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Plant RNA Biology

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Front. Plant Sci. | doi: 10.3389/fpls.2019.00235

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

Cristiane P. Calixto1, Nikoleta A. Tzioutziou1,  Allan B. James2,  Csaba Hornyik3,  Wenbin Guo1, 3, 4,  Runxuan Zhang3, 4,  Hugh G. Nimmo2 and  John W. Brown1*
  • 1Plant Science Division, University of Dundee, United Kingdom
  • 2Institute of Molecular, Cell and Systems Biology, University of Glasgow, United Kingdom
  • 3Cell and Molecular Sciences, James Hutton Institute, United Kingdom
  • 4Information and Computational Sciences, James Hutton Institute, United Kingdom

Plants re-programme 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 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 have now identified cold-dependent differential expression and differential alternative splicing of long non-coding RNAs (lncRNAs) including lncRNA pre-cursors of microRNAs (miRNAs) and trans-acting small-interfering RNAs (tasiRNAs). The high resolution of the time-series identified lncRNA genes which are regulated only at the level of AS, showed rapid cold-responsive changes in expression/AS. Detailed analyses suggest that the AS of some lncRNAs is highly sensitive to small temperature changes. The AtRTD2 transcriptome used in the RNA-seq analysis contained novel transcript isoform models for many lncRNAs. 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 phased siRNAs 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

Received: 23 Nov 2018; Accepted: 12 Feb 2019.

Edited by:

Mathew G. Lewsey, La Trobe University, Australia

Reviewed by:

Yuichiro Watanabe, The University of Tokyo, Japan
Anthony Gobert, UPR2357 Institut de biologie moléculaire des plantes (IBMP), France
Alice Pajoro, Max Planck Institute for Plant Breeding Research, Germany  

Copyright: © 2019 Calixto, Tzioutziou, James, Hornyik, Guo, Zhang, Nimmo and Brown. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. John W. Brown, University of Dundee, Plant Science Division, Dundee, DD2 5DA, Scotland, United Kingdom, j.w.s.brown@dundee.ac.uk