Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome

Cristiane P. G. Calixto, Wenbin Guo, Allan B James, Nikoleta A. Tzioutziou, Juan C. Entizne, Paige E. Panter, Heather Knight, Hugh Nimmo, Runxuan Zhang, John W. S. Brown

Research output: Contribution to journalArticle

17 Citations (Scopus)
59 Downloads (Pure)

Abstract

Plants have adapted to tolerate and survive constantly changing environmental conditions by re-programming gene expression. The dynamics of the contribution of alternative splicing (AS) to stress responses are unknown. RNA-sequencing of a time-series of Arabidopsis thaliana plants exposed to cold determines the timing of significant AS changes. This shows a massive and rapid AS response with coincident waves of transcriptional and AS activity occurring in the first few hours of temperature reduction, and further AS throughout the cold. In particular, hundreds of genes showed changes in expression due to rapidly occurring AS in response to cold ("early AS" genes); these included numerous novel cold-responsive transcription factors and splicing factors/RNA-binding proteins regulated only by AS. The speed and sensitivity to small temperature changes of AS of some of these genes suggest that fine-tuning expression via AS pathways contributes to the thermo-plasticity of expression. Four "early AS" splicing regulatory genes have been shown previously to be required for freezing tolerance and acclimation; we provide evidence of a fifth gene, U2B"-LIKE. Such factors likely drive cascades of AS of downstream genes which alongside transcription modulate transcriptome reprogramming that together govern the physiological and survival responses of plants to low temperature.

Original languageEnglish
Pages (from-to)1424-1444
Number of pages21
JournalPlant Cell
Volume30
Issue number7
Early online date15 May 2018
DOIs
Publication statusPublished - 1 Jul 2018

Fingerprint

alternative splicing
Alternative Splicing
Transcriptome
Arabidopsis
transcriptome
Genes
genes
Temperature
RNA Sequence Analysis
temperature
RNA-binding proteins
RNA-Binding Proteins
Acclimatization
Regulator Genes
regulator genes
cold tolerance
Freezing
plant response
time series analysis
stress response

Cite this

Calixto, Cristiane P. G. ; Guo, Wenbin ; James, Allan B ; Tzioutziou, Nikoleta A. ; Entizne, Juan C. ; Panter, Paige E. ; Knight, Heather ; Nimmo, Hugh ; Zhang, Runxuan ; Brown, John W. S. / Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome. In: Plant Cell. 2018 ; Vol. 30, No. 7. pp. 1424-1444.
@article{42fe8d99cfc143a68d888743dfff22e1,
title = "Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome",
abstract = "Plants have adapted to tolerate and survive constantly changing environmental conditions by re-programming gene expression. The dynamics of the contribution of alternative splicing (AS) to stress responses are unknown. RNA-sequencing of a time-series of Arabidopsis thaliana plants exposed to cold determines the timing of significant AS changes. This shows a massive and rapid AS response with coincident waves of transcriptional and AS activity occurring in the first few hours of temperature reduction, and further AS throughout the cold. In particular, hundreds of genes showed changes in expression due to rapidly occurring AS in response to cold ({"}early AS{"} genes); these included numerous novel cold-responsive transcription factors and splicing factors/RNA-binding proteins regulated only by AS. The speed and sensitivity to small temperature changes of AS of some of these genes suggest that fine-tuning expression via AS pathways contributes to the thermo-plasticity of expression. Four {"}early AS{"} splicing regulatory genes have been shown previously to be required for freezing tolerance and acclimation; we provide evidence of a fifth gene, U2B{"}-LIKE. Such factors likely drive cascades of AS of downstream genes which alongside transcription modulate transcriptome reprogramming that together govern the physiological and survival responses of plants to low temperature.",
author = "Calixto, {Cristiane P. G.} and Wenbin Guo and James, {Allan B} and Tzioutziou, {Nikoleta A.} and Entizne, {Juan C.} and Panter, {Paige E.} and Heather Knight and Hugh Nimmo and Runxuan Zhang and Brown, {John W. S.}",
note = "Funding: BBSRC (BB/K006568/1; BB/P009751/1; BB/N022807/1), Scottish Government Rural and Environment Science and Analytical Services Division (RESAS).",
year = "2018",
month = "7",
day = "1",
doi = "10.1105/tpc.18.00177",
language = "English",
volume = "30",
pages = "1424--1444",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "7",

}

Calixto, CPG, Guo, W, James, AB, Tzioutziou, NA, Entizne, JC, Panter, PE, Knight, H, Nimmo, H, Zhang, R & Brown, JWS 2018, 'Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome', Plant Cell, vol. 30, no. 7, pp. 1424-1444. https://doi.org/10.1105/tpc.18.00177

Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome. / Calixto, Cristiane P. G.; Guo, Wenbin; James, Allan B; Tzioutziou, Nikoleta A.; Entizne, Juan C.; Panter, Paige E.; Knight, Heather; Nimmo, Hugh; Zhang, Runxuan; Brown, John W. S.

In: Plant Cell, Vol. 30, No. 7, 01.07.2018, p. 1424-1444.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome

AU - Calixto, Cristiane P. G.

AU - Guo, Wenbin

AU - James, Allan B

AU - Tzioutziou, Nikoleta A.

AU - Entizne, Juan C.

AU - Panter, Paige E.

AU - Knight, Heather

AU - Nimmo, Hugh

AU - Zhang, Runxuan

AU - Brown, John W. S.

N1 - Funding: BBSRC (BB/K006568/1; BB/P009751/1; BB/N022807/1), Scottish Government Rural and Environment Science and Analytical Services Division (RESAS).

PY - 2018/7/1

Y1 - 2018/7/1

N2 - Plants have adapted to tolerate and survive constantly changing environmental conditions by re-programming gene expression. The dynamics of the contribution of alternative splicing (AS) to stress responses are unknown. RNA-sequencing of a time-series of Arabidopsis thaliana plants exposed to cold determines the timing of significant AS changes. This shows a massive and rapid AS response with coincident waves of transcriptional and AS activity occurring in the first few hours of temperature reduction, and further AS throughout the cold. In particular, hundreds of genes showed changes in expression due to rapidly occurring AS in response to cold ("early AS" genes); these included numerous novel cold-responsive transcription factors and splicing factors/RNA-binding proteins regulated only by AS. The speed and sensitivity to small temperature changes of AS of some of these genes suggest that fine-tuning expression via AS pathways contributes to the thermo-plasticity of expression. Four "early AS" splicing regulatory genes have been shown previously to be required for freezing tolerance and acclimation; we provide evidence of a fifth gene, U2B"-LIKE. Such factors likely drive cascades of AS of downstream genes which alongside transcription modulate transcriptome reprogramming that together govern the physiological and survival responses of plants to low temperature.

AB - Plants have adapted to tolerate and survive constantly changing environmental conditions by re-programming gene expression. The dynamics of the contribution of alternative splicing (AS) to stress responses are unknown. RNA-sequencing of a time-series of Arabidopsis thaliana plants exposed to cold determines the timing of significant AS changes. This shows a massive and rapid AS response with coincident waves of transcriptional and AS activity occurring in the first few hours of temperature reduction, and further AS throughout the cold. In particular, hundreds of genes showed changes in expression due to rapidly occurring AS in response to cold ("early AS" genes); these included numerous novel cold-responsive transcription factors and splicing factors/RNA-binding proteins regulated only by AS. The speed and sensitivity to small temperature changes of AS of some of these genes suggest that fine-tuning expression via AS pathways contributes to the thermo-plasticity of expression. Four "early AS" splicing regulatory genes have been shown previously to be required for freezing tolerance and acclimation; we provide evidence of a fifth gene, U2B"-LIKE. Such factors likely drive cascades of AS of downstream genes which alongside transcription modulate transcriptome reprogramming that together govern the physiological and survival responses of plants to low temperature.

U2 - 10.1105/tpc.18.00177

DO - 10.1105/tpc.18.00177

M3 - Article

VL - 30

SP - 1424

EP - 1444

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 7

ER -