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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. https://doi.org/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. https://doi.org/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 = {Fri Jun 24 00:00:00 EDT 2016},
month = {Fri Jun 24 00:00:00 EDT 2016}
}

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  • Reddy, Anireddy S. N.; Marquez, Yamile; Kalyna, Maria
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Genome-Wide Analysis of Alternative Splicing Landscapes Modulated during Plant-Virus Interactions in Brachypodium distachyon
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journal, December 2009


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journal, June 2015


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


miRBase: microRNA sequences, targets and gene nomenclature.
text, January 2006

  • Griffiths-Jones, Sam; Grocock, Russell J.; Van Dongen, Stijn
  • Apollo - University of Cambridge Repository
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Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis
journal, January 2017


Screening and characterization of long noncoding RNAs involved in the albinism of Ananas comosus var. bracteatus leaves
journal, November 2019


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


Reviving the Transcriptome Studies: An Insight Into the Emergence of Single-Molecule Transcriptome Sequencing
journal, April 2019


Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching
journal, February 2018

  • Filichkin, Sergei A.; Hamilton, Michael; Dharmawardhana, Palitha D.
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00005

Expanding Alternative Splicing Identification by Integrating Multiple Sources of Transcription Data in Tomato
journal, May 2019


Isoform Sequencing and State-of-Art Applications for Unravelling Complexity of Plant Transcriptomes
journal, January 2018


Full-Length Transcriptome Sequencing and Different Chemotype Expression Profile Analysis of Genes Related to Monoterpenoid Biosynthesis in Cinnamomum porrectum
journal, December 2019

  • Qiu, Fengying; Wang, Xindong; Zheng, Yongjie
  • International Journal of Molecular Sciences, Vol. 20, Issue 24
  • DOI: 10.3390/ijms20246230

PacBio single-molecule long-read sequencing shed new light on the transcripts and splice isoforms of the perennial ryegrass
journal, January 2020


Analysis of transcripts and splice isoforms in Medicago sativa L. by single-molecule long-read sequencing
journal, January 2019


Piercing the dark matter: bioinformatics of long-range sequencing and mapping
journal, March 2018

  • Sedlazeck, Fritz J.; Lee, Hayan; Darby, Charlotte A.
  • Nature Reviews Genetics, Vol. 19, Issue 6
  • DOI: 10.1038/s41576-018-0003-4

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


A survey of transcriptome complexity in Sus scrofa using single-molecule long-read sequencing
journal, May 2018


Genome and Transcriptome Sequencing of the Astaxanthin-Producing Green Microalga, Haematococcus pluvialis
journal, November 2018

  • Luo, Qiulan; Bian, Chao; Tao, Ming
  • Genome Biology and Evolution, Vol. 11, Issue 1
  • DOI: 10.1093/gbe/evy263

De novo clustering of long reads by gene from transcriptomics data
journal, September 2018

  • Marchet, Camille; Lecompte, Lolita; Silva, Corinne Da
  • Nucleic Acids Research, Vol. 47, Issue 1
  • DOI: 10.1093/nar/gky834

IsoCon: Deciphering highly similar multigene family transcripts from Iso-Seq data
posted_content, January 2018

  • Sahlin, Kristoffer; Tomaszkiewicz, Marta; Makova, Kateryna D.
  • bioRxiv
  • DOI: 10.1101/246066

Transcriptome assembly from long-read RNA-seq alignments with StringTie2
posted_content, July 2019

  • Kovaka, Sam; Zimin, Aleksey V.; Pertea, Geo M.
  • bioRxiv
  • DOI: 10.1101/694554

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 developmental dynamics of the Populus stem transcriptome
journal, June 2018

  • Chao, Qing; Gao, Zhi-Fang; Zhang, Dong
  • Plant Biotechnology Journal, Vol. 17, Issue 1
  • DOI: 10.1111/pbi.12958

Genome assembly provides insights into the genome evolution and flowering regulation of orchardgrass
journal, July 2019

  • Huang, Linkai; Feng, Guangyan; Yan, Haidong
  • Plant Biotechnology Journal, Vol. 18, Issue 2
  • DOI: 10.1111/pbi.13205

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


Root Hair Single Cell Type Specific Profiles of Gene Expression and Alternative Polyadenylation Under Cadmium Stress
journal, May 2019


PacBio Long-Read Sequencing Reveals the Transcriptomic Complexity and Aux/IAA Gene Evolution in Gnetum (Gnetales)
journal, November 2019

  • Hou, Chen; Deng, Nan; Su, Yingjuan
  • Forests, Vol. 10, Issue 11
  • DOI: 10.3390/f10111043

Investigation of RNA Editing Sites within Bound Regions of RNA-Binding Proteins
journal, November 2019

  • Weirick, Tyler; Militello, Giuseppe; Hosen, Mohammed Rabiul
  • High-Throughput, Vol. 8, Issue 4
  • DOI: 10.3390/ht8040019

Dynamic Changes in Metabolite Accumulation and the Transcriptome during Leaf Growth and Development in Eucommia ulmoides
journal, August 2019

  • Li, Long; Liu, Minhao; Shi, Kan
  • International Journal of Molecular Sciences, Vol. 20, Issue 16
  • DOI: 10.3390/ijms20164030

Transcriptome Analysis of Drought-Resistant and Drought-Sensitive Sorghum (Sorghum bicolor) Genotypes in Response to PEG-Induced Drought Stress
journal, January 2020

  • Abdel-Ghany, Salah E.; Ullah, Fahad; Ben-Hur, Asa
  • International Journal of Molecular Sciences, Vol. 21, Issue 3
  • DOI: 10.3390/ijms21030772

The Complete Chloroplast Genome Sequence of the Medicinal Plant Swertia mussotii Using the PacBio RS II Platform
journal, August 2016


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


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

PacBio full-length cDNA sequencing integrated with RNA-seq reads drastically improves the discovery of splicing transcripts in rice
journal, December 2018

  • Zhang, Guoqiang; Sun, Min; Wang, Jianfeng
  • The Plant Journal, Vol. 97, Issue 2
  • DOI: 10.1111/tpj.14120

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


Analysis of transcripts and splice isoforms in red clover (Trifolium pratense L.) by single-molecule long-read sequencing
journal, November 2018


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


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

Multi-strategic RNA-seq analysis reveals a high-resolution transcriptional landscape in cotton
journal, October 2019


Poly(A) inclusive RNA isoform sequencing (PAIso−seq) reveals wide-spread non-adenosine residues within RNA poly(A) tails
journal, November 2019


Transcriptomic profiles of 33 opium poppy samples in different tissues, growth phases, and cultivars
journal, May 2019


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


Long noncoding RNAs in the model species Brachypodium distachyon
journal, September 2017


Unveiling novel targets of paclitaxel resistance by single molecule long-read RNA sequencing in breast cancer
journal, April 2019


Variant phasing and haplotypic expression from long-read sequencing in maize
journal, February 2020


De novo hybrid assembly of the rubber tree genome reveals evidence of paleotetraploidy in Hevea species
journal, February 2017

  • Pootakham, Wirulda; Sonthirod, Chutima; Naktang, Chaiwat
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep41457

Genome-wide analysis of complex wheat gliadins, the dominant carriers of celiac disease epitopes
journal, March 2017

  • Wang, Da-Wei; Li, Da; Wang, Junjun
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep44609

Long-read sequencing of the coffee bean transcriptome reveals the diversity of full-length transcripts
journal, August 2017


Single-molecule, full-length transcript sequencing provides insight into the extreme metabolism of the ruby-throated hummingbird Archilochus colubris
journal, February 2018


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


Exploring the fate of mRNA in aging seeds: protection, destruction, or slow decay?
journal, June 2018

  • Fleming, Margaret B.; Patterson, Eric L.; Reeves, Patrick A.
  • Journal of Experimental Botany, Vol. 69, Issue 18
  • DOI: 10.1093/jxb/ery215

High resolution annotation of zebrafish transcriptome using long-read sequencing
journal, July 2018

  • Nudelman, German; Frasca, Antonio; Kent, Brandon
  • Genome Research, Vol. 28, Issue 9
  • DOI: 10.1101/gr.223586.117

The developmental dynamics of the Populus stem transcriptome
journal, June 2018

  • Chao, Qing; Gao, Zhi-Fang; Zhang, Dong
  • Plant Biotechnology Journal, Vol. 17, Issue 1
  • DOI: 10.1111/pbi.12958

Plant ISOform sequencing database (PISO): a comprehensive repertory of full‐length transcripts in plants
journal, January 2019

  • Feng, Jia‐Wu; Huang, Shanshan; Guo, Yi‐Xiong
  • Plant Biotechnology Journal, Vol. 17, Issue 6
  • DOI: 10.1111/pbi.13076

Hybrid sequencing reveals insight into heat sensing and signaling of bread wheat
journal, April 2019

  • Wang, Xiaoming; Chen, Siyuan; Shi, Xue
  • The Plant Journal, Vol. 98, Issue 6
  • DOI: 10.1111/tpj.14299

Characterization and Functional Analysis of Polyadenylation Sites in Fast and Slow Muscles
journal, March 2020

  • Deng, Lulu; Li, Long; Zou, Cheng
  • BioMed Research International, Vol. 2020
  • DOI: 10.1155/2020/2626584

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


Analysis of transcripts and splice isoforms in red clover (Trifolium pratense L.) by single-molecule long-read sequencing
journal, November 2018


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


Revealing the transcriptomic complexity of switchgrass by PacBio long-read sequencing
journal, June 2018

  • Zuo, Chunman; Blow, Matthew; Sreedasyam, Avinash
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1167-z

Dual Platform Long-Read RNA-Sequencing Dataset of the Human Cytomegalovirus Lytic Transcriptome
journal, September 2018


Getting the Entire Message: Progress in Isoform Sequencing
journal, August 2019


Long Non-coding RNAs in Endothelial Biology
journal, May 2018


Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching
journal, February 2018

  • Filichkin, Sergei A.; Hamilton, Michael; Dharmawardhana, Palitha D.
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00005

Integrative Analysis of Three RNA Sequencing Methods Identifies Mutually Exclusive Exons of MADS-Box Isoforms During Early Bud Development in Picea abies
journal, November 2018

  • Akhter, Shirin; Kretzschmar, Warren W.; Nordal, Veronika
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01625

Root Hair Single Cell Type Specific Profiles of Gene Expression and Alternative Polyadenylation Under Cadmium Stress
journal, May 2019


Expanding Alternative Splicing Identification by Integrating Multiple Sources of Transcription Data in Tomato
journal, May 2019


Investigation of RNA Editing Sites within Bound Regions of RNA-Binding Proteins
journal, November 2019

  • Weirick, Tyler; Militello, Giuseppe; Hosen, Mohammed Rabiul
  • High-Throughput, Vol. 8, Issue 4
  • DOI: 10.3390/ht8040019

Dynamic Changes in Metabolite Accumulation and the Transcriptome during Leaf Growth and Development in Eucommia ulmoides
journal, August 2019

  • Li, Long; Liu, Minhao; Shi, Kan
  • International Journal of Molecular Sciences, Vol. 20, Issue 16
  • DOI: 10.3390/ijms20164030

Full-Length Transcriptome Assembly of Italian Ryegrass Root Integrated with RNA-Seq to Identify Genes in Response to Plant Cadmium Stress
journal, February 2020

  • Hu, Zhaoyang; Zhang, Yufei; He, Yue
  • International Journal of Molecular Sciences, Vol. 21, Issue 3
  • DOI: 10.3390/ijms21031067

Co-Expression Network Analysis of Spleen Transcriptome in Rock Bream (Oplegnathus fasciatus) Naturally Infected with Rock Bream Iridovirus (RBIV)
journal, March 2020

  • Kim, Ahran; Yoon, Dahye; Lim, Yunjin
  • International Journal of Molecular Sciences, Vol. 21, Issue 5
  • DOI: 10.3390/ijms21051707

Analyses of alternative polyadenylation: from old school biochemistry to high-throughput technologies
journal, April 2017


Uncovering full-length transcript isoforms of sugarcane cultivar Khon Kaen 3 using single-molecule long-read sequencing
journal, October 2018

  • Piriyapongsa, Jittima; Kaewprommal, Pavita; Vaiwsri, Sirintra
  • PeerJ, Vol. 6
  • DOI: 10.7717/peerj.5818