Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome

Hotto, Amber M.; Schmitz, Robert J.; Fei, Zhangjun; Ecker, Joseph R.; Stern, David B.

doi:10.1534/g3.111.000752

Title: Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome

Journal Article · Thu Dec 01 00:00:00 EST 2011 · G3

DOI:https://doi.org/10.1534/g3.111.000752· OSTI ID:1627940

Hotto, Amber M. ^[1]; Schmitz, Robert J. ^[2]; Fei, Zhangjun ^[3]; Ecker, Joseph R. ^[4]; Stern, David B. ^[1]

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

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.

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Research Organization:: Boyce Thompson Institute for Plant Research, Ithaca, NY (United States); Salk Institute for Biological Studies, La Jolla, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: FG02-90ER20015; FG02-04ER15517

OSTI ID:: 1627940

Journal Information:: G3, Vol. 1, Issue 7; ISSN 2160-1836

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

PNPase is a key player in the regulation of small RNAs that control the expression of outer membrane proteins Andrade, J. M.; Arraiano, C. M. RNA, Vol. 14, Issue 3 https://doi.org/10.1261/rna.683308	journal	January 2008
Transcription and transcriptional regulation in plastids Liere, Karsten; Börner, Thomas Cell and Molecular Biology of Plastids, 121–174 https://doi.org/10.1007/4735_2007_0232	book	January 2007
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation Pfeiffer, Verena; Papenfort, Kai; Lucchini, Sacha Nature Structural & Molecular Biology, Vol. 16, Issue 8 https://doi.org/10.1038/nsmb.1631	journal	July 2009
Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species Zhang, Y. Nucleic Acids Research, Vol. 34, Issue 12 https://doi.org/10.1093/nar/gkl473	journal	July 2006
Overexpression of a natural chloroplast-encoded antisense RNA in tobacco destabilizes 5S rRNA and retards plant growth Hotto, Amber M.; Huston, Zoe E.; Stern, David B. BMC Plant Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2229-10-213	journal	January 2010
Expression of complementary RNA from chloroplast transgenes affects editing efficiency of transgene and endogenous chloroplast transcripts Hegeman, C. E. Nucleic Acids Research, Vol. 33, Issue 5 https://doi.org/10.1093/nar/gki286	journal	March 2005
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Trapnell, Cole; Williams, Brian A.; Pertea, Geo Nature Biotechnology, Vol. 28, Issue 5 https://doi.org/10.1038/nbt.1621	journal	May 2010
PNPase activity determines the efficiency of mRNA 3'-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts Walter, M. The EMBO Journal, Vol. 21, Issue 24 https://doi.org/10.1093/emboj/cdf686	journal	December 2002
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Processing, degradation, and polyadenylation of chloroplast transcripts Bollenbach, Thomas J.; Schuster, Gadi; Portnoy, Victoria Cell and Molecular Biology of Plastids https://doi.org/10.1007/4735_2007_0235	book	January 2007
Translation and translational regulation in chloroplasts Peled-Zehavi, Hadas; Danon, Avihai Cell and Molecular Biology of Plastids https://doi.org/10.1007/4735_2007_0234	book	January 2007
Antisense Transcript and RNA Processing Alterations Suppress Instability of Polyadenylated mRNA in Chlamydomonas Chloroplasts Nishimura, Yoshiki; Kikis, Elise A.; Zimmer, Sara L. The Plant Cell, Vol. 16, Issue 11 https://doi.org/10.1105/tpc.104.026203	journal	October 2004
A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa) Wang, Lu; Yu, Xiang; Wang, Han BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-289	journal	June 2011
RNR1, a 3'-5' exoribonuclease belonging to the RNR superfamily, catalyzes 3' maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana Bollenbach, T. J. Nucleic Acids Research, Vol. 33, Issue 8 https://doi.org/10.1093/nar/gki576	journal	April 2005
The Challenge of Regulation in a Minimal Photoautotroph: Non-Coding RNAs in Prochlorococcus Steglich, Claudia; Futschik, Matthias E.; Lindell, Debbie PLoS Genetics, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pgen.1000173	journal	August 2008
Identification of small non-coding RNAs from mitochondria and chloroplasts Lung, Birgit; Zemann, Anja; Madej, Monika J. Nucleic Acids Research, Vol. 34, Issue 14 https://doi.org/10.1093/nar/gkl448	journal	August 2006
A subpopulation of spinach chloroplast tRNA genes does not require upstream promoter elements for transcription Gruissem, W.; Elsner-Menzel, C.; Latshaw, S. Nucleic Acids Research, Vol. 14, Issue 19 https://doi.org/10.1093/nar/14.19.7541	journal	January 1986
Plastid RNA Polymerases in Higher Plants Liere, Karsten; Maliga, Pal Regulation of Photosynthesis https://doi.org/10.1007/0-306-48148-0_2	book	January 2001
Sensitive detection of bacterial transcription initiation sites and differentiation from RNA processing sites in the pheromone-induced plasmid transfer system of Enterococcus faecalis. Bensing, B. A.; Meyer, B. J.; Dunny, G. M. Proceedings of the National Academy of Sciences, Vol. 93, Issue 15 https://doi.org/10.1073/pnas.93.15.7794	journal	July 1996
Characterization of plastid psb T sense and antisense RNAs Zghidi-Abouzid, Ouafa; Merendino, Livia; Buhr, Frank Nucleic Acids Research, Vol. 39, Issue 13 https://doi.org/10.1093/nar/gkr143	journal	March 2011
An Abundance of rna Regulators Storz, Gisela; Altuvia, Shoshy; Wassarman, Karen M. Annual Review of Biochemistry, Vol. 74, Issue 1 https://doi.org/10.1146/annurev.biochem.74.082803.133136	journal	June 2005
Overaccumulation of the chloroplast antisense RNA AS5 is correlated with decreased abundance of 5S rRNA in vivo and inefficient 5S rRNA maturation in vitro Sharwood, R. E.; Hotto, A. M.; Bollenbach, T. J. RNA, Vol. 17, Issue 2 https://doi.org/10.1261/rna.2336611	journal	December 2010
Improving RNA-Seq expression estimates by correcting for fragment bias Roberts, Adam; Trapnell, Cole; Donaghey, Julie Genome Biology, Vol. 12, Issue 3 https://doi.org/10.1186/gb-2011-12-3-r22	journal	January 2011
A long antisense RNA in plant chloroplasts: Rapid report Georg, J.; Honsel, A.; Voß, B. New Phytologist, Vol. 186, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03203.x	journal	February 2010
Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes. Gruissem, W.; Zurawski, G. The EMBO Journal, Vol. 4, Issue 13A https://doi.org/10.1002/j.1460-2075.1985.tb04093.x	journal	December 1985
Genomic sequencing. Church, G. M.; Gilbert, W. Proceedings of the National Academy of Sciences, Vol. 81, Issue 7 https://doi.org/10.1073/pnas.81.7.1991	journal	April 1984
Evidence for a major role of antisense RNAs in cyanobacterial gene regulation Georg, Jens; Voß, Björn; Scholz, Ingeborg Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.63	journal	January 2009
RNA-Seq: a revolutionary tool for transcriptomics Wang, Zhong; Gerstein, Mark; Snyder, Michael Nature Reviews Genetics, Vol. 10, Issue 1 https://doi.org/10.1038/nrg2484	journal	January 2009
Small RNA gene identification and mRNA target predictions in bacteria Pichon, C.; Felden, B. Bioinformatics, Vol. 24, Issue 24 https://doi.org/10.1093/bioinformatics/btn560	journal	October 2008
Natural antisense transcripts with coding capacity in Arabidopsismay have a regulatory role that is not linked to double-stranded RNA degradation Jen, Chih-Hung; Michalopoulos, Ioannis; Westhead, David R. Genome Biology, Vol. 6, Issue 6, p. R51 https://doi.org/10.1186/gb-2005-6-6-r51	journal	January 2005
RNA-quality control by the exosome Houseley, Jonathan; LaCava, John; Tollervey, David Nature Reviews Molecular Cell Biology, Vol. 7, Issue 7 https://doi.org/10.1038/nrm1964	journal	July 2006
Possible Involvement of the 5′-Flanking Region and the 5′UTR of Plastid accD Gene in NEP-Dependent Transcription Hirata, Norihiro; Yonekura, Daizou; Yanagisawa, Shuichi Plant and Cell Physiology, Vol. 45, Issue 2 https://doi.org/10.1093/pcp/pch021	journal	February 2004
Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription Stern, David B.; Gruissem, Wilhelm Cell, Vol. 51, Issue 6 https://doi.org/10.1016/0092-8674(87)90600-3	journal	December 1987
Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays Stead, Mark B.; Marshburn, Sarah; Mohanty, Bijoy K. Nucleic Acids Research, Vol. 39, Issue 8 https://doi.org/10.1093/nar/gkq1242	journal	December 2010
Characterization of the role of ribonucleases in Salmonella small RNA decay Viegas, Sandra C.; Pfeiffer, Verena; Sittka, Alexandra Nucleic Acids Research, Vol. 35, Issue 22 https://doi.org/10.1093/nar/gkm916	journal	November 2007
The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids Hajdukiewicz, Peter T. J.; Allison, Lori A.; Maliga, Pal The EMBO Journal, Vol. 16, Issue 13 https://doi.org/10.1093/emboj/16.13.4041	journal	July 1997
A 125 kDa RNase E/G-like protein is present in plastids and is essential for chloroplast development and autotrophic growth in Arabidopsis* Mudd, Elisabeth A.; Sullivan, Stuart; Gisby, Martin F. Journal of Experimental Botany, Vol. 59, Issue 10 https://doi.org/10.1093/jxb/ern126	journal	May 2008
Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1 Britton, Robert A.; Wen, Tingyi; Schaefer, Laura Molecular Microbiology, Vol. 63, Issue 1 https://doi.org/10.1111/j.1365-2958.2006.05499.x	journal	January 2007
Abnormal Physiological and Molecular Mutant Phenotypes Link Chloroplast Polynucleotide Phosphorylase to the Phosphorus Deprivation Response in Arabidopsis Marchive, Chloe; Yehudai-Resheff, Shlomit; Germain, Arnaud Plant Physiology, Vol. 151, Issue 2 https://doi.org/10.1104/pp.109.145144	journal	August 2009
High diversity of plastidial promoters in Arabidopsis thaliana Swiatecka-Hagenbruch, Monika; Liere, Karsten; Börner, Thomas Molecular Genetics and Genomics, Vol. 277, Issue 6 https://doi.org/10.1007/s00438-007-0222-4	journal	March 2007
Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis Lister, Ryan; O'Malley, Ronan C.; Tonti-Filippini, Julian Cell, Vol. 133, Issue 3 https://doi.org/10.1016/j.cell.2008.03.029	journal	May 2008
Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana Wang, Xiu-Jie; Gaasterland, Terry; Chua, Nam-Hai Genome Biology, Vol. 6, Issue 4, p. R30 https://doi.org/10.1186/gb-2005-6-4-r30	journal	January 2005
Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA Desnoyers, Guillaume; Morissette, Audrey; Prévost, Karine The EMBO Journal, Vol. 28, Issue 11 https://doi.org/10.1038/emboj.2009.116	journal	April 2009
Role of Bacillus subtilis RNase J1 Endonuclease and 5′-Exonuclease Activities in trp Leader RNA Turnover Deikus, Gintaras; Condon, Ciarán; Bechhofer, David H. Journal of Biological Chemistry, Vol. 283, Issue 25 https://doi.org/10.1074/jbc.M801461200	journal	June 2008
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 Germain, Arnaud; Herlich, Shira; Larom, Shirley The Plant Journal, Vol. 67, Issue 3 https://doi.org/10.1111/j.1365-313X.2011.04601.x	journal	May 2011
Relaxed Transcription in Arabidopsis Mitochondria Is Counterbalanced by RNA Stability Control Mediated by Polyadenylation and Polynucleotide Phosphorylase Holec, Sarah; Lange, Heike; Kühn, Kristina Molecular and Cellular Biology, Vol. 26, Issue 7 https://doi.org/10.1128/MCB.26.7.2869-2876.2006	journal	April 2006
Experimental RNomics Marker, Claudia; Zemann, Anja; Terhörst, Tanja Current Biology, Vol. 12, Issue 23 https://doi.org/10.1016/S0960-9822(02)01304-0	journal	December 2002
Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns: Time course study of short RNAs during fruit development Mohorianu, Irina; Schwach, Frank; Jing, Runchun The Plant Journal, Vol. 67, Issue 2 https://doi.org/10.1111/j.1365-313X.2011.04586.x	journal	May 2011
GadY, a Small-RNA Regulator of Acid Response Genes in Escherichia coli Opdyke, Jason A.; Kang, Ju-Gyeong; Storz, Gisela Journal of Bacteriology, Vol. 186, Issue 20 https://doi.org/10.1128/JB.186.20.6698-6705.2004	journal	October 2004
Small regulatory non-coding RNAs in bacteria: physiology and mechanistic aspects Repoila, Francis; Darfeuille, Fabien Biology of the Cell, Vol. 101, Issue 2 https://doi.org/10.1042/BC20070137	journal	February 2009
Sequence and transcriptional analysis of the barley ctDNA region upstream of psbD-psbC encoding trnK(UUU), rps16, trnQ(UUG), psbK, psbI, and trnS(GCU) Sexton, Tineke Berends; Jones, Jennifer T.; Mullet, John E. Current Genetics, Vol. 17, Issue 5 https://doi.org/10.1007/BF00334526	journal	May 1990
Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency: Functions of a chloroplast RNase E Walter, Michael; Piepenburg, Katrin; Schöttler, Mark Aurel The Plant Journal, Vol. 64, Issue 5 https://doi.org/10.1111/j.1365-313X.2010.04377.x	journal	October 2010
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 Yukawa, Maki; Kuroda, Hiroshi; Sugiura, Masahiro The Plant Journal, Vol. 49, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02948.x	journal	December 2006
Genomic sequencing Kahl, Gunter The Dictionary of Genomics, Transcriptomics and Proteomics https://doi.org/10.1002/9783527678679.dg05136	book	December 2015
SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation Zoch, Ansgar; Auchynnikava, Tania; Berrens, Rebecca V. Nature, Vol. 584, Issue 7822 https://doi.org/10.1038/s41586-020-2557-5	journal	July 2020
Genomic insight into diet adaptation in the biological control agent Cryptolaemus montrouzieri Li, Hao-Sen; Huang, Yu-Hao; Chen, Mei-Lan BMC Genomics, Vol. 22, Issue 1 https://doi.org/10.1186/s12864-021-07442-3	journal	February 2021
Genomic Sequencing Pfeifer, Gerd P.; Riggs, Arthur D. DNA Sequencing Protocols https://doi.org/10.1385/0-89603-248-5:169	book
Identification of the transcription start site for the spinach chloroplast serine tRNA gene Wu, Chih-Yu; Lin, Chi-Hui; Chen, Liang-Jwu FEBS Letters, Vol. 418, Issue 1-2 https://doi.org/10.1016/s0014-5793(97)01373-2	journal	November 1997
Correction: The Challenge of Regulation in a Minimal Photoautotroph: Non-Coding RNAs in Prochlorococcus Steglich, Claudia; Futschik, Matthias E.; Lindell, Debbie PLoS Genetics, Vol. 4, Issue 11 https://doi.org/10.1371/annotation/411b74ae-c4ce-43c9-bdd2-60c2bf60e672	journal	November 2008

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Title: Unexpected Diversity of Chloroplast Noncoding RNAs as Revealed by Deep Sequencing of the Arabidopsis Transcriptome

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