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Title: Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching

Abstract

Abiotic stresses affect plant physiology, development, growth, and alter pre-mRNA splicing. Western poplar is a model woody tree and a potential bioenergy feedstock. To investigate the extent of stress-regulated alternative splicing (AS), we conducted an in-depth survey of leaf, root, and stem xylem transcriptomes under drought, salt, or temperature stress. Analysis of approximately one billion of genome-aligned RNA-Seq reads from tissue- or stress-specific libraries revealed over fifteen millions of novel splice junctions. Transcript models supported by both RNA-Seq and single molecule isoform sequencing (Iso-Seq) data revealed a broad array of novel stress- and/or tissue-specific isoforms. Analysis of Iso-Seq data also resulted in the discovery of 15,087 novel transcribed regions of which 164 show AS. Our findings demonstrate that abiotic stresses profoundly perturb transcript isoform profiles and trigger widespread intron retention (IR) events. Stress treatments often increased or decreased retention of specific introns – a phenomenon described here as differential intron retention (DIR). Many differentially retained introns were regulated in a stress- and/or tissue-specific manner. A subset of transcripts harboring super stress-responsive DIR events showed persisting fluctuations in the degree of IR across all treatments and tissue types. To investigate coordinated dynamics of intron-containing transcripts in the study we quantified absolutemore » copy number of isoforms of two conserved transcription factors (TFs) using Droplet Digital PCR. This case study suggests that stress treatments can be associated with coordinated switches in relative ratios between fully spliced and intron-retaining isoforms and may play a role in adjusting transcriptome to abiotic stresses.« less

Authors:
; ; ; ; ; ; ;
Publication Date:
Research Org.:
Oregon State Univ., Corvallis, OR (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1437195
Alternate Identifier(s):
OSTI ID: 1510777
Grant/Contract Number:  
SC0008570
Resource Type:
Published Article
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Name: Frontiers in Plant Science Journal Volume: 9; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Media SA
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; western poplar; transcriptome; alternative splicing; abiotic stress; isoform switching; differential intron retention; stress adaptation

Citation Formats

Filichkin, Sergei A., Hamilton, Michael, Dharmawardhana, Palitha D., Singh, Sunil K., Sullivan, Christopher, Ben-Hur, Asa, Reddy, Anireddy S. N., and Jaiswal, Pankaj. Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching. Switzerland: N. p., 2018. Web. doi:10.3389/fpls.2018.00005.
Filichkin, Sergei A., Hamilton, Michael, Dharmawardhana, Palitha D., Singh, Sunil K., Sullivan, Christopher, Ben-Hur, Asa, Reddy, Anireddy S. N., & Jaiswal, Pankaj. Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching. Switzerland. doi:10.3389/fpls.2018.00005.
Filichkin, Sergei A., Hamilton, Michael, Dharmawardhana, Palitha D., Singh, Sunil K., Sullivan, Christopher, Ben-Hur, Asa, Reddy, Anireddy S. N., and Jaiswal, Pankaj. Mon . "Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching". Switzerland. doi:10.3389/fpls.2018.00005.
@article{osti_1437195,
title = {Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching},
author = {Filichkin, Sergei A. and Hamilton, Michael and Dharmawardhana, Palitha D. and Singh, Sunil K. and Sullivan, Christopher and Ben-Hur, Asa and Reddy, Anireddy S. N. and Jaiswal, Pankaj},
abstractNote = {Abiotic stresses affect plant physiology, development, growth, and alter pre-mRNA splicing. Western poplar is a model woody tree and a potential bioenergy feedstock. To investigate the extent of stress-regulated alternative splicing (AS), we conducted an in-depth survey of leaf, root, and stem xylem transcriptomes under drought, salt, or temperature stress. Analysis of approximately one billion of genome-aligned RNA-Seq reads from tissue- or stress-specific libraries revealed over fifteen millions of novel splice junctions. Transcript models supported by both RNA-Seq and single molecule isoform sequencing (Iso-Seq) data revealed a broad array of novel stress- and/or tissue-specific isoforms. Analysis of Iso-Seq data also resulted in the discovery of 15,087 novel transcribed regions of which 164 show AS. Our findings demonstrate that abiotic stresses profoundly perturb transcript isoform profiles and trigger widespread intron retention (IR) events. Stress treatments often increased or decreased retention of specific introns – a phenomenon described here as differential intron retention (DIR). Many differentially retained introns were regulated in a stress- and/or tissue-specific manner. A subset of transcripts harboring super stress-responsive DIR events showed persisting fluctuations in the degree of IR across all treatments and tissue types. To investigate coordinated dynamics of intron-containing transcripts in the study we quantified absolute copy number of isoforms of two conserved transcription factors (TFs) using Droplet Digital PCR. This case study suggests that stress treatments can be associated with coordinated switches in relative ratios between fully spliced and intron-retaining isoforms and may play a role in adjusting transcriptome to abiotic stresses.},
doi = {10.3389/fpls.2018.00005},
journal = {Frontiers in Plant Science},
number = ,
volume = 9,
place = {Switzerland},
year = {2018},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.3389/fpls.2018.00005

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Cited by: 6 works
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    Works referencing / citing this record:

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


    Alternative Splicing and Protein Diversity: Plants Versus Animals
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