Cold-Dependent Expression and Alternative Splicing of Arabidopsis Long Non-coding RNAs

Cristiane Calixto, Nikoleta Tzioutziou, Allan B. James, Csaba Hornyik, Wenbin Guo, Runxuan Zhang, Hugh G. Nimmo, John Brown (Lead / Corresponding author)

Research output: Contribution to journalArticle

23 Downloads (Pure)

Abstract

Plants re-program their gene expression when responding to changing environmental conditions. Besides differential gene expression, extensive alternative splicing (AS) of pre-mRNAs and changes in expression of long non-coding RNAs (lncRNAs) are associated with stress responses. RNA-sequencing of a diel time-series of the initial response of Arabidopsis thaliana rosettes to low temperature showed massive and rapid waves of both transcriptional and AS activity in protein-coding genes. We exploited the high diversity of transcript isoforms in AtRTD2 to examine regulation and post-transcriptional regulation of lncRNA gene expression in response to cold stress. We identified 135 lncRNA genes with cold-dependent differential expression (DE) and/or differential alternative splicing (DAS) of lncRNAs including natural antisense RNAs, sORF lncRNAs, and precursors of microRNAs (miRNAs) and trans-acting small-interfering RNAs (tasiRNAs). The high resolution (HR) of the time-series allowed the dynamics of changes in transcription and AS to be determined and identified early and adaptive transcriptional and AS changes in the cold response. Some lncRNA genes were regulated only at the level of AS and using plants grown at different temperatures and a HR time-course of the first 3 h of temperature reduction, we demonstrated that the AS of some lncRNAs is highly sensitive to small temperature changes suggesting tight regulation of expression. In particular, a splicing event in TAS1a which removed an intron that contained the miR173 processing and phased siRNAs generation sites was differentially alternatively spliced in response to cold. The cold-induced reduction of the spliced form of TAS1a and of the tasiRNAs suggests that splicing may enhance production of the siRNAs. Our results identify candidate lncRNAs that may contribute to the regulation of expression that determines the physiological processes essential for acclimation and freezing tolerance.

Original languageEnglish
Article number235
Pages (from-to)1-16
Number of pages16
JournalFrontiers in Plant Science
Volume10
DOIs
Publication statusPublished - 28 Feb 2019

Fingerprint

alternative splicing
Arabidopsis
small interfering RNA
time series analysis
temperature
RNA splicing
antisense RNA
gene expression
genes
non-coding RNA
gene expression regulation
cold stress
microRNA
cold tolerance
introns
stress response
acclimation
sequence analysis
Arabidopsis thaliana
transcription (genetics)

Keywords

  • Long non-coding RNA
  • Primary microRNA
  • Alternative splicing
  • Diel time-course
  • High-resolution RNA-seq
  • Cold transcriptome

Cite this

Calixto, Cristiane ; Tzioutziou, Nikoleta ; James, Allan B. ; Hornyik, Csaba ; Guo, Wenbin ; Zhang, Runxuan ; Nimmo, Hugh G. ; Brown, John. / Cold-Dependent Expression and Alternative Splicing of Arabidopsis Long Non-coding RNAs. In: Frontiers in Plant Science. 2019 ; Vol. 10. pp. 1-16.
@article{829c77b5336a4090b87a198eb777a968,
title = "Cold-Dependent Expression and Alternative Splicing of Arabidopsis Long Non-coding RNAs",
abstract = "Plants re-program their gene expression when responding to changing environmental conditions. Besides differential gene expression, extensive alternative splicing (AS) of pre-mRNAs and changes in expression of long non-coding RNAs (lncRNAs) are associated with stress responses. RNA-sequencing of a diel time-series of the initial response of Arabidopsis thaliana rosettes to low temperature showed massive and rapid waves of both transcriptional and AS activity in protein-coding genes. We exploited the high diversity of transcript isoforms in AtRTD2 to examine regulation and post-transcriptional regulation of lncRNA gene expression in response to cold stress. We identified 135 lncRNA genes with cold-dependent differential expression (DE) and/or differential alternative splicing (DAS) of lncRNAs including natural antisense RNAs, sORF lncRNAs, and precursors of microRNAs (miRNAs) and trans-acting small-interfering RNAs (tasiRNAs). The high resolution (HR) of the time-series allowed the dynamics of changes in transcription and AS to be determined and identified early and adaptive transcriptional and AS changes in the cold response. Some lncRNA genes were regulated only at the level of AS and using plants grown at different temperatures and a HR time-course of the first 3 h of temperature reduction, we demonstrated that the AS of some lncRNAs is highly sensitive to small temperature changes suggesting tight regulation of expression. In particular, a splicing event in TAS1a which removed an intron that contained the miR173 processing and phased siRNAs generation sites was differentially alternatively spliced in response to cold. The cold-induced reduction of the spliced form of TAS1a and of the tasiRNAs suggests that splicing may enhance production of the siRNAs. Our results identify candidate lncRNAs that may contribute to the regulation of expression that determines the physiological processes essential for acclimation and freezing tolerance.",
keywords = "Long non-coding RNA, Primary microRNA, Alternative splicing, Diel time-course, High-resolution RNA-seq, Cold transcriptome",
author = "Cristiane Calixto and Nikoleta Tzioutziou and James, {Allan B.} and Csaba Hornyik and Wenbin Guo and Runxuan Zhang and Nimmo, {Hugh G.} and John Brown",
note = "This work was supported by funding from the Biotechnology and Biological Sciences Research Council (BBSRC) (BB/K006568/1, BB/P009751/1, BB/N022807/1 to JB; BB/K006835/1 to HN) and the Scottish Government Rural and Environment Science and Analytical Services division (RESAS) (to JB and RZ).",
year = "2019",
month = "2",
day = "28",
doi = "10.3389/fpls.2019.00235",
language = "English",
volume = "10",
pages = "1--16",
journal = "Frontiers in Plant Science",
issn = "1664-462X",
publisher = "Frontiers Media",

}

Cold-Dependent Expression and Alternative Splicing of Arabidopsis Long Non-coding RNAs. / Calixto, Cristiane; Tzioutziou, Nikoleta; James, Allan B.; Hornyik, Csaba; Guo, Wenbin; Zhang, Runxuan; Nimmo, Hugh G.; Brown, John (Lead / Corresponding author).

In: Frontiers in Plant Science, Vol. 10, 235, 28.02.2019, p. 1-16.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Cold-Dependent Expression and Alternative Splicing of Arabidopsis Long Non-coding RNAs

AU - Calixto, Cristiane

AU - Tzioutziou, Nikoleta

AU - James, Allan B.

AU - Hornyik, Csaba

AU - Guo, Wenbin

AU - Zhang, Runxuan

AU - Nimmo, Hugh G.

AU - Brown, John

N1 - This work was supported by funding from the Biotechnology and Biological Sciences Research Council (BBSRC) (BB/K006568/1, BB/P009751/1, BB/N022807/1 to JB; BB/K006835/1 to HN) and the Scottish Government Rural and Environment Science and Analytical Services division (RESAS) (to JB and RZ).

PY - 2019/2/28

Y1 - 2019/2/28

N2 - Plants re-program their gene expression when responding to changing environmental conditions. Besides differential gene expression, extensive alternative splicing (AS) of pre-mRNAs and changes in expression of long non-coding RNAs (lncRNAs) are associated with stress responses. RNA-sequencing of a diel time-series of the initial response of Arabidopsis thaliana rosettes to low temperature showed massive and rapid waves of both transcriptional and AS activity in protein-coding genes. We exploited the high diversity of transcript isoforms in AtRTD2 to examine regulation and post-transcriptional regulation of lncRNA gene expression in response to cold stress. We identified 135 lncRNA genes with cold-dependent differential expression (DE) and/or differential alternative splicing (DAS) of lncRNAs including natural antisense RNAs, sORF lncRNAs, and precursors of microRNAs (miRNAs) and trans-acting small-interfering RNAs (tasiRNAs). The high resolution (HR) of the time-series allowed the dynamics of changes in transcription and AS to be determined and identified early and adaptive transcriptional and AS changes in the cold response. Some lncRNA genes were regulated only at the level of AS and using plants grown at different temperatures and a HR time-course of the first 3 h of temperature reduction, we demonstrated that the AS of some lncRNAs is highly sensitive to small temperature changes suggesting tight regulation of expression. In particular, a splicing event in TAS1a which removed an intron that contained the miR173 processing and phased siRNAs generation sites was differentially alternatively spliced in response to cold. The cold-induced reduction of the spliced form of TAS1a and of the tasiRNAs suggests that splicing may enhance production of the siRNAs. Our results identify candidate lncRNAs that may contribute to the regulation of expression that determines the physiological processes essential for acclimation and freezing tolerance.

AB - Plants re-program their gene expression when responding to changing environmental conditions. Besides differential gene expression, extensive alternative splicing (AS) of pre-mRNAs and changes in expression of long non-coding RNAs (lncRNAs) are associated with stress responses. RNA-sequencing of a diel time-series of the initial response of Arabidopsis thaliana rosettes to low temperature showed massive and rapid waves of both transcriptional and AS activity in protein-coding genes. We exploited the high diversity of transcript isoforms in AtRTD2 to examine regulation and post-transcriptional regulation of lncRNA gene expression in response to cold stress. We identified 135 lncRNA genes with cold-dependent differential expression (DE) and/or differential alternative splicing (DAS) of lncRNAs including natural antisense RNAs, sORF lncRNAs, and precursors of microRNAs (miRNAs) and trans-acting small-interfering RNAs (tasiRNAs). The high resolution (HR) of the time-series allowed the dynamics of changes in transcription and AS to be determined and identified early and adaptive transcriptional and AS changes in the cold response. Some lncRNA genes were regulated only at the level of AS and using plants grown at different temperatures and a HR time-course of the first 3 h of temperature reduction, we demonstrated that the AS of some lncRNAs is highly sensitive to small temperature changes suggesting tight regulation of expression. In particular, a splicing event in TAS1a which removed an intron that contained the miR173 processing and phased siRNAs generation sites was differentially alternatively spliced in response to cold. The cold-induced reduction of the spliced form of TAS1a and of the tasiRNAs suggests that splicing may enhance production of the siRNAs. Our results identify candidate lncRNAs that may contribute to the regulation of expression that determines the physiological processes essential for acclimation and freezing tolerance.

KW - Long non-coding RNA

KW - Primary microRNA

KW - Alternative splicing

KW - Diel time-course

KW - High-resolution RNA-seq

KW - Cold transcriptome

U2 - 10.3389/fpls.2019.00235

DO - 10.3389/fpls.2019.00235

M3 - Article

VL - 10

SP - 1

EP - 16

JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

SN - 1664-462X

M1 - 235

ER -