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Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome

View ORCID ProfileCristiane P. G. Calixto, Wenbin Guo, Allan B. James, Nikoleta A. Tzioutziou, Juan Carlos Entizne, Paige E. Panter, Heather Knight, Hugh G. Nimmo, Runxuan Zhang, John W. S. Brown
doi: https://doi.org/10.1101/251876
Cristiane P. G. Calixto
1Plant Sciences Division, School of Life Sciences, University of Dundee, Invergowrie, Dundee, Scotland, UK.
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  • ORCID record for Cristiane P. G. Calixto
Wenbin Guo
1Plant Sciences Division, School of Life Sciences, University of Dundee, Invergowrie, Dundee, Scotland, UK.
2Information and Computational Sciences, The James Hutton Institute, Invergowrie, Dundee, Scotland, UK.
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Allan B. James
3Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland.
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Nikoleta A. Tzioutziou
1Plant Sciences Division, School of Life Sciences, University of Dundee, Invergowrie, Dundee, Scotland, UK.
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Juan Carlos Entizne
1Plant Sciences Division, School of Life Sciences, University of Dundee, Invergowrie, Dundee, Scotland, UK.
4Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, Dundee, Scotland, UK.
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Paige E. Panter
5Department of Biosciences, Durham University, Durham DH1 3LE, UK.
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Heather Knight
5Department of Biosciences, Durham University, Durham DH1 3LE, UK.
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Hugh G. Nimmo
3Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland.
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  • For correspondence: j.w.s.brown@dundee.ac.uk hugh.nimmo@glasgow.ac.uk runxuan.zhang@hutton.ac.uk
Runxuan Zhang
2Information and Computational Sciences, The James Hutton Institute, Invergowrie, Dundee, Scotland, UK.
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  • For correspondence: j.w.s.brown@dundee.ac.uk hugh.nimmo@glasgow.ac.uk runxuan.zhang@hutton.ac.uk
John W. S. Brown
1Plant Sciences Division, School of Life Sciences, University of Dundee, Invergowrie, Dundee, Scotland, UK.
4Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, Dundee, Scotland, UK.
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  • For correspondence: j.w.s.brown@dundee.ac.uk hugh.nimmo@glasgow.ac.uk runxuan.zhang@hutton.ac.uk
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Abstract

Background Plants have adapted to tolerate and survive constantly changing environmental conditions by re-programming gene expression. The scale of the contribution of alternative splicing (AS) to stress responses has been underestimated due to limitations in RNA-seq analysis programs and poor representation of AS transcripts in plant databases. Significantly, the dynamics of the AS response have not been investigated but this is now possible with accurate transcript quantification programs and AtRTD2, a new, comprehensive transcriptome for Arabidopsis.

Results Using ultra-deep RNA-sequencing of a time-course of Arabidopsis thaliana plants exposed to cold treatment, we identified 8,949 genes with altered expression of which 2,442 showed significant differential alternative splicing (DAS) and 1,647 genes were regulated only at the level of AS (DAS-only). The high temporal resolution demonstrated the rapid induction of both transcription and AS resulting in coincident waves of differential expression (transcription) and differential alternative splicing in the first 6-9 hours of cold. The differentially expressed and DAS gene sets were largely non-overlapping, each comprising thousands of genes. The dynamic analysis of AS identified genes with rapid and sensitive AS within 3 h of transfer to the cold (early AS genes), which were enriched for splicing and transcription factors. A detailed investigation of the novel cold-response DAS-only gene, U2B”-LIKE, suggested that it regulates AS and is required for tolerance to freezing.

Conclusions Our data indicate that transcription and AS are the major regulators of transcriptome reprogramming that together govern the physiological and survival responses of plants to low temperature.

Footnotes

  • ↵† Equal contributors.

  • CPGC c.p.g.calixto{at}dundee.ac.uk, WG wenbin.guo{at}hutton.ac.uk, ABJ Allan.James{at}glasgow.ac.uk, NAT nikoleta.tzioutziou{at}hutton.ac.uk, JCE Juan.Carlos.Entizne{at}hutton.ac.uk, PEP p.e.panter{at}durham.ac.uk, HK p.h.knight{at}durham.ac.uk, HGN Hugh.nimmo{at}glasgow.ac.uk, RZ Runxuan.Zhang{at}hutton.ac.uk, JWSB j.w.s.brown{at}dundee.ac.uk.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 22, 2018.
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Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome
Cristiane P. G. Calixto, Wenbin Guo, Allan B. James, Nikoleta A. Tzioutziou, Juan Carlos Entizne, Paige E. Panter, Heather Knight, Hugh G. Nimmo, Runxuan Zhang, John W. S. Brown
bioRxiv 251876; doi: https://doi.org/10.1101/251876
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Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome
Cristiane P. G. Calixto, Wenbin Guo, Allan B. James, Nikoleta A. Tzioutziou, Juan Carlos Entizne, Paige E. Panter, Heather Knight, Hugh G. Nimmo, Runxuan Zhang, John W. S. Brown
bioRxiv 251876; doi: https://doi.org/10.1101/251876

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