ChloroSeq, an optimized chloroplast RNA-Seq bioinformatic pipeline, reveals remodeling of the organellar transcriptome under heat stress
Abstract
Although RNA-Seq has revolutionized transcript analysis, organellar transcriptomes are rarely assessed even when present in published datasets. Here, we describe the development and application of a rapid and convenient method, ChloroSeq, to delineate qualitative and quantitative features of chloroplast RNA metabolism from strand-specific RNA-Seq datasets, including processing, editing, splicing, and relative transcript abundance. The use of a single experiment to analyze systematically chloroplast transcript maturation and abundance is of particular interest due to frequent pleiotropic effects observed in mutants that affect chloroplast gene expression and/or photosynthesis. To illustrate its utility, ChloroSeq was applied to published RNA-Seq datasets derived from Arabidopsis thaliana grown under control and abiotic stress conditions, where the organellar transcriptome had not been examined. The most appreciable effects were found for heat stress, which induces a global reduction in splicing and editing efficiency, and leads to increased abundance of chloroplast transcripts, including genic, intergenic, and antisense transcripts. Moreover, by concomitantly analyzing nuclear transcripts that encode chloroplast gene expression regulators from the same libraries, we demonstrate the possibility of achieving a holistic understanding of the nucleus-organelle system. ChloroSeq thus represents a unique method for streamlining RNA-Seq data interpretation of the chloroplast transcriptome and its regulators.
- Publication Date:
- Research Org.:
- Boyce Thompson Inst., Ithaca, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1361698
- Alternate Identifier(s):
- OSTI ID: 1393425
- Grant/Contract Number:
- FG02-90ER20015; FG02-10ER20015
- Resource Type:
- Accepted Manuscript
- Journal Name:
- G3
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 9; Journal ID: ISSN 2160-1836
- Publisher:
- Genetics Society of America
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Arabidopsis thaliana; chloroplast; RNA-Seq; heat stress; transcriptome; noncoding RNAs; introns; RNA splicing; RNA editing; RNA-SEQ
Citation Formats
Castandet, Benoît, Hotto, Amber M., Strickler, Susan R., and Stern, David B. ChloroSeq, an optimized chloroplast RNA-Seq bioinformatic pipeline, reveals remodeling of the organellar transcriptome under heat stress. United States: N. p., 2016.
Web. doi:10.1534/g3.116.030783.
Castandet, Benoît, Hotto, Amber M., Strickler, Susan R., & Stern, David B. ChloroSeq, an optimized chloroplast RNA-Seq bioinformatic pipeline, reveals remodeling of the organellar transcriptome under heat stress. United States. https://doi.org/10.1534/g3.116.030783
Castandet, Benoît, Hotto, Amber M., Strickler, Susan R., and Stern, David B. Wed .
"ChloroSeq, an optimized chloroplast RNA-Seq bioinformatic pipeline, reveals remodeling of the organellar transcriptome under heat stress". United States. https://doi.org/10.1534/g3.116.030783. https://www.osti.gov/servlets/purl/1361698.
@article{osti_1361698,
title = {ChloroSeq, an optimized chloroplast RNA-Seq bioinformatic pipeline, reveals remodeling of the organellar transcriptome under heat stress},
author = {Castandet, Benoît and Hotto, Amber M. and Strickler, Susan R. and Stern, David B.},
abstractNote = {Although RNA-Seq has revolutionized transcript analysis, organellar transcriptomes are rarely assessed even when present in published datasets. Here, we describe the development and application of a rapid and convenient method, ChloroSeq, to delineate qualitative and quantitative features of chloroplast RNA metabolism from strand-specific RNA-Seq datasets, including processing, editing, splicing, and relative transcript abundance. The use of a single experiment to analyze systematically chloroplast transcript maturation and abundance is of particular interest due to frequent pleiotropic effects observed in mutants that affect chloroplast gene expression and/or photosynthesis. To illustrate its utility, ChloroSeq was applied to published RNA-Seq datasets derived from Arabidopsis thaliana grown under control and abiotic stress conditions, where the organellar transcriptome had not been examined. The most appreciable effects were found for heat stress, which induces a global reduction in splicing and editing efficiency, and leads to increased abundance of chloroplast transcripts, including genic, intergenic, and antisense transcripts. Moreover, by concomitantly analyzing nuclear transcripts that encode chloroplast gene expression regulators from the same libraries, we demonstrate the possibility of achieving a holistic understanding of the nucleus-organelle system. ChloroSeq thus represents a unique method for streamlining RNA-Seq data interpretation of the chloroplast transcriptome and its regulators.},
doi = {10.1534/g3.116.030783},
journal = {G3},
number = 9,
volume = 6,
place = {United States},
year = {Wed Jul 06 00:00:00 EDT 2016},
month = {Wed Jul 06 00:00:00 EDT 2016}
}
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Figures / Tables:
Figure 1: Flow chart of the ChloroSeq strategy. RNA-Seq reads (obtained from public databases or a sequencing facility) in the FastQ format are aligned to the plastome genome using TopHat2. ChloroSeq is then applied to the bam file containing aligned reads, giving a complete view of the chloroplast transcriptome. Usingmore »
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journal, December 2011
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journal, December 2011
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journal, October 2011
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journal, March 2007
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A Cytoplasmically Inherited Barley Mutant Is Defective in Photosystem I Assembly Due to a Temperature-Sensitive Defect in ycf3 Splicing
journal, October 2009
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journal, September 2007
- Rumeau, Dominique; Peltier, Gilles; Cournac, Laurent
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Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features
journal, October 2014
- Di, Chao; Yuan, Jiapei; Wu, Yue
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A tiling microarray for global analysis of chloroplast genome expression in cucumber and other plants
journal, January 2011
- Żmieńko, Agnieszka; Guzowska-Nowowiejska, Magdalena; Urbaniak, Radosław
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TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013
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Chloroplast RNase J compensates for inefficient transcription termination by removal of antisense RNA
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Overaccumulation of the chloroplast antisense RNA AS5 is correlated with decreased abundance of 5S rRNA in vivo and inefficient 5S rRNA maturation in vitro
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- Bioscience, Biotechnology, and Biochemistry, Vol. 68, Issue 3
Comprehensive High-Resolution Analysis of the Role of an Arabidopsis Gene Family in RNA Editing
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- Bentolila, Stéphane; Oh, Julyun; Hanson, Maureen R.
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Mediated Plastid RNA Editing in Plant Immunity
journal, October 2013
- García-Andrade, Javier; Ramírez, Vicente; López, Ana
- PLoS Pathogens, Vol. 9, Issue 10
Catalyzing plant science research with RNA-seq
journal, January 2013
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- Frontiers in Plant Science, Vol. 4
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- BMC Plant Biology
Complete mitochondrial genomes from transcriptomes: assessing pros and cons of data mining for assembling new mitogenomes
journal, October 2019
- Forni, Giobbe; Puccio, Guglielmo; Bourguignon, Thomas
- Scientific Reports, Vol. 9, Issue 1
Two interacting PPR proteins are major Arabidopsis editing factors in plastid and mitochondria
journal, July 2017
- Guillaumot, Damien; Lopez-Obando, Mauricio; Baudry, Kevin
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 33
Unraveling chloroplast transcriptomes with ChloroSeq, an organelle RNA-Seq bioinformatics pipeline
journal, September 2016
- Smith, David Roy; Sanitá Lima, Matheus
- Briefings in Bioinformatics
ORRM5, an RNA recognition motif-containing protein, has a unique effect on mitochondrial RNA editing
journal, May 2017
- Shi, Xiaowen; Castandet, Benoit; Germain, Arnaud
- Journal of Experimental Botany, Vol. 68, Issue 11
Systematic sequencing of chloroplast transcript termini from Arabidopsis thaliana reveals >200 transcription initiation sites and the extensive imprints of RNA-binding proteins and secondary structures
journal, November 2019
- Castandet, Benoît; Germain, Arnaud; Hotto, Amber M.
- Nucleic Acids Research
Systematic sequencing of chloroplast transcript termini from Arabidopsis thaliana reveals >200 transcription initiation sites and the extensive imprints of RNA-binding proteins and secondary structures
journal, September 2019
- Castandet, Benoît; Germain, Arnaud; Hotto, Amber M.
- Nucleic Acids Research
Chloroplast cold-resistance is mediated by the acidic domain of the RNA binding protein CP31A
journal, December 2019
- Okuzaki, Ayako; Lehniger, Marie-Kristin; Muino, Jose M.
- Journal of Experimental Botany
Transcription is a major driving force for plastid genome instability in Arabidopsis
journal, April 2019
- Pérez Di Giorgio, Juliana Andrea; Lepage, Étienne; Tremblay-Belzile, Samuel
- PLOS ONE, Vol. 14, Issue 4
Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
journal, September 2017
- Sanitá Lima, Matheus; Smith, David Roy
- G3: Genes|Genomes|Genetics, Vol. 7, Issue 11
Variation in plastid genomes in the gynodioecious species Silene vulgaris
journal, December 2019
- Kruger, Manuela; Abeyawardana, Oushadee A. J.; Juricek, Miloslav
- BMC Plant Biology
Sequencing the Plastid Genome of Giant Ragweed (Ambrosia trifida, Asteraceae) From a Herbarium Specimen
journal, February 2019
- Sablok, Gaurav; Amiryousefi, Ali; He, Xiaolan
- Frontiers in Plant Science, Vol. 10
MORF9 Functions in Plastid RNA Editing with Tissue Specificity
journal, September 2019
- Tian, Faan; Yu, Jinfa; Zhang, Ya
- International Journal of Molecular Sciences, Vol. 20, Issue 18
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