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 »
- Authors:
- Publication Date:
- Research Org.:
- Oregon State Univ., Corvallis, OR (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- 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. https://doi.org/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. https://doi.org/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 = {Mon Feb 12 00:00:00 EST 2018},
month = {Mon Feb 12 00:00:00 EST 2018}
}
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https://doi.org/10.3389/fpls.2018.00005
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Works referenced in this record:
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
SpliceGrapher: detecting patterns of alternative splicing from RNA-Seq data in the context of gene models and EST data
journal, January 2012
- Rogers, Mark F.; Thomas, Julie; Reddy, Anireddy SN
- Genome Biology, Vol. 13, Issue 1
Role of DREBs in regulation of abiotic stress responses in plants
journal, July 2011
- Lata, C.; Prasad, M.
- Journal of Experimental Botany, Vol. 62, Issue 14
Interactome analysis reveals versatile functions of Arabidopsis COLD SHOCK DOMAIN PROTEIN 3 in RNA processing within the nucleus and cytoplasm
journal, January 2013
- Kim, Myung-Hee; Sonoda, Yutaka; Sasaki, Kentaro
- Cell Stress and Chaperones, Vol. 18, Issue 4
Extensive coupling of alternative splicing of pre-mRNAs of serine/arginine (SR) genes with nonsense-mediated decay: Rapid reports
journal, October 2009
- Palusa, Saiprasad G.; Reddy, Anireddy S. N.
- New Phytologist, Vol. 185, Issue 1
Identification and characterization of novel factors that act in the nonsense‐mediated mRNA decay pathway in nematodes, flies and mammals
journal, November 2014
- Casadio, Angela; Longman, Dasa; Hug, Nele
- EMBO reports, Vol. 16, Issue 1
Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses: Stress regulation of alternative splicing of SR genes
journal, February 2007
- Palusa, Saiprasad Goud; Ali, Gul Shad; Reddy, Anireddy S. N.
- The Plant Journal, Vol. 49, Issue 6
Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis
journal, November 2011
- Kalyna, Maria; Simpson, Craig G.; Syed, Naeem H.
- Nucleic Acids Research, Vol. 40, Issue 6
LoRDEC: accurate and efficient long read error correction
journal, August 2014
- Salmela, Leena; Rivals, Eric
- Bioinformatics, Vol. 30, Issue 24
STAR: ultrafast universal RNA-seq aligner
journal, October 2012
- Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix
- Bioinformatics, Vol. 29, Issue 1
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
Patatin-Related Phospholipase pPLAIIIβ-Induced Changes in Lipid Metabolism Alter Cellulose Content and Cell Elongation in Arabidopsis
journal, March 2011
- Li, Maoyin; Bahn, Sung Chul; Guo, Liang
- The Plant Cell, Vol. 23, Issue 3
Nonsense-mediated mRNA decay in mammals
journal, May 2005
- Maquat, L. E.
- Journal of Cell Science, Vol. 118, Issue 9
Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis
journal, January 2014
- Ding, Feng; Cui, Peng; Wang, Zhenyu
- BMC Genomics, Vol. 15, Issue 1
High-Resolution Expression Map of the Arabidopsis Root Reveals Alternative Splicing and lincRNA Regulation
journal, November 2016
- Li, Song; Yamada, Masashi; Han, Xinwei
- Developmental Cell, Vol. 39, Issue 4
A survey of the sorghum transcriptome using single-molecule long reads
journal, June 2016
- Abdel-Ghany, Salah E.; Hamilton, Michael; Jacobi, Jennifer L.
- Nature Communications, Vol. 7, Issue 1
Removal of Retained Introns Regulates Translation in the Rapidly Developing Gametophyte of Marsilea vestita
journal, March 2013
- Boothby, Thomas C.; Zipper, Richard S.; van der Weele, Corine M.
- Developmental Cell, Vol. 24, Issue 5
Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements
journal, March 2007
- Lareau, Liana F.; Inada, Maki; Green, Richard E.
- Nature, Vol. 446, Issue 7138
Widespread intron retention in mammals functionally tunes transcriptomes
journal, September 2014
- Braunschweig, Ulrich; Barbosa-Morais, Nuno L.; Pan, Qun
- Genome Research, Vol. 24, Issue 11
Integrating Omics and Alternative Splicing Reveals Insights into Grape Response to High Temperature
journal, January 2017
- Jiang, Jianfu; Liu, Xinna; Liu, Chonghuai
- Plant Physiology, Vol. 173, Issue 2
Genome-Wide Identification, Classification, and Expression Analysis of 14-3-3 Gene Family in Populus
journal, April 2015
- Tian, Fengxia; Wang, Tan; Xie, Yuli
- PLOS ONE, Vol. 10, Issue 4
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
Phytozome: a comparative platform for green plant genomics
journal, November 2011
- Goodstein, David M.; Shu, Shengqiang; Howson, Russell
- Nucleic Acids Research, Vol. 40, Issue D1
Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice
journal, January 2012
- Todaka, Daisuke; Nakashima, Kazuo; Shinozaki, Kazuo
- Rice, Vol. 5, Issue 1
A Comprehensive Analysis of Alternative Splicing in Paleopolyploid Maize
journal, May 2017
- Mei, Wenbin; Liu, Sanzhen; Schnable, James C.
- Frontiers in Plant Science, Vol. 8
Transcriptome-Wide Identification of RNA Targets of Arabidopsis SERINE/ARGININE-RICH45 Uncovers the Unexpected Roles of This RNA Binding Protein in RNA Processing
journal, November 2015
- Xing, Denghui; Wang, Yajun; Hamilton, Michael
- The Plant Cell, Vol. 27, Issue 12
Transcriptional Regulatory Networks in Response to Abiotic Stresses in Arabidopsis and Grasses: Figure 1.
journal, January 2009
- Nakashima, Kazuo; Ito, Yusuke; Yamaguchi-Shinozaki, Kazuko
- Plant Physiology, Vol. 149, Issue 1
Conservation and functional influence of alternative splicing in wood formation of Populus and Eucalyptus
journal, January 2014
- Xu, Peng; Kong, Yimeng; Song, Dongliang
- BMC Genomics, Vol. 15, Issue 1
Masked mRNA is stored with aggregated nuclear speckles and its asymmetric redistribution requires a homolog of mago nashi
journal, October 2011
- Boothby, Thomas C.; Wolniak, Stephen M.
- BMC Cell Biology, Vol. 12, Issue 1
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
Unproductive alternative splicing and nonsense mRNAs: A widespread phenomenon among plant circadian clock genes
journal, January 2012
- Filichkin, Sergei A.; Mockler, Todd C.
- Biology Direct, Vol. 7, Issue 1
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Imaging of Endogenous Messenger RNA Splice Variants in Living Cells Reveals Nuclear Retention of Transcripts Inaccessible to Nonsense-Mediated Decay in Arabidopsis
journal, February 2014
- Göhring, Janett; Jacak, Jaroslaw; Barta, Andrea
- The Plant Cell, Vol. 26, Issue 2
The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors
journal, June 2008
- Huang, Daiqing; Wu, Weiren; Abrams, Suzanne R.
- Journal of Experimental Botany, Vol. 59, Issue 11
Genes That Are Uniquely Stress Regulated in Salt Overly Sensitive ( sos ) Mutants
journal, May 2001
- Gong, Zhizhong; Koiwa, Hisashi; Cushman, Mary Ann
- Plant Physiology, Vol. 126, Issue 1
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
Introns of plant pri-miRNAs enhance miRNA biogenesis
journal, May 2013
- Bielewicz, Dawid; Kalak, Malgorzata; Kalyna, Maria
- EMBO reports, Vol. 14, Issue 7
Full and partial genome-wide assembly and disassembly of the yeast transcription machinery in response to heat shock
journal, August 2006
- Zanton, S. J.
- Genes & Development, Vol. 20, Issue 16
Lost in Translation: Pitfalls in Deciphering Plant Alternative Splicing Transcripts
journal, August 2015
- Brown, John W. S.; Simpson, Craig G.; Marquez, Yamile
- The Plant Cell, Vol. 27, Issue 8
Environmental Stresses Modulate Abundance and Timing of Alternatively Spliced Circadian Transcripts in Arabidopsis
journal, February 2015
- Filichkin, Sergei A.; Cumbie, Jason S.; Dharmawardhana, Palitha
- Molecular Plant, Vol. 8, Issue 2
Evolutionarily Conserved Alternative Splicing Across Monocots
journal, August 2017
- Mei, Wenbin; Boatwright, Lucas; Feng, Guanqiao
- Genetics
A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype
journal, January 2014
- Vitulo, Nicola; Forcato, Claudio; Carpinelli, Elisa
- BMC Plant Biology, Vol. 14, Issue 1
Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans
journal, December 2002
- Lewis, B. P.; Green, R. E.; Brenner, S. E.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 1
Global Dissection of Alternative Splicing in Paleopolyploid Soybean
journal, March 2014
- Shen, Yanting; Zhou, Zhengkui; Wang, Zheng
- The Plant Cell, Vol. 26, Issue 3
The developing xylem transcriptome and genome-wide analysis of alternative splicing in Populus trichocarpa (black cottonwood) populations
journal, January 2013
- Bao, Hua; Li, Eryang; Mansfield, Shawn D.
- BMC Genomics, Vol. 14, Issue 1
Organizing Principles of Mammalian Nonsense-Mediated mRNA Decay
journal, November 2013
- Popp, Maximilian Wei-Lin; Maquat, Lynne E.
- Annual Review of Genetics, Vol. 47, Issue 1
Genome-wide analyses of alternative splicing in plants: Opportunities and challenges
journal, July 2008
- Barbazuk, W. B.; Fu, Y.; McGinnis, K. M.
- Genome Research, Vol. 18, Issue 9
Alternative Splicing at the Intersection of Biological Timing, Development, and Stress Responses
journal, October 2013
- Staiger, Dorothee; Brown, John W. S.
- The Plant Cell, Vol. 25, Issue 10
Comparative physiology of allopatric Populus species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens
journal, July 2015
- Soolanayakanahally, Raju Y.; Guy, Robert D.; Street, Nathaniel R.
- Frontiers in Plant Science, Vol. 6
Intron-Mediated Alternative Splicing of WOOD-ASSOCIATED NAC TRANSCRIPTION FACTOR1B Regulates Cell Wall Thickening during Fiber Development in Populus Species
journal, January 2014
- Zhao, Yunjun; Sun, Jiayan; Xu, Peng
- Plant Physiology, Vol. 164, Issue 2
Gene structures and processing of Arabidopsis thaliana HYL1-dependent pri-miRNAs
journal, March 2009
- Szarzynska, Bogna; Sobkowiak, Lukasz; Pant, Bikram Datt
- Nucleic Acids Research, Vol. 37, Issue 9
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
Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses: Plant SR-rich proteins
journal, July 2011
- Reddy, Anireddy S. N.; Shad Ali, Gul
- Wiley Interdisciplinary Reviews: RNA, Vol. 2, Issue 6
Widespread intron retention diversifies most cancer transcriptomes
journal, May 2015
- Dvinge, Heidi; Bradley, Robert K.
- Genome Medicine, Vol. 7, Issue 1
Intron retention is a widespread mechanism of tumor-suppressor inactivation
journal, October 2015
- Jung, Hyunchul; Lee, Donghoon; Lee, Jongkeun
- Nature Genetics, Vol. 47, Issue 11
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
Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress
journal, April 2015
- Filichkin, Sergei; Priest, Henry D.; Megraw, Molly
- Current Opinion in Plant Biology, Vol. 24
Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation
journal, May 2012
- Kesari, R.; Lasky, J. R.; Villamor, J. G.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 23
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
- Zhao, Liangzhen; Zhang, Hangxiao; Kohnen, Markus V.
- Frontiers in Genetics, Vol. 10
Alternative Splicing and Protein Diversity: Plants Versus Animals
journal, June 2019
- Chaudhary, Saurabh; Khokhar, Waqas; Jabre, Ibtissam
- Frontiers in Plant Science, Vol. 10
Populus trichocarpa clade A PP2C protein phosphatases: their stress-induced expression patterns, interactions in core abscisic acid signaling, and potential for regulation of growth and development
journal, April 2019
- Rigoulot, Stephen B.; Petzold, H. Earl; Williams, Sarah P.
- Plant Molecular Biology, Vol. 100, Issue 3
Molecular bases of responses to abiotic stress in trees
journal, November 2019
- Estravis-Barcala, Maximiliano; Mattera, María Gabriela; Soliani, Carolina
- Journal of Experimental Botany, Vol. 71, Issue 13
Does co-transcriptional regulation of alternative splicing mediate plant stress responses?
journal, February 2019
- Jabre, Ibtissam; Reddy, Anireddy S. N.; Kalyna, Maria
- Nucleic Acids Research, Vol. 47, Issue 6
Recent advances in the characterization of plant transcriptomes in response to drought, salinity, heat, and cold stress
journal, January 2019
- Bashir, Khurram; Matsui, Akihiro; Rasheed, Sultana
- F1000Research, Vol. 8
Cold Hardiness in Trees: A Mini-Review
journal, September 2018
- Wisniewski, Michael; Nassuth, Annette; Arora, Rajeev
- Frontiers in Plant Science, Vol. 9
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