How does temperature affect splicing events? Isoform switching of splicing factors regulates splicing of LATE ELONGATED HYPOCOTYL (LHY)

Allan B. James (Lead / Corresponding author), Cristiane P. G. Calixto, Nikoleta A. Tzioutziou, Wenbin Guo, Runxuan Zhang, Craig G. Simpson, Wenying Jiang, Gillian A. Nimmo, John W. S. Brown, Hugh G. Nimmo

Research output: Contribution to journalArticle

3 Citations (Scopus)
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Abstract

One of the ways in which plants can respond to temperature is via alternative splicing (AS). Previous work showed that temperature changes affected the splicing of several circadian clock gene transcripts. Here we investigated the role of RNA-binding splicing factors (SFs) in temperature-sensitive alternative splicing (AS) of the clock gene LATE ELONGATED HYPOCOTYL (LHY). We characterised, in wild type plants, temperature-associated isoform switching and expression patterns for SF transcripts from a high-resolution temperature and time series RNA-seq experiment. In addition we employed quantitative RT-PCR of SF mutant plants to explore the role of the SFs in cooling-associated AS of LHY. We show that the splicing and expression of several SFs responds sufficiently rapidly and sensitively to temperature changes to contribute to the splicing of the 5'UTR of LHY. Moreover the choice of splice site in LHY was altered in some SF mutants. The splicing of the 5'UTR region of LHY has characteristics of a molecular thermostat, where the ratio of transcript isoforms is sensitive to temperature changes as modest as 2°C and is scalable over a wide dynamic range of temperature. Our work provides novel insight into SF-mediated coupling of the perception of temperature to post-transcriptional regulation of the clock.

Original languageEnglish
Pages (from-to)1539-1550
Number of pages12
JournalPlant, Cell & Environment
Volume41
Issue number7
Early online date13 Mar 2018
DOIs
Publication statusPublished - 1 Jul 2018

Fingerprint

Hypocotyl
hypocotyls
Protein Isoforms
Temperature
temperature
alternative splicing
Alternative Splicing
5' Untranslated Regions
5' untranslated regions
thermostats
RNA
RNA Splicing Factors
mutants
Circadian Clocks
circadian rhythm
Genes
time series analysis
genes
cooling
reverse transcriptase polymerase chain reaction

Keywords

  • Journal article
  • Circadian
  • Signalling
  • 5’UTR
  • Alternative splicing
  • Arabidopsis
  • Temperature
  • Thermostat
  • Isoform switch
  • Splicing factors

Cite this

James, Allan B. ; Calixto, Cristiane P. G. ; Tzioutziou, Nikoleta A. ; Guo, Wenbin ; Zhang, Runxuan ; Simpson, Craig G. ; Jiang, Wenying ; Nimmo, Gillian A. ; Brown, John W. S. ; Nimmo, Hugh G. / How does temperature affect splicing events? Isoform switching of splicing factors regulates splicing of LATE ELONGATED HYPOCOTYL (LHY). In: Plant, Cell & Environment. 2018 ; Vol. 41, No. 7. pp. 1539-1550.
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title = "How does temperature affect splicing events? Isoform switching of splicing factors regulates splicing of LATE ELONGATED HYPOCOTYL (LHY)",
abstract = "One of the ways in which plants can respond to temperature is via alternative splicing (AS). Previous work showed that temperature changes affected the splicing of several circadian clock gene transcripts. Here we investigated the role of RNA-binding splicing factors (SFs) in temperature-sensitive alternative splicing (AS) of the clock gene LATE ELONGATED HYPOCOTYL (LHY). We characterised, in wild type plants, temperature-associated isoform switching and expression patterns for SF transcripts from a high-resolution temperature and time series RNA-seq experiment. In addition we employed quantitative RT-PCR of SF mutant plants to explore the role of the SFs in cooling-associated AS of LHY. We show that the splicing and expression of several SFs responds sufficiently rapidly and sensitively to temperature changes to contribute to the splicing of the 5'UTR of LHY. Moreover the choice of splice site in LHY was altered in some SF mutants. The splicing of the 5'UTR region of LHY has characteristics of a molecular thermostat, where the ratio of transcript isoforms is sensitive to temperature changes as modest as 2°C and is scalable over a wide dynamic range of temperature. Our work provides novel insight into SF-mediated coupling of the perception of temperature to post-transcriptional regulation of the clock.",
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author = "James, {Allan B.} and Calixto, {Cristiane P. G.} and Tzioutziou, {Nikoleta A.} and Wenbin Guo and Runxuan Zhang and Simpson, {Craig G.} and Wenying Jiang and Nimmo, {Gillian A.} and Brown, {John W. S.} and Nimmo, {Hugh G.}",
note = "This work was supported by funding from the Biotechnology and Biological Sciences Research Council (BBSRC) [BB/K006568/1 and BB/P009751/1 to J.W.S.B. BB/H000135/1, BB/K006835/1 and BB/P006868/1 to H.G.N.] and the Scottish Government Rural and Environment Science and Analytical Services division (RESAS) [to J.W.S.B. and R.Z.].",
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How does temperature affect splicing events? Isoform switching of splicing factors regulates splicing of LATE ELONGATED HYPOCOTYL (LHY). / James, Allan B. (Lead / Corresponding author); Calixto, Cristiane P. G.; Tzioutziou, Nikoleta A.; Guo, Wenbin; Zhang, Runxuan; Simpson, Craig G.; Jiang, Wenying; Nimmo, Gillian A.; Brown, John W. S.; Nimmo, Hugh G.

In: Plant, Cell & Environment, Vol. 41, No. 7, 01.07.2018, p. 1539-1550.

Research output: Contribution to journalArticle

TY - JOUR

T1 - How does temperature affect splicing events? Isoform switching of splicing factors regulates splicing of LATE ELONGATED HYPOCOTYL (LHY)

AU - James, Allan B.

AU - Calixto, Cristiane P. G.

AU - Tzioutziou, Nikoleta A.

AU - Guo, Wenbin

AU - Zhang, Runxuan

AU - Simpson, Craig G.

AU - Jiang, Wenying

AU - Nimmo, Gillian A.

AU - Brown, John W. S.

AU - Nimmo, Hugh G.

N1 - This work was supported by funding from the Biotechnology and Biological Sciences Research Council (BBSRC) [BB/K006568/1 and BB/P009751/1 to J.W.S.B. BB/H000135/1, BB/K006835/1 and BB/P006868/1 to H.G.N.] and the Scottish Government Rural and Environment Science and Analytical Services division (RESAS) [to J.W.S.B. and R.Z.].

PY - 2018/7/1

Y1 - 2018/7/1

N2 - One of the ways in which plants can respond to temperature is via alternative splicing (AS). Previous work showed that temperature changes affected the splicing of several circadian clock gene transcripts. Here we investigated the role of RNA-binding splicing factors (SFs) in temperature-sensitive alternative splicing (AS) of the clock gene LATE ELONGATED HYPOCOTYL (LHY). We characterised, in wild type plants, temperature-associated isoform switching and expression patterns for SF transcripts from a high-resolution temperature and time series RNA-seq experiment. In addition we employed quantitative RT-PCR of SF mutant plants to explore the role of the SFs in cooling-associated AS of LHY. We show that the splicing and expression of several SFs responds sufficiently rapidly and sensitively to temperature changes to contribute to the splicing of the 5'UTR of LHY. Moreover the choice of splice site in LHY was altered in some SF mutants. The splicing of the 5'UTR region of LHY has characteristics of a molecular thermostat, where the ratio of transcript isoforms is sensitive to temperature changes as modest as 2°C and is scalable over a wide dynamic range of temperature. Our work provides novel insight into SF-mediated coupling of the perception of temperature to post-transcriptional regulation of the clock.

AB - One of the ways in which plants can respond to temperature is via alternative splicing (AS). Previous work showed that temperature changes affected the splicing of several circadian clock gene transcripts. Here we investigated the role of RNA-binding splicing factors (SFs) in temperature-sensitive alternative splicing (AS) of the clock gene LATE ELONGATED HYPOCOTYL (LHY). We characterised, in wild type plants, temperature-associated isoform switching and expression patterns for SF transcripts from a high-resolution temperature and time series RNA-seq experiment. In addition we employed quantitative RT-PCR of SF mutant plants to explore the role of the SFs in cooling-associated AS of LHY. We show that the splicing and expression of several SFs responds sufficiently rapidly and sensitively to temperature changes to contribute to the splicing of the 5'UTR of LHY. Moreover the choice of splice site in LHY was altered in some SF mutants. The splicing of the 5'UTR region of LHY has characteristics of a molecular thermostat, where the ratio of transcript isoforms is sensitive to temperature changes as modest as 2°C and is scalable over a wide dynamic range of temperature. Our work provides novel insight into SF-mediated coupling of the perception of temperature to post-transcriptional regulation of the clock.

KW - Journal article

KW - Circadian

KW - Signalling

KW - 5’UTR

KW - Alternative splicing

KW - Arabidopsis

KW - Temperature

KW - Thermostat

KW - Isoform switch

KW - Splicing factors

U2 - 10.1111/pce.13193

DO - 10.1111/pce.13193

M3 - Article

VL - 41

SP - 1539

EP - 1550

JO - Plant, Cell & Environment

JF - Plant, Cell & Environment

SN - 1365-3040

IS - 7

ER -