Participation of non-coding RNAs in plant organellar biogenesis

  • Michal Rurek Department of Cellular & Molecular Biology, Institute of Molecular Biology & Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznań, Umultowska 89, 61- 614 Poznań, Poland
Keywords: non-coding RNAs, chloroplast DNA, mitochondrial DNA, organellar gene expression, stress response

Abstract

The biogenesis of plant mitochondria and plastids is a multistep process that depends on the expression of both organellar and nuclear genes. A growing body of evidence suggest that the indispensable coordination between different steps of this process may be gained by the participation of non-coding RNAs. A plethora of non-coding RNAs of diverse length, both intraorganellar ones as well as encoded by the nuclear genome (including microRNAs and short interfering RNAs) were also suggested to play a role in stress response by regulating the expression levels of targeted genes important for the organellar biogenesis. Selected aspects of current interest, regarding the regulation of plant mitochondrial and plastid gene expression by diverse non-coding RNAs also under abiotic stress conditions, were highlighted.

Author Biography

Michal Rurek, Department of Cellular & Molecular Biology, Institute of Molecular Biology & Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznań, Umultowska 89, 61- 614 Poznań, Poland

Michal Rurek, D.Sc.

Assistant Professor

Department of Molecular and Cellular Biology

Institute of Molecular Biology and Biotechnology

Faculty of Biology

Adam Mickiewicz University in Poznań

References

Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283: 15932–15945. http://dx.doi.org/10.1074/jbc.M801406200

Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18: 758–762. http://dx.doi.org/10.1016/j.cub.2008.04.042

Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD (2011) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23: 2499–2513. http://dx.doi.org/10.1105/tpc.111.087189

Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70: 385–401. http://dx.doi.org/10.1007%2Fs11103-009-9480-3

Baev V, Milev I, Naydenov M, Vachev T, Apostolova E, Mehterov N, Gozmanva M, Minkov G, Sablok G, Yahubyan G (2014) Insight into small RNA abundance and expression in high- and low-temperature stress response using deep sequencing in Arabidopsis. Plant Physiol Biochem 84: 105–114. http://dx.doi.org/10.1016/j.plaphy.2014.09.007

Bandiera S, Rüberg S, Girard M, Cagnard N, Hanein S, Chrétien D, Munnich A, Lyonnet S, Henrion-Caude A (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6: e20746. http://dx.doi.org/10.1371/journal.pone.0020746

Billoud B, De Paepe R, Baulcombe D, Boccara M (2005) Identification of new small non-coding RNAs from tobacco and Arabidopsis. Biochimie 87: 905–910. http://dx.doi.org/ 10.1016/j.biochi.2005.06.001

Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu J-K (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123: 1279–1291. http://dx.doi.org/10.1016/j.cell.2005.11.035

Bouché N (2010) New insights into miR398 functions in Arabidopsis. Plant Signal Behav 5: 684–686. http://dx.doi.org/10.4161/psb.5.6.11573

Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185–1190. http://dx.doi.org/10.1126/science.1159151

Chen C-C, Fu S-F, Norikazu M, Yang Y-W, Liu Y-J, Ikeo K, Gojobori T, Huang H-J (2015) Comparative miRNAs analysis of two contrasting broccoli inbred lines with divergent head-forming capacity under temperature stress. BMC Genomics 16: 1026. http://dx.doi.org/10.1186/s12864-015-2201-1

Chen H, Zhang J, Yuan G, Liu C (2014) Complex interplay among DNA modification, noncoding RNA expression and protein-coding RNA expression in Salvia miltiorrhiza chloroplast genome. PLoS One 9: e99314. http://dx.doi.org/10.1371/journal.pone.0099314

Chen L, Ren Y, Zhang Y, Xu J, Zhang Z, Wang Y (2012) Genome-wide profiling of novel and conserved Populus microRNAs involved in pathogen stress response by deep sequencing. Planta 235: 873–883. http://dx.doi.org/10.1007/s00425-011-1548-z

Chevalier F, Ghulam MM, Rondet D, Pfannschmidt T, Merendino L, Lerbs-Mache S (2015) Characterization of the psbH precursor RNAs reveals a precise endoribonuclease cleavage site in the psbT/psbH intergenic region that is dependent on psbN gene expression. Plant Mol Biol 88: 357–367. http://dx.doi.org/10.1007/s11103-015-0325-y

Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30: 323–332. http://dx.doi.org/10.1111/j.1365-3040.2007.01643.x

Chou CH, Chang NW, Shrestha S, Hsu SD, Lin YL, Lee WH, Yang CD, Hong HC, Wei TY, Tu SJ, Tsai TR, Ho SY, Jian TY, Wu HY, Chen PR, Lin NC, Huang HT, Yang TL, Pai CY, Tai CS, Chen WL, Huang CY, Liu CC, Weng SL, Liao KW, Hsu WL, Huang HD (2016) miRTarBase 2016: updates to the experimentally validated miRNA-target interactions database. Nucl Acids Res 44: D239–D247. http://dx.doi.org/10.1093/nar/gkv1258

Confraria A, Martinho C, Elias A, Rubio-Somoza I, Baena-González E (2013) miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis. Front Plant Sci 4: 197. http://dx.doi.org/10.3389/fpls.2013.00197

Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucl Acids Res 39: W155–W159. http://dx.doi.org/10.1093/nar/gkr319

Das S, Ferlito M, Kent OA, Fox-Talbot K, Wang R, Liu D, Raghavachari N, Yang Y, Wheelan SJ, Murphy E, Steenbergen C (2012) Nuclear microRNA regulates the mitochondrial genome in the heart. Circ Res 110: 1596–1603. http://dx.doi.org/10.1161/CIRCRESAHA.112.267732

Desloire S, Gherbi H, Laloui W, Marhadour S, Clouet V, Cattolico L, Falentin C, Giancola S, Renard M, Budar F, Small I, Caboche M, Delourme R, Bendahmane A (2003) Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 4: 588–594. http://dx.doi.org/10.1038/sj.embor.embor848

Dietrich A, Wallet C, Iqbal RK, Gualberto JM, Lotfi F (2015) Organellar non-coding RNAs: emerging regulation mechanisms. Biochimie 117: 48–62. http://dx.doi.org/10.1016/j.biochi.2015.06.027

Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103: 29–38. http://dx.doi.org/10.1093/aob/mcn205

Ding X, Li J, Zhang H, He T, Han S, Li Y, Yang S, Gai J (2016) Identification of miRNAs and their targets by high-throughput sequencing and degradome analysis in cytoplasmic male-sterile line NJCMS1A and its maintainer NJCMS1B of soybean. BMC Genomics 17: 24. http://dx.doi.org/10.1186/s12864-015-2352-0

Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67: 403–417. http://dx.doi.org/10.1007/s11103-008-9329-1

Georg J, Honsel A, Voss B, Rennenberg H, Hess WR (2010) A long antisense RNA in plant chloroplasts. New Phytol 186: 615–622. http://dx.doi.org/10.1111/j.1469-8137.2010.03203.x

German MA, Pillay M, Jeong D-H, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers BC, Green PJ (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26: 941–946. http://dx.doi.org/10.1038/nbt1417

Gläßer C, Haberer G, Finkemeier I, Pfannschmidt T, Kleine T, Leister D, Dietz K-J, Häusler RE, Grimm B, Mayer KFX (2014) Meta-analysis of retrograde signaling in Arabidopsis thaliana reveals a core module of genes embedded in complex cellular signaling networks. Mol Plant 7: 1167–1190. http://dx.doi.org/10.1093/mp/ssu042

Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix JD (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65: 135–143. http://dx.doi.org/10.1016/0092-8674(91)90415-U

Gómez G, Pallás V (2010a) Noncoding RNA mediated traffic of foreign mRNA into chloroplasts reveals a novel signaling mechanism in plants. PLoS One 5: e12269. http://dx.doi.org/10.1371/journal.pone.0012269

Gómez G, Pallás V (2010b) Can the import of mRNA into chloroplasts be mediated by a secondary structure of a small non-coding RNA? Plant Signal Behav 5: 1517–1519. http://dx.doi.org/10.4161/psb.5.11.13711

Grant-Downton R, Le Trionnaire G, Schmid R, Rodriguez-Enriquez J, Hafidh S, Mehdi S, Twell D, Dickinson H (2009) MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 10: 643. http://dx.doi.org/10.1186/1471-2164-10-643

Grimes BT, Sisay AK, Carroll HD, Cahoon A (2014) Deep sequencing of the tobacco mitochondrial transcriptome reveals expressed ORFs and numerous editing sites outside coding regions. BMC Genomics 15: 31. http://dx.doi.org/10.1186/1471-2164-15-31

Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138: 226–237. http://dx.doi.org/10.1111/j.1399-3054.2009.01320.x

Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74: 840–851. http://dx.doi.org/10.1111/tpj.12169

Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148: 1055–1067. http://dx.doi.org/10.1104/pp.108.125237

Hackenberg M, Gustafson P, Langridge P, Shi B-J (2015) Differential expression of microRNAs and other small RNAs in barley between water and drought conditions. Plant Biotechnol J 13: 2–13. http://dx.doi.org/10.1111/pbi.12220

Higashi Y, Takechi K, Takano H, Takio S (2013) Involvement of microRNA in copper deficiency-induced repression of chloroplastic CuZn-superoxide dismutase genes in the moss Physcomitrella patens. Plant Cell Physiol 54: 1345–1355. http://dx.doi.org/10.1093/pcp/pct084

Holec S, Lange H, Kühn K, Alioua M, Börner T, Gagliardi D (2006) Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol Cell Biol 26: 2869–2876. http://dx.doi.org/10.1128/MCB.26.7.2869-2876.2006

Hotto AM, Huston ZE, Stern DB (2010) Overexpression of a natural chloroplast-encoded antisense RNA in tobacco destabilizes 5S rRNA and retards plant growth. BMC Plant Biol 10: 213. http://dx.doi.org/10.1186/1471-2229-10-213

Hotto AM, Schmitz RJ, Fei Z, Ecker JR, Stern DB, Kim JK (2011) Unexpected diversity of chloroplast noncoding RNAs as revealed by deep sequencing of the Arabidopsis transcriptome. Genes|Genomes|Genetics 1: 559–570. http://dx.doi.org/10.1534/g3.111.000752

Itaya A, Bundschuh R, Archual AJ, Joung J-G, Fei Z, Dai X, Zhao PX, Tang Y, Nelson RS, Ding B (2008) Small RNAs in tomato fruit and leaf development. Biochim Biophys Acta 1779: 99–107. http://dx.doi.org/10.1016/j.bbagrm.2007.09.003

Jacoby RP, Li L, Huang S, Pong Lee C, Millar AH, Taylor NL (2012) Mitochondrial composition, function and stress response in plants. J Integr Plant Biol 54: 887–906. http://dx.doi.org/10.1111/j.1744-7909.2012.01177.x

Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229: 1009–1014. http://dx.doi.org/10.1007/s00425-009-0889-3

Jia X, Wang W-X, Ren L, Chen Q-J, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71: 51–59. http://dx.doi.org/10.1007/s11103-009-9508-8

Jiang J, Lv M, Liang Y, Ma Z, Cao J (2014) Identification of novel and conserved miRNAs involved in pollen development in Brassica campestris ssp. chinensis by high-throughput sequencing and degradome analysis. BMC Genomics 15: 146. http://dx.doi.org/10.1186/1471-2164-15-146

Jin H, Vacic V, Girke T, Lonardi S, Zhu J-K (2008) Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis. BMC Mol Biol 9: 6. http://dx.doi.org/10.1186/1471-2199-9-6

Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787–799. http://dx.doi.org/10.1016/j.molcel.2004.05.027

Jovanović Ž, Stanisavljević N, Mikić A, Radović S, Maksimović V (2014) Water deficit down-regulates miR398 and miR408 in pea (Pisum sativum L.). Plant Physiol Biochem 83: 26–31. http://dx.doi.org/10.1016/j.plaphy.2014.07.008

Juszczak I, Baier M (2012) The strength of the miR398-Csd2-CCS1 regulon is subject to natural variation in Arabidopsis thaliana. FEBS Lett 586: 3385–3390. http://dx.doi.org/10.1016/j.febslet.2012.07.049

Kotakis C (2015) Non-coding RNAs’ partitioning in the evolution of photosynthetic organisms via energy transduction and redox signaling. RNA Biol 12: 101–104. http://dx.doi.org/10.1080/15476286.2015.1017201

Leung AKL (2015) The whereabouts of microRNA actions: cytoplasm and beyond. Trends Cell Biol 25: 601–610. http://dx.doi.org/10.1016/j.tcb.2015.07.005

Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62: 3765–3779. http://dx.doi.org/10.1093/jxb/err051

Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci Rep 5: 11813. http://dx.doi.org/10.1038/srep11813

Liu H-H, Tian X, Li Y-J, Wu C-A, Zheng C-C (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836–843. http://dx.doi.org/10.1261/rna.895308

Liu T-T, Zhu D, Chen W, Deng W, He H, He G, Bai B, Qi Y, Chen R, Deng XW (2013) A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol Plant 6: 830–846. http://dx.doi.org/10.1093/mp/sss087

Lu S, Sun Y-H, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55: 131–151. http://dx.doi.org/10.1111/j.1365-313X.2008.03497.x

Lu S, Sun Y-H, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17: 2186–2203. http://dx.doi.org/10.1105/tpc.105.033456

Lu X, Guan Q, Zhu J (2013) Downregulation of CSD2 by a heat-inducible miR398 is required for thermotolerance in Arabidopsis. Plant Signal Behav 8: pii: e24952. http://dx.doi.org/10.4161/psb.24952

Lung B, Zemann A, Madej MJ, Schuelke M, Techritz S, Rut S, Bock R, Hüttenhofer A (2006) Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucleic Acids Res 34: 3842–3852. http://dx.doi.org/10.1093/nar/gkl448

Ma C, Burd S, Lers A (2015) miR408 is involved in abiotic stress responses in Arabidopsis. Plant J 84: 169–187. http://dx.doi.org/10.1111/tpj.12999

Marker C, Zemann A, Terhörst T, Kiefmann M, Kastenmayer JP, Green P, Bachellerie J-P, Brosius J, Hüttenhofer A (2002) Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana. Curr Biol 12: 2002–2013. http://dx.doi.org/10.1016/S0960-9822(02)01304-0

Matsui A, Nguyen AH, Nakaminami K, Seki M (2013) Arabidopsis non-coding RNA regulation in abiotic stress responses. Int J Mol Sci 14: 22642–22654. http://dx.doi.org/10.3390/ijms141122642

Mileshina D, Niazi AK, Wyszko E, Szymanski M, Val R, Valentin C, Barciszewski J, Dietrich A (2015) Mitochondrial targeting of catalytic RNAs. Methods Mol Biol 1265: 227–254. http://dx.doi.org/10.1007/978-1-4939-2288-8_17

Mohorianu I, Schwach F, Jing R, Lopez-Gomollon S, Moxon S, Szittya G, Sorefan K, Moulton V, Dalmay T (2011) Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns. Plant J 67: 232–246. http://dx.doi.org/ 10.1111/j.1365-313X.2011.04586.x

Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2010) Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61: 165–177. http://dx.doi.org/10.1093/jxb/erp296

Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, Sahinalp SC, Unrau PJ (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18: 571–584. http://dx.doi.org/10.1101/gr.6897308

Nishimura Y, Kikis EA, Zimmer SL, Komine Y, Stern DB (2004) Antisense transcript and RNA processing alterations suppress instability of polyadenylated mRNA in Chlamydomonas chloroplasts. Plant Cell 16: 2849–2869. http://dx.doi.org/10.1105/tpc.104.026203

Park YJ, Lee HJ, Kwak KJ, Lee K, Hong SW, Kang H (2014) MicroRNA400-guided cleavage of pentatricopeptide repeat protein mRNAs renders Arabidopsis thaliana more susceptible to pathogenic bacteria and fungi. Plant Cell Physiol 55: 1660–1668. http://dx.doi.org/10.1093/pcp/pcu096

Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, Liu Y, Wu Y, Jiang D (2012) OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytol 193: 109–120. http://dx.doi.org/10.1111/j.1469-8137.2011.03910.x

Qiu Y, Filipenko SJ, Darracq A, Adams KL (2014) Expression of a transferred nuclear gene in a mitochondrial genome. Curr Plant Biol 1: 6–10. http://dx.doi.org/10.1016/j.cpb.2014.08.002

Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20: 3407–3425. http://dx.doi.org/10.1101/gad.1476406

Ro S, Ma H-Y, Park C, Ortogero N, Song R, Hennig GW, Zheng H, Lin Y-M, Moro L, Hsieh J-T, Yan W (2013) The mitochondrial genome encodes abundant small noncoding RNAs. Cell Res 23: 759–774. http://dx.doi.org/10.1038/cr.2013.37

Rurek M (2014) Plant mitochondria under a variety of temperature stress conditions. Mitochondrion 19: 289–294. http://dx.doi.org/10.1016/j.mito.2014.02.007

Ruwe H, Schmitz-Linneweber C (2012) Short non-coding RNA fragments accumulating in chloroplasts: footprints of RNA binding proteins? Nucl Acids Res 40: 3106–3116. http://dx.doi.org/10.1093/nar/gkr1138

Sharwood RE, Halpert M, Luro S, Schuster G, Stern DB (2011a) Chloroplast RNase J compensates for inefficient transcription termination by removal of antisense RNA. RNA 17: 2165–2176. http://dx.doi.org/10.1261/rna.028043.111

Sharwood RE, Hotto AM, Bollenbach TJ, Stern DB (2011b) Overaccumulation of the chloroplast antisense RNA AS5 is correlated with decreased abundance of 5S rRNA in vivo and inefficient 5S rRNA maturation in vitro. RNA 17: 230–243. http://dx.doi.org/10.1261/rna.2336611

Shuai P, Liang D, Zhang Z, Yin W, Xia X (2013) Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genomics 14: 233. http://dx.doi.org/10.1186/1471-2164-14-233

Stoll B, Zendler D, Binder S (2014) RNA processing factor 7 and polynucleotide phosphorylase are necessary for processing and stability of nad2 mRNA in Arabidopsis mitochondria. RNA Biol 11: 968–976. http://dx.doi.org/10.4161/rna.29781

Sugita M, Svab Z, Maliga P, Sugiura M (1997) Targeted deletion of sprA from the tobacco plastid genome indicates that the encoded small RNA is not essential for pre-16S rRNA maturation in plastids. Mol Gen Genet 257: 23–27.

Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18: 2051–2065. http://dx.doi.org/10.1105/tpc.106.041673

Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17: 196–203. http://dx.doi.org/10.1016/j.tplants.2012.01.010

Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001–2019. http://dx.doi.org/10.1105/tpc.104.022830

Taylor NL, Tan Y-F, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteomics 72: 367–378. http://dx.doi.org/10.1016/j.jprot.2008.11.006

Trindade I, Capitão C, Dalmay T, Fevereiro MP, Santos DMD (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231: 705–716. http://dx.doi.org/10.1007/s00425-009-1078-0

Val R, Wyszko E, Valentin C, Szymanski M, Cosset A, Alioua M, Dreher TW, Barciszewski J, Dietrich A (2011) Organelle trafficking of chimeric ribozymes and genetic manipulation of mitochondria. Nucl Acids Res 39: 9262–9274. http://dx.doi.org/10.1093/nar/gkr580

Vera A, Sugiura M (1994) A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16S rRNA. EMBO J 13: 2211–2217.

Wang L, Yu X, Wang H, Lu Y-Z, de Ruiter M, Prins M, He Y-K (2011) A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa). BMC Genomics 12: 289. http://dx.doi.org/10.1186/1471-2164-12-289

Wang Y, Wang X, Deng W, Fan X, Liu T-T, He G, Chen R, Terzaghi W, Zhu D, Deng XW (2014) Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol Plant 7: 514–527. http://dx.doi.org/10.1093/mp/sst177

Wei X, Zhang X, Yao Q, Yuan Y, Li X, Wei F, Zhao Y, Zhang Q, Wang Z, Jiang W, Zhang X (2015) The miRNAs and their regulatory networks responsible for pollen abortion in Ogura-CMS Chinese cabbage revealed by high-throughput sequencing of miRNAs, degradomes, and transcriptomes. Front Plant Sci 6: 894. http://dx.doi.org/10.3389/fpls.2015.00894

Wu C-Y, Li Q-Z, Feng Z-X (2016) Non-coding RNA identification based on topology secondary structure and reading frame in organelle genome level. Genomics 107: 9–15. http://dx.doi.org/ 10.1016/j.ygeno.2015.12.002

Wu Z, Stone JD, Štorchová H, Sloan DB (2015) High transcript abundance, RNA editing, and small RNAs in intergenic regions within the massive mitochondrial genome of the angiosperm Silene noctiflora. BMC Genomics 16: 938. http://dx.doi.org/10.1186/s12864-015-2155-3

Xie F, Stewart CN, Taki FA, He Q, Liu H, Zhang B (2014) High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol J 12: 354–366. http://dx.doi.org/10.1111/pbi.12142

Xu P, Mohorianu I, Yang L, Zhao H, Gao Z, Dalmay T (2014) Small RNA profile in moso bamboo root and leaf obtained by high definition adapters. PLoS One 9: e103590. http://dx.doi.org/ 10.1371/journal.pone.0103590

Xu Z, Zhong S, Li X, Li W, Rothstein SJ, Zhang S, Bi Y, Xie C (2011) Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. PLoS One 6: e28009. http://dx.doi.org/10.1371/journal.pone.0028009

Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282: 16369–16378. http://dx.doi.org/10.1074/jbc.M700138200

Yan K, Liu P, Wu C-A, Yang G-D, Xu R, Guo Q-H, Huang J-G, Zheng C-C (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48: 521–531. http://dx.doi.org/10.1016/j.molcel.2012.08.032

Yang J, Liu X, Xu B, Zhao N, Yang X, Zhang M (2013) Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of Brassica juncea. BMC Genomics 14: 9. http://dx.doi.org/10.1186/1471-2164-14-9

Yi X, Zhang Z, Ling Y, Xu W, Su Z (2015) PNRD: a plant non-coding RNA database. Nucl Acids Res 43: D982–D989. http://dx.doi.org/10.1093/nar/gku1162

Yu X, Yang J, Li X, Liu X, Sun C, Wu F, He Y (2013) Global analysis of cis-natural antisense transcripts and their heat-responsive nat-siRNAs in Brassica rapa. BMC Plant Biol 13: 208. http://dx.doi.org/10.1186/1471-2229-13-208

Yuan C, Wang J, Harrison AP, Meng X, Chen D, Chen M (2015) Genome-wide view of natural antisense transcripts in Arabidopsis thaliana. DNA Res 22: 233–243. http://dx.doi.org/10.1093/dnares/dsv008

Zghidi-Abouzid O, Merendino L, Buhr F, Malik Ghulam M, Lerbs-Mache S (2011) Characterization of plastid psbT sense and antisense RNAs. Nucl Acids Res 39: 5379–5387. http://dx.doi.org/ 10.1093/nar/gkr143

Zhang H, He H, Wang X, Wang X, Yang X, Li L, Deng XW (2011) Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65: 346–358. http://dx.doi.org/10.1111/j.1365-313X.2010.04426.x

Zhang X, Lii Y, Wu Z, Polishko A, Zhang H, Chinnusamy V, Lonardi S, Zhu J-K, Liu R, Jin H (2013) Mechanisms of small RNA generation from cis-NATs in response to environmental and developmental cues. Mol Plant 6: 704–715. http://dx.doi.org/10.1093/mp/sst051

Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y, Huang J, Zhao X, Zhou J, Yan Y, et al. (2014) MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158: 607–619. http://dx.doi.org/10.1016/j.cell.2014.05.047

Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot 102: 509–519. http://dx.doi.org/10.1093/aob/mcn129

Zhelyazkova P, Sharma CM, Förstner KU, Liere K, Vogel J, Börner T (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24: 123–136. http://dx.doi.org/ 10.1105/tpc.111.089441

Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61: 4157–4168. http://dx.doi.org/ 10.1093/jxb/erq237

Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3: 103. http://dx.doi.org/10.1038/msb4100143

Published
2017-03-04