1755-0998.12670

    A global survey of alternative splicing in allopolyploid cotton: landscape, complexity and regulation
    journal, September 2017

    • Wang, Maojun; Wang, Pengcheng; Liang, Fan
    • New Phytologist, Vol. 217, Issue 1
    • DOI: 10.1111/nph.14762

    The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization
    journal, December 2017

    • McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash
    • The Plant Journal, Vol. 93, Issue 2
    • DOI: 10.1111/tpj.13781

    Genome-wide profiling of the alternative splicing provides insights into development in Plutella xylostella
    journal, June 2019


    Comparative transcriptome and coexpression network analysis of carpel quantitative variation in Paeonia rockii
    journal, August 2019


    Single-molecule real-time transcript sequencing identified flowering regulatory genes in Crocus sativus
    journal, November 2019


    Candidate genes for grape white rot resistance based on SMRT and Illumina sequencing
    journal, November 2019


    Bridging the gap between reference and real transcriptomes
    journal, June 2019


    ReorientExpress: reference-free orientation of nanopore cDNA reads with deep learning
    journal, November 2019


    Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis
    journal, January 2017


    Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis
    journal, January 2017


    Analysis of Transcriptome and Epitranscriptome in Plants Using PacBio Iso-Seq and Nanopore-Based Direct RNA Sequencing
    journal, March 2019


    Analysis and comprehensive comparison of PacBio and nanopore-based RNA sequencing of the Arabidopsis transcriptome
    journal, June 2020


    Transcriptome analysis of heat stress and drought stress in pearl millet based on Pacbio full-length transcriptome sequencing
    journal, July 2020