Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome
Abstract
Noncoding RNAs (ncRNA) are widely expressed in both prokaryotes and eukaryotes. Eukaryotic ncRNAs are commonly micro- and small-interfering RNAs (18–25 nt) involved in posttranscriptional gene silencing, whereas prokaryotic ncRNAs vary in size and are involved in various aspects of gene regulation. Given the prokaryotic origin of organelles, the presence of ncRNAs might be expected; however, the full spectrum of organellar ncRNAs has not been determined systematically. Here, strand-specific RNA-Seq analysis was used to identify 107 candidate ncRNAs from Arabidopsis thaliana chloroplasts, primarily encoded opposite protein-coding and tRNA genes. Forty-eight ncRNAs were shown to accumulate by RNA gel blot as discrete transcripts in wild-type (WT) plants and/or the pnp1-1 mutant, which lacks the chloroplast ribonuclease polynucleotide phosphorylase (cpPNPase). Ninety-eight percent of the ncRNAs detected by RNA gel blot had different transcript patterns between WT and pnp1-1, suggesting cpPNPase has a significant role in chloroplast ncRNA biogenesis and accumulation. Analysis of materials deficient for other major chloroplast ribonucleases, RNase R, RNase E, and RNase J, showed differential effects on ncRNA accumulation and/or form, suggesting specificity in RNase-ncRNA interactions. 59 end mapping demonstrates that some ncRNAs are transcribed from dedicated promoters, whereas others result from transcriptional read-through. Finally, correlations between accumulation of somemore »
- Authors:
-
- US Dept. of Agriculture (USDA), Ithaca, NY (United States). Boyce Thompson Inst. for Plant Research
- Howard Hughes Medical Inst., La Jolla, CA (United States). Plant Biology and Genomic Analysis Labs.
- US Dept. of Agriculture (USDA), Ithaca, NY (United States). Boyce Thompson Inst. for Plant Research; US Dept. of Agriculture (USDA), Ithaca, NY (United States). Agricultural Research Service (ARS). Robert W. Holley Center for Agriculture and Health
- Howard Hughes Medical Inst., La Jolla, CA (United States). Plant Biology and Genomic Analysis Labs.; Howard Hughes Medical Inst., La Jolla, CA (United States). The Salk Inst. for Biological Studies
- Publication Date:
- Research Org.:
- Boyce Thompson Institute for Plant Research, Ithaca, NY (United States); Salk Institute for Biological Studies, La Jolla, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1627940
- Grant/Contract Number:
- FG02-90ER20015; FG02-04ER15517
- Resource Type:
- Accepted Manuscript
- Journal Name:
- G3
- Additional Journal Information:
- Journal Volume: 1; Journal Issue: 7; Journal ID: ISSN 2160-1836
- Publisher:
- Genetics Society of America
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Genetics & Heredity; RNA-Seq; posttranscriptional regulation; transcription; organelle; plastid
Citation Formats
Hotto, Amber M., Schmitz, Robert J., Fei, Zhangjun, Ecker, Joseph R., and Stern, David B. Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome. United States: N. p., 2011.
Web. doi:10.1534/g3.111.000752.
Hotto, Amber M., Schmitz, Robert J., Fei, Zhangjun, Ecker, Joseph R., & Stern, David B. Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome. United States. https://doi.org/10.1534/g3.111.000752
Hotto, Amber M., Schmitz, Robert J., Fei, Zhangjun, Ecker, Joseph R., and Stern, David B. Thu .
"Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome". United States. https://doi.org/10.1534/g3.111.000752. https://www.osti.gov/servlets/purl/1627940.
@article{osti_1627940,
title = {Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome},
author = {Hotto, Amber M. and Schmitz, Robert J. and Fei, Zhangjun and Ecker, Joseph R. and Stern, David B.},
abstractNote = {Noncoding RNAs (ncRNA) are widely expressed in both prokaryotes and eukaryotes. Eukaryotic ncRNAs are commonly micro- and small-interfering RNAs (18–25 nt) involved in posttranscriptional gene silencing, whereas prokaryotic ncRNAs vary in size and are involved in various aspects of gene regulation. Given the prokaryotic origin of organelles, the presence of ncRNAs might be expected; however, the full spectrum of organellar ncRNAs has not been determined systematically. Here, strand-specific RNA-Seq analysis was used to identify 107 candidate ncRNAs from Arabidopsis thaliana chloroplasts, primarily encoded opposite protein-coding and tRNA genes. Forty-eight ncRNAs were shown to accumulate by RNA gel blot as discrete transcripts in wild-type (WT) plants and/or the pnp1-1 mutant, which lacks the chloroplast ribonuclease polynucleotide phosphorylase (cpPNPase). Ninety-eight percent of the ncRNAs detected by RNA gel blot had different transcript patterns between WT and pnp1-1, suggesting cpPNPase has a significant role in chloroplast ncRNA biogenesis and accumulation. Analysis of materials deficient for other major chloroplast ribonucleases, RNase R, RNase E, and RNase J, showed differential effects on ncRNA accumulation and/or form, suggesting specificity in RNase-ncRNA interactions. 59 end mapping demonstrates that some ncRNAs are transcribed from dedicated promoters, whereas others result from transcriptional read-through. Finally, correlations between accumulation of some ncRNAs and the symmetrically transcribed sense RNA are consistent with a role in RNA stability. Overall, our data suggest that this extensive population of ncRNAs has the potential to underpin a previously underappreciated regulatory mode in the chloroplast.},
doi = {10.1534/g3.111.000752},
journal = {G3},
number = 7,
volume = 1,
place = {United States},
year = {Thu Dec 01 00:00:00 EST 2011},
month = {Thu Dec 01 00:00:00 EST 2011}
}
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Works referenced in this record:
PNPase is a key player in the regulation of small RNAs that control the expression of outer membrane proteins
journal, January 2008
- Andrade, J. M.; Arraiano, C. M.
- RNA, Vol. 14, Issue 3
Transcription and transcriptional regulation in plastids
book, January 2007
- Liere, Karsten; Börner, Thomas
- Cell and Molecular Biology of Plastids, 121–174
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana
journal, August 2003
- Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J.
- Science, Vol. 301, Issue 5633, p. 653-657
Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation
journal, July 2009
- Pfeiffer, Verena; Papenfort, Kai; Lucchini, Sacha
- Nature Structural & Molecular Biology, Vol. 16, Issue 8
Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species
journal, July 2006
- Zhang, Y.
- Nucleic Acids Research, Vol. 34, Issue 12
Overexpression of a natural chloroplast-encoded antisense RNA in tobacco destabilizes 5S rRNA and retards plant growth
journal, January 2010
- Hotto, Amber M.; Huston, Zoe E.; Stern, David B.
- BMC Plant Biology, Vol. 10, Issue 1
Expression of complementary RNA from chloroplast transgenes affects editing efficiency of transgene and endogenous chloroplast transcripts
journal, March 2005
- Hegeman, C. E.
- Nucleic Acids Research, Vol. 33, Issue 5
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010
- Trapnell, Cole; Williams, Brian A.; Pertea, Geo
- Nature Biotechnology, Vol. 28, Issue 5
PNPase activity determines the efficiency of mRNA 3'-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts
journal, December 2002
- Walter, M.
- The EMBO Journal, Vol. 21, Issue 24
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009
- Langmead, Ben; Trapnell, Cole; Pop, Mihai
- Genome Biology, Vol. 10, Issue 3
Processing, degradation, and polyadenylation of chloroplast transcripts
book, January 2007
- Bollenbach, Thomas J.; Schuster, Gadi; Portnoy, Victoria
- Cell and Molecular Biology of Plastids
Translation and translational regulation in chloroplasts
book, January 2007
- Peled-Zehavi, Hadas; Danon, Avihai
- Cell and Molecular Biology of Plastids
Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts
journal, October 2004
- Nishimura, Yoshiki; Kikis, Elise A.; Zimmer, Sara L.
- The Plant Cell, Vol. 16, Issue 11
A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa)
journal, June 2011
- Wang, Lu; Yu, Xiang; Wang, Han
- BMC Genomics, Vol. 12, Issue 1
RNR1, a 3'-5' exoribonuclease belonging to the RNR superfamily, catalyzes 3' maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana
journal, April 2005
- Bollenbach, T. J.
- Nucleic Acids Research, Vol. 33, Issue 8
The Challenge of Regulation in a Minimal Photoautotroph: Non-Coding RNAs in Prochlorococcus
journal, August 2008
- Steglich, Claudia; Futschik, Matthias E.; Lindell, Debbie
- PLoS Genetics, Vol. 4, Issue 8
Identification of small non-coding RNAs from mitochondria and chloroplasts
journal, August 2006
- Lung, Birgit; Zemann, Anja; Madej, Monika J.
- Nucleic Acids Research, Vol. 34, Issue 14
A subpopulation of spinach chloroplast tRNA genes does not require upstream promoter elements for transcription
journal, January 1986
- Gruissem, W.; Elsner-Menzel, C.; Latshaw, S.
- Nucleic Acids Research, Vol. 14, Issue 19
Plastid RNA Polymerases in Higher Plants
book, January 2001
- Liere, Karsten; Maliga, Pal
- Regulation of Photosynthesis
Sensitive detection of bacterial transcription initiation sites and differentiation from RNA processing sites in the pheromone-induced plasmid transfer system of Enterococcus faecalis.
journal, July 1996
- Bensing, B. A.; Meyer, B. J.; Dunny, G. M.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 15
Characterization of plastid psb T sense and antisense RNAs
journal, March 2011
- Zghidi-Abouzid, Ouafa; Merendino, Livia; Buhr, Frank
- Nucleic Acids Research, Vol. 39, Issue 13
An Abundance of rna Regulators
journal, June 2005
- Storz, Gisela; Altuvia, Shoshy; Wassarman, Karen M.
- Annual Review of Biochemistry, Vol. 74, Issue 1
Overaccumulation of the chloroplast antisense RNA AS5 is correlated with decreased abundance of 5S rRNA in vivo and inefficient 5S rRNA maturation in vitro
journal, December 2010
- Sharwood, R. E.; Hotto, A. M.; Bollenbach, T. J.
- RNA, Vol. 17, Issue 2
Improving RNA-Seq expression estimates by correcting for fragment bias
journal, January 2011
- Roberts, Adam; Trapnell, Cole; Donaghey, Julie
- Genome Biology, Vol. 12, Issue 3
A long antisense RNA in plant chloroplasts: Rapid report
journal, February 2010
- Georg, J.; Honsel, A.; Voß, B.
- New Phytologist, Vol. 186, Issue 3
Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes.
journal, December 1985
- Gruissem, W.; Zurawski, G.
- The EMBO Journal, Vol. 4, Issue 13A
Genomic sequencing.
journal, April 1984
- Church, G. M.; Gilbert, W.
- Proceedings of the National Academy of Sciences, Vol. 81, Issue 7
Evidence for a major role of antisense RNAs in cyanobacterial gene regulation
journal, January 2009
- Georg, Jens; Voß, Björn; Scholz, Ingeborg
- Molecular Systems Biology, Vol. 5, Issue 1
RNA-Seq: a revolutionary tool for transcriptomics
journal, January 2009
- Wang, Zhong; Gerstein, Mark; Snyder, Michael
- Nature Reviews Genetics, Vol. 10, Issue 1
Small RNA gene identification and mRNA target predictions in bacteria
journal, October 2008
- Pichon, C.; Felden, B.
- Bioinformatics, Vol. 24, Issue 24
Natural antisense transcripts with coding capacity in Arabidopsismay have a regulatory role that is not linked to double-stranded RNA degradation
journal, January 2005
- Jen, Chih-Hung; Michalopoulos, Ioannis; Westhead, David R.
- Genome Biology, Vol. 6, Issue 6, p. R51
RNA-quality control by the exosome
journal, July 2006
- Houseley, Jonathan; LaCava, John; Tollervey, David
- Nature Reviews Molecular Cell Biology, Vol. 7, Issue 7
Possible Involvement of the 5′-Flanking Region and the 5′UTR of Plastid accD Gene in NEP-Dependent Transcription
journal, February 2004
- Hirata, Norihiro; Yonekura, Daizou; Yanagisawa, Shuichi
- Plant and Cell Physiology, Vol. 45, Issue 2
Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription
journal, December 1987
- Stern, David B.; Gruissem, Wilhelm
- Cell, Vol. 51, Issue 6
Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays
journal, December 2010
- Stead, Mark B.; Marshburn, Sarah; Mohanty, Bijoy K.
- Nucleic Acids Research, Vol. 39, Issue 8
Characterization of the role of ribonucleases in Salmonella small RNA decay
journal, November 2007
- Viegas, Sandra C.; Pfeiffer, Verena; Sittka, Alexandra
- Nucleic Acids Research, Vol. 35, Issue 22
The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids
journal, July 1997
- Hajdukiewicz, Peter T. J.; Allison, Lori A.; Maliga, Pal
- The EMBO Journal, Vol. 16, Issue 13
A 125 kDa RNase E/G-like protein is present in plastids and is essential for chloroplast development and autotrophic growth in Arabidopsis*
journal, May 2008
- Mudd, Elisabeth A.; Sullivan, Stuart; Gisby, Martin F.
- Journal of Experimental Botany, Vol. 59, Issue 10
Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1
journal, January 2007
- Britton, Robert A.; Wen, Tingyi; Schaefer, Laura
- Molecular Microbiology, Vol. 63, Issue 1
Abnormal Physiological and Molecular Mutant Phenotypes Link Chloroplast Polynucleotide Phosphorylase to the Phosphorus Deprivation Response in Arabidopsis
journal, August 2009
- Marchive, Chloe; Yehudai-Resheff, Shlomit; Germain, Arnaud
- Plant Physiology, Vol. 151, Issue 2
High diversity of plastidial promoters in Arabidopsis thaliana
journal, March 2007
- Swiatecka-Hagenbruch, Monika; Liere, Karsten; Börner, Thomas
- Molecular Genetics and Genomics, Vol. 277, Issue 6
Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis
journal, May 2008
- Lister, Ryan; O'Malley, Ronan C.; Tonti-Filippini, Julian
- Cell, Vol. 133, Issue 3
Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana
journal, January 2005
- Wang, Xiu-Jie; Gaasterland, Terry; Chua, Nam-Hai
- Genome Biology, Vol. 6, Issue 4, p. R30
Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA
journal, April 2009
- Desnoyers, Guillaume; Morissette, Audrey; Prévost, Karine
- The EMBO Journal, Vol. 28, Issue 11
Role of Bacillus subtilis RNase J1 Endonuclease and 5′-Exonuclease Activities in trp Leader RNA Turnover
journal, June 2008
- Deikus, Gintaras; Condon, Ciarán; Bechhofer, David H.
- Journal of Biological Chemistry, Vol. 283, Issue 25
Mutational analysis of Arabidopsis chloroplast polynucleotide phosphorylase reveals roles for both RNase PH core domains in polyadenylation, RNA 3′-end maturation and intron degradation: Chloroplast PNPase function
journal, May 2011
- Germain, Arnaud; Herlich, Shira; Larom, Shirley
- The Plant Journal, Vol. 67, Issue 3
Relaxed Transcription in Arabidopsis Mitochondria Is Counterbalanced by RNA Stability Control Mediated by Polyadenylation and Polynucleotide Phosphorylase
journal, April 2006
- Holec, Sarah; Lange, Heike; Kühn, Kristina
- Molecular and Cellular Biology, Vol. 26, Issue 7
Experimental RNomics
journal, December 2002
- Marker, Claudia; Zemann, Anja; Terhörst, Tanja
- Current Biology, Vol. 12, Issue 23
Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns: Time course study of short RNAs during fruit development
journal, May 2011
- Mohorianu, Irina; Schwach, Frank; Jing, Runchun
- The Plant Journal, Vol. 67, Issue 2
GadY, a Small-RNA Regulator of Acid Response Genes in Escherichia coli
journal, October 2004
- Opdyke, Jason A.; Kang, Ju-Gyeong; Storz, Gisela
- Journal of Bacteriology, Vol. 186, Issue 20
Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects
journal, February 2009
- Repoila, Francis; Darfeuille, Fabien
- Biology of the Cell, Vol. 101, Issue 2
Sequence and transcriptional analysis of the barley ctDNA region upstream of psbD-psbC encoding trnK(UUU), rps16, trnQ(UUG), psbK, psbI, and trnS(GCU)
journal, May 1990
- Sexton, Tineke Berends; Jones, Jennifer T.; Mullet, John E.
- Current Genetics, Vol. 17, Issue 5
Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency: Functions of a chloroplast RNase E
journal, October 2010
- Walter, Michael; Piepenburg, Katrin; Schöttler, Mark Aurel
- The Plant Journal, Vol. 64, Issue 5
A new in vitro translation system for non-radioactive assay from tobacco chloroplasts: effect of pre-mRNA processing on translation in vitro: Improved chloroplast in vitro translation system
journal, December 2006
- Yukawa, Maki; Kuroda, Hiroshi; Sugiura, Masahiro
- The Plant Journal, Vol. 49, Issue 2
Genomic sequencing
book, December 2015
- Kahl, Gunter
- The Dictionary of Genomics, Transcriptomics and Proteomics
SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation
journal, July 2020
- Zoch, Ansgar; Auchynnikava, Tania; Berrens, Rebecca V.
- Nature, Vol. 584, Issue 7822
Genomic insight into diet adaptation in the biological control agent Cryptolaemus montrouzieri
journal, February 2021
- Li, Hao-Sen; Huang, Yu-Hao; Chen, Mei-Lan
- BMC Genomics, Vol. 22, Issue 1
Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes.
journal, December 1985
- Gruissem, W.; Zurawski, G.
- The EMBO Journal, Vol. 4, Issue 13A
Transcription and transcriptional regulation in plastids
book, January 2007
- Liere, Karsten; Börner, Thomas
- Cell and Molecular Biology of Plastids, 121–174
High diversity of plastidial promoters in Arabidopsis thaliana
journal, March 2007
- Swiatecka-Hagenbruch, Monika; Liere, Karsten; Börner, Thomas
- Molecular Genetics and Genomics, Vol. 277, Issue 6
Identification of the transcription start site for the spinach chloroplast serine tRNA gene
journal, November 1997
- Wu, Chih-Yu; Lin, Chi-Hui; Chen, Liang-Jwu
- FEBS Letters, Vol. 418, Issue 1-2
Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA
journal, April 2009
- Desnoyers, Guillaume; Morissette, Audrey; Prévost, Karine
- The EMBO Journal, Vol. 28, Issue 11
Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation
journal, July 2009
- Pfeiffer, Verena; Papenfort, Kai; Lucchini, Sacha
- Nature Structural & Molecular Biology, Vol. 16, Issue 8
Small RNA gene identification and mRNA target predictions in bacteria
journal, October 2008
- Pichon, C.; Felden, B.
- Bioinformatics, Vol. 24, Issue 24
The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids
journal, July 1997
- Hajdukiewicz, Peter T. J.; Allison, Lori A.; Maliga, Pal
- The EMBO Journal, Vol. 16, Issue 13
A 125 kDa RNase E/G-like protein is present in plastids and is essential for chloroplast development and autotrophic growth in Arabidopsis*
journal, May 2008
- Mudd, Elisabeth A.; Sullivan, Stuart; Gisby, Martin F.
- Journal of Experimental Botany, Vol. 59, Issue 10
Expression of complementary RNA from chloroplast transgenes affects editing efficiency of transgene and endogenous chloroplast transcripts
journal, March 2005
- Hegeman, C. E.
- Nucleic Acids Research, Vol. 33, Issue 5
RNR1, a 3'-5' exoribonuclease belonging to the RNR superfamily, catalyzes 3' maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana
journal, April 2005
- Bollenbach, T. J.
- Nucleic Acids Research, Vol. 33, Issue 8
Identification of small non-coding RNAs from mitochondria and chloroplasts
journal, August 2006
- Lung, Birgit; Zemann, Anja; Madej, Monika J.
- Nucleic Acids Research, Vol. 34, Issue 14
Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species
journal, July 2006
- Zhang, Y.
- Nucleic Acids Research, Vol. 34, Issue 12
Characterization of the role of ribonucleases in Salmonella small RNA decay
journal, November 2007
- Viegas, Sandra C.; Pfeiffer, Verena; Sittka, Alexandra
- Nucleic Acids Research, Vol. 35, Issue 22
Possible Involvement of the 5′-Flanking Region and the 5′UTR of Plastid accD Gene in NEP-Dependent Transcription
journal, February 2004
- Hirata, Norihiro; Yonekura, Daizou; Yanagisawa, Shuichi
- Plant and Cell Physiology, Vol. 45, Issue 2
Abnormal Physiological and Molecular Mutant Phenotypes Link Chloroplast Polynucleotide Phosphorylase to the Phosphorus Deprivation Response in Arabidopsis
journal, August 2009
- Marchive, Chloe; Yehudai-Resheff, Shlomit; Germain, Arnaud
- Plant Physiology, Vol. 151, Issue 2
Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts
journal, October 2004
- Nishimura, Yoshiki; Kikis, Elise A.; Zimmer, Sara L.
- The Plant Cell, Vol. 16, Issue 11
An Abundance of rna Regulators
journal, June 2005
- Storz, Gisela; Altuvia, Shoshy; Wassarman, Karen M.
- Annual Review of Biochemistry, Vol. 74, Issue 1
PNPase is a key player in the regulation of small RNAs that control the expression of outer membrane proteins
journal, January 2008
- Andrade, J. M.; Arraiano, C. M.
- RNA, Vol. 14, Issue 3
Correction: The Challenge of Regulation in a Minimal Photoautotroph: Non-Coding RNAs in Prochlorococcus
journal, November 2008
- Steglich, Claudia; Futschik, Matthias E.; Lindell, Debbie
- PLoS Genetics, Vol. 4, Issue 11
Works referencing / citing this record:
Long Non-Coding RNAs: Rising Regulators of Plant Reproductive Development
journal, January 2019
- Yu, Tongtong; Zhu, Hongliang
- Agronomy, Vol. 9, Issue 2
Variation in plastid genomes in the gynodioecious species Silene vulgaris
journal, December 2019
- Krüger, Manuela; Abeyawardana, Oushadee A. J.; Juříček, Miloslav
- BMC Plant Biology, Vol. 19, Issue 1
It's a small, small world: unravelling the role and evolution of small RNAs in organelle and endosymbiont genomes
journal, March 2019
- Thairu, Margaret W.; Hansen, Allison K.
- FEMS Microbiology Letters, Vol. 366, Issue 5
Multifarious Evolutionary Pathways of a Nuclear RNA Editing Factor: Disjunctions in Coevolution of DOT4 and Its Chloroplast Target rpoC1eU488SL
journal, February 2019
- Hein, Anke; Brenner, Sarah; Knoop, Volker
- Genome Biology and Evolution, Vol. 11, Issue 3
Expression of the chloroplast genome: Modern concepts and experimental approaches
journal, July 2016
- Siniauskaya, M. G.; Danilenko, N. G.; Lukhanina, N. V.
- Russian Journal of Genetics: Applied Research, Vol. 6, Issue 5
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
Arabidopsis chloroplast quantitative editotype
journal, March 2013
- Ruwe, Hannes; Castandet, Benoit; Schmitz-Linneweber, Christian
- FEBS Letters, Vol. 587, Issue 9
RNA processing and decay in plastids: RNA processing and decay in plastids
journal, March 2013
- Germain, Arnaud; Hotto, Amber M.; Barkan, Alice
- Wiley Interdisciplinary Reviews: RNA, Vol. 4, Issue 3
Chloroplast Gene Expression—RNA Synthesis and Processing
book, January 2014
- Börner, Thomas; Zhelyazkova, Petya; Legen, Julia
- Plastid Biology
Full transcription of the chloroplast genome in photosynthetic eukaryotes
journal, July 2016
- Shi, Chao; Wang, Shuo; Xia, En-Hua
- Scientific Reports, Vol. 6, Issue 1
Systematic analysis of plant mitochondrial and chloroplast small RNAs suggests organelle-specific mRNA stabilization mechanisms
journal, May 2016
- Ruwe, Hannes; Wang, Gongwei; Gusewski, Sandra
- 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, November 2019
- Castandet, Benoît; Germain, Arnaud; Hotto, Amber M.
- Nucleic Acids Research
The accumulation of chloroplast small RNAs in unicellular alga Chlamydomonas reinhardtii is affected by nitrogen deprivation
preprint, November 2019
- Che-Ani, Suhaimi; Azzam, Ghows; Najimudin, Nazalan
Bacterial antisense RNAs are mainly the product of transcriptional noise
journal, March 2016
- Lloréns-Rico, Verónica; Cano, Jaime; Kamminga, Tjerko
- Science Advances, Vol. 2, Issue 3
LncRNA expression profile and ceRNA analysis in tomato during flowering
journal, January 2019
- Yang, Zhenchao; Yang, Chengcheng; Wang, Zhengyan
- PLOS ONE, Vol. 14, Issue 1
ChloroSeq, an Optimized Chloroplast RNA-Seq Bioinformatic Pipeline, Reveals Remodeling of the Organellar Transcriptome Under Heat Stress
journal, July 2016
- Castandet, Benoît; Hotto, Amber M.; Strickler, Susan R.
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 9
Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
text, January 2017
- Shao, Mon-Ray; Kumar Kenchanmane Raju, Sunil; Laurie, John D.
- Apollo - University of Cambridge Repository
Variation in plastid genomes in the gynodioecious species Silene vulgaris
journal, December 2019
- Kruger, Manuela; Abeyawardana, Oushadee A. J.; Juricek, Miloslav
- BMC Plant Biology
Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
journal, February 2017
- Shao, Mon-Ray; Kumar Kenchanmane Raju, Sunil; Laurie, John D.
- BMC Plant Biology, Vol. 17, Issue 1
Expression of the chloroplast genome: modern concepts and experimental approaches
journal, December 2015
- Siniauskaya, M. G.; Danilenko, N. G.; Lukhanina, N. V.
- Vavilov Journal of Genetics and Breeding, Vol. 19, Issue 5
Variation in plastid genomes in the gynodioecious species Silene vulgaris
journal, December 2019
- Kruger, Manuela; Abeyawardana, Oushadee A. J.; Juricek, Miloslav
- BMC Plant Biology
Full transcription of the chloroplast genome in photosynthetic eukaryotes
journal, July 2016
- Shi, Chao; Wang, Shuo; Xia, En-Hua
- Scientific Reports, Vol. 6, Issue 1
Small RNAs reveal two target sites of the RNA-maturation factor Mbb1 in the chloroplast of Chlamydomonas
journal, December 2013
- Loizeau, Karen; Qu, Yujiao; Depp, Sébastien
- Nucleic Acids Research, Vol. 42, Issue 5
Systematic analysis of plant mitochondrial and chloroplast small RNAs suggests organelle-specific mRNA stabilization mechanisms
journal, May 2016
- Ruwe, Hannes; Wang, Gongwei; Gusewski, Sandra
- 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
Bacterial antisense RNAs are mainly the product of transcriptional noise
journal, March 2016
- Lloréns-Rico, Verónica; Cano, Jaime; Kamminga, Tjerko
- Science Advances, Vol. 2, Issue 3
Complex Interplay among DNA Modification, Noncoding RNA Expression and Protein-Coding RNA Expression in Salvia miltiorrhiza Chloroplast Genome
journal, June 2014
- Chen, Haimei; Zhang, Jianhui; Yuan, George
- PLoS ONE, Vol. 9, Issue 6
Exploring the Genes of Yerba Mate (Ilex paraguariensis A. St.-Hil.) by NGS and De Novo Transcriptome Assembly
journal, October 2014
- Debat, Humberto J.; Grabiele, Mauro; Aguilera, Patricia M.
- PLoS ONE, Vol. 9, Issue 10
LncRNA expression profile and ceRNA analysis in tomato during flowering
journal, January 2019
- Yang, Zhenchao; Yang, Chengcheng; Wang, Zhengyan
- PLOS ONE, Vol. 14, Issue 1
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
Genome-wide Discovery of Circular RNAs in the Leaf and Seedling Tissues of Arabidopsis Thaliana
journal, July 2017
- Dou, Yongchao; Li, Shengjun; Yang, Weilong
- Current Genomics, Vol. 18, Issue 4
Recent advances in the study of chloroplast gene expression and its evolution
journal, January 2014
- Yagi, Yusuke; Shiina, Takashi
- Frontiers in Plant Science, Vol. 5
The Pokeweed Leaf mRNA Transcriptome and Its Regulation by Jasmonic Acid
journal, March 2016
- Neller, Kira C. M.; Klenov, Alexander; Hudak, Katalin A.
- Frontiers in Plant Science, Vol. 7
Novel Insights into Insect-Microbe Interactions—Role of Epigenomics and Small RNAs
journal, August 2016
- Kim, Dohyup; Thairu, Margaret W.; Hansen, Allison K.
- Frontiers in Plant Science, Vol. 7
A Single Cell but Many Different Transcripts: A Journey into the World of Long Non-Coding RNAs
journal, January 2020
- Alessio, Enrico; Bonadio, Raphael Severino; Buson, Lisa
- International Journal of Molecular Sciences, Vol. 21, Issue 1