The Role of Non-Coding RNAs in Cytoplasmic Male Sterility in Flowering Plants

. 2017 Nov 16 ; 18 (11) : . [epub] 20171116

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid29144434

The interactions between mitochondria and nucleus substantially influence plant development, stress response and morphological features. The prominent example of a mitochondrial-nuclear interaction is cytoplasmic male sterility (CMS), when plants produce aborted anthers or inviable pollen. The genes responsible for CMS are located in mitochondrial genome, but their expression is controlled by nuclear genes, called fertility restorers. Recent explosion of high-throughput sequencing methods enabled to study transcriptomic alterations in the level of non-coding RNAs under CMS biogenesis. We summarize current knowledge of the role of nucleus encoded regulatory non-coding RNAs (long non-coding RNA, microRNA as well as small interfering RNA) in CMS. We also focus on the emerging data of non-coding RNAs encoded by mitochondrial genome and their possible involvement in mitochondrial-nuclear interactions and CMS development.

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Tester M., Langridge P. Breeding technologies to increase crop production in a changing world. Science. 2010;327:818–822. doi: 10.1126/science.1183700. PubMed DOI

Vendramin R., Marine J.C., Leucci E. Non-coding RNAs: The dark side of nuclear-mitochondrial communication. EMBO J. 2017;36:1123–1133. doi: 10.15252/embj.201695546. PubMed DOI PMC

Horn R., Gupta K.J., Colombo N. Mitochondrion role in molecular basis of cytoplasmic male sterility. Mitochondrion. 2014;19:198–205. doi: 10.1016/j.mito.2014.04.004. PubMed DOI

Touzet P., Meyer E.H. Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion. 2014;19:166–171. doi: 10.1016/j.mito.2014.04.009. PubMed DOI

Hanson M.R., Bentolila S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell. 2004;16:S154–S169. doi: 10.1105/tpc.015966. PubMed DOI PMC

Gillman J.D., Bentolila S., Hanson M.R. The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS-associated locus. Plant J. 2007;49:217–227. doi: 10.1111/j.1365-313X.2006.02953.x. PubMed DOI

Kim D.H., Kang J.G., Kim B.D. Isolation and characterization of the cytoplasmic male sterility-associated orf456 gene of chili pepper (Capsicum annuum L.) Plant Mol. Biol. 2007;63:519–532. doi: 10.1007/s11103-006-9106-y. PubMed DOI

Duroc Y., Hiard S., Vrielynck N., Ragu S., Budar F. The Ogura sterility-inducing protein forms a large complex without interfering with the oxidative phosphorylation components in rapeseed mitochondria. Plant Mol. Biol. 2009;70:123–137. doi: 10.1007/s11103-009-9461-6. PubMed DOI

Dewey R.E., Timothy D.H., Levings C.S. A mitochondrial protein associated with cytoplasmic male-sterility in the T-cytoplasm of maize. Proc. Natl. Acad. Sci. USA. 1987;84:5374–5378. doi: 10.1073/pnas.84.15.5374. PubMed DOI PMC

Ducos E., Touzet P., Boutry M. The male sterile G cytoplasm of wild beet displays modified mitochondrial respiratory complexes. Plant J. 2001;26:171–180. doi: 10.1046/j.1365-313x.2001.01017.x. PubMed DOI

Itabashi E., Kazama T., Toriyama K. Characterization of cytoplasmic male sterility of rice with Lead Rice cytoplasm in comparison with that with Chinsurah Boro II cytoplasm. Plant Cell Rep. 2009;28:233–239. doi: 10.1007/s00299-008-0625-7. PubMed DOI

Wang K., Gao F., Ji Y.X., Liu Y., Dan Z.W., Yang P.F., Zhu Y.G., Li S.Q. ORFH79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice. New Phytol. 2013;198:408–418. doi: 10.1111/nph.12180. PubMed DOI

Zabala G., Gabay-Laughnan S., Laughnan J.R. The nuclear gene Rf3 affects the expression of the mitochondrial chimeric sequence R implicated in S-type male sterility in maize. Genetics. 1997;147:847–860. PubMed PMC

Yamamoto M.P., Kubo T., Mikami T. The 5′-leader sequence of sugar beet mitochondrial atp6 encodes a novel polypeptide that is characteristic of Owen cytoplasmic male sterility. Mol. Genet. Genom. 2005;273:342–349. doi: 10.1007/s00438-005-1140-y. PubMed DOI

Grelon M., Budar F., Bonhomme S., Pelletier G. Ogura cytoplasmic male sterility (CMS)-associated ORF138 is translated into a mitochondrial-membrane polypeptide in male-sterile Brassica cybrids. Mol. Gen. Genet. 1994;243:540–547. doi: 10.1007/BF00284202. PubMed DOI

Kazama T., Itabashi E., Fujii S., Nakamura T., Toriyama K. Mitochondrial ORF79 levels determine pollen abortion in cytoplasmic male sterile rice. Plant J. 2016;85:707–716. doi: 10.1111/tpj.13135. PubMed DOI

Balk J., Leaver C.J. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell. 2001;13:1803–1818. doi: 10.1105/tpc.13.8.1803. PubMed DOI PMC

Twell D. Male gametogenesis and germline specification in flowering plants. Sex. Plant Reprod. 2011;24:149–160. doi: 10.1007/s00497-010-0157-5. PubMed DOI

Luo D.P., Xu H., Liu Z.L., Guo J.X., Li H.Y., Chen L.T., Fang C., Zhang Q.Y., Bai M., Yao N., et al. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat. Genet. 2013;45:573–577. doi: 10.1038/ng.2570. PubMed DOI

Shafiq S., Li J.R., Sun Q.W. Functions of plants long non-coding RNAs. Biochim. Biophys. Acta. 2016;1859:155–162. doi: 10.1016/j.bbagrm.2015.06.009. PubMed DOI

Schnable P.S., Wise R.P. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci. 1998;3:175–180. doi: 10.1016/S1360-1385(98)01235-7. DOI

Sabar M., Gagliardi D., Balk J., Leaver C.J. ORFB is a subunit of F1FO-ATP synthase: Insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep. 2003;4:381–386. doi: 10.1038/sj.embor.embor800. PubMed DOI PMC

Kazama T., Nakamura T., Watanabe M., Sugita M., Toriyama K. Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J. 2008;55:619–628. doi: 10.1111/j.1365-313X.2008.03529.x. PubMed DOI

Chakraborty A., Mitra J., Bhattacharyya J., Pradhan S., Sikdar N., Das S., Chakraborty S., Kumar S., Lakhanpaul S., Sen S.K. Transgenic expression of an unedited mitochondrial orfB gene product from wild abortive (WA) cytoplasm of rice (Oryza sativa L.) generates male sterility in fertile rice lines. Planta. 2015;241:1463–1479. doi: 10.1007/s00425-015-2269-5. PubMed DOI

Uyttewaal M., Arnal N., Quadrado M., Martin-Canadell A., Vrielynck N., Hiard S., Gherbi H., Bendahmane A., Budar F., Mireau H. Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for Ogura cytoplasmic male sterility. Plant Cell. 2008;20:3331–3345. doi: 10.1105/tpc.107.057208. PubMed DOI PMC

Sarria R., Lyznik A., Vallejos C.E., Mackenzie S.A. A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell. 1998;10:1217–1228. doi: 10.2307/3870723. PubMed DOI PMC

Gaborieau L., Brown G.G., Mireau H. The propensity of pentatricopeptide repeat genes to evolve into restorers of cytoplasmic male sterility. Front. Plant Sci. 2016;7:1816. doi: 10.3389/fpls.2016.01816. PubMed DOI PMC

Takenaka M., Zehrmann A., Verbitskiy D., Haertel B., Brennicke A. RNA Editing in plants and its evolution. Annu. Rev. Genet. 2013;47:335–352. doi: 10.1146/annurev-genet-111212-133519. PubMed DOI

Fujii S., Bond C.S., Small I.D. Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl. Acad. Sci. USA. 2011;108:1723–1728. doi: 10.1073/pnas.1007667108. PubMed DOI PMC

Melonek J., Stone J.D., Small I. Evolutionary plasticity of restorer-of-fertility-like proteins in rice. Sci. Rep. 2016;6:35152. doi: 10.1038/srep35152. PubMed DOI PMC

Gouyon P.H., Couvet D. A conflict between two sexes, females and hermaphrodites. In: Stearns S.C., editor. The Evolution of Sex and Its Consequences. Birkhauser Verlag; Basel, Switzerland: 1987. pp. 245–261. PubMed

Cui X., Wise R.P., Schnable P.S. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science. 1996;272:1334–1336. doi: 10.1126/science.272.5266.1334. PubMed DOI

Liu F., Cui X., Horner H.T., Weiner H., Schnable P.S. Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell. 2001;13:1063–1078. doi: 10.1105/tpc.13.5.1063. PubMed DOI PMC

Fujii S., Toriyama K. Suppressed expression of RETROGRADE-REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. Proc. Natl. Acad. Sci. USA. 2009;106:9513–9518. doi: 10.1073/pnas.0901860106. PubMed DOI PMC

McCauley D.E., Olson M.S. Do recent findings in plant mitochondrial molecular and population genetics have implications for the study of gynodioecy and cytonuclear conflict? Evolution. 2008;62:1013–1025. doi: 10.1111/j.1558-5646.2008.00363.x. PubMed DOI

Case A.L., Willis J.H. Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution. 2008;62:1026–1039. doi: 10.1111/j.1558-5646.2008.00360.x. PubMed DOI

Darracq A., Varré J.S., Marechal-Drouard L., Courseaux A., Castric V., Saumitou-Laprade P., Oztas S., Lenoble P., Vacherie B., Barbe V., et al. Structural and content diversity of mitochondrial genome in beet: A comparative genomic analysis. Genome Biol. Evol. 2011;3:723–736. doi: 10.1093/gbe/evr042. PubMed DOI PMC

Mower J.P., Case A.L., Floro E.R., Willis J.H. Evidence against equimolarity of large repeat arrangements and a predominant master circle structure of the mitochondrial genome from a monkeyflower (Mimulus guttatus) lineage with cryptic CMS. Genome Biol. Evol. 2012;4:670–686. doi: 10.1093/gbe/evs042. PubMed DOI PMC

Štorchová H., Müller K., Lau S., Olson M.S. Mosaic origin of a complex chimeric mitochondrial gene in Silene vulgaris. PLoS ONE. 2012;7:e30401. doi: 10.1371/journal.pone.0030401. PubMed DOI PMC

Song J.H., Yang J., Pan F., Jin B. Differential expression of microRNAs may regulate pollen development in Brassica oleracea. Genet. Mol. Res. 2015;14:15024–15034. doi: 10.4238/2015.November.24.10. PubMed DOI

Stone J.D., Štorchová H. The application of RNA-seq to the comprehensive analysis of plant mitochondrial transcriptomes. Mol. Genet. Genom. 2015;290:1–9. doi: 10.1007/s00438-014-0905-6. PubMed DOI

Yan J.J., Zhang H.Y., Zheng Y.Z., Ding Y. Comparative expression profiling of miRNAs between the cytoplasmic male sterile line MeixiangA and its maintainer line MeixiangB during rice anther development. Planta. 2015;241:109–123. doi: 10.1007/s00425-014-2167-2. PubMed DOI

Zhang W., Xie Y., Xu L., Wang Y., Zhu X.W., Wang R.H., Zhang Y., Muleke E.M., Liu L.W. Identification of microRNAs and Their Target Genes Explores miRNA-Mediated Regulatory Network of Cytoplasmic Male Sterility Occurrence during Anther Development in Radish (Raphanus sativus L.) Front. Plant Sci. 2016;7:1054. doi: 10.3389/fpls.2016.01054. PubMed DOI PMC

Liu T.K., Li Y., Zhang C.W., Duan W.K., Huang F.Y., Hou X.L. Basic helix-loop-helix transcription factor BcbHLHpol functions as a positive regulator of pollen development in non-heading Chinese cabbage. Funct. Integr. Genom. 2014;14:731–739. doi: 10.1007/s10142-014-0390-3. PubMed DOI

Li Y.W., Ding X.L., Wang X., He T.T., Zhang H., Yang L.S., Wang T.L., Chen L.F., Gai J.Y., Yang S.P. Genome-wide comparative analysis of DNA methylation between soybean cytoplasmic male-sterile line NJCMS5A and its maintainer NJCMS5B. BMC Genom. 2017;18:596. doi: 10.1186/s12864-017-3962-5. PubMed DOI PMC

Guttman M., Rinn J.L. Modular regulatory principles of large non-coding RNAs. Nature. 2012;482:339–346. doi: 10.1038/nature10887. PubMed DOI PMC

Achkar N.P., Cambiagno D.A., Manavella P.A. miRNA biogenesis: A dynamic pathway. Trends Plant Sci. 2016;21:1034–1044. doi: 10.1016/j.tplants.2016.09.003. PubMed DOI

Li S.J., Castillo-Gonzalez C., Yu B., Zhang X.R. The functions of plant small RNAs in development and in stress responses. Plant J. 2017;90:654–670. doi: 10.1111/tpj.13444. PubMed DOI

Hamilton A., Voinnet O., Chappell L., Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J. 2002;21:4671–4679. doi: 10.1093/emboj/cdf464. PubMed DOI PMC

Zilberman D., Cao X.F., Jacobsen S.E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 2003;299:716–719. doi: 10.1126/science.1079695. PubMed DOI

Burkhart K.B., Guang S., Buckley B.A., Wong L., Bochner A.F., Kennedy S. A pre-mRNA-associating factor links endogenous siRNAs to chromatin regulation. PLoS Genet. 2011;7:e1002249. doi: 10.1371/journal.pgen.1002249. PubMed DOI PMC

MacLean D., Elina N., Havecker E.R., Heimstaedt S.B., Studholme D.J., Baulcombe D.C. Evidence for Large Complex Networks of Plant Short Silencing RNAs. PLoS ONE. 2010;5:e9901. doi: 10.1371/journal.pone.0009901. PubMed DOI PMC

Kamthan A., Chaudhuri A., Kamthan M., Datta A. Small RNAs in plants: Recent development and application for crop improvement. Front. Plant Sci. 2015;6:208. doi: 10.3389/fpls.2015.00208. PubMed DOI PMC

Rogers K., Chen X.M. Biogenesis, Turnover, and Mode of Action of Plant MicroRNAs. Plant Cell. 2013;25:2383–2399. doi: 10.1105/tpc.113.113159. PubMed DOI PMC

Cui J., You C.J., Chen X.M. The evolution of microRNAs in plants. Curr. Opin. Plant Biol. 2017;35:61–67. doi: 10.1016/j.pbi.2016.11.006. PubMed DOI PMC

Li H., Wang Y., Wu M., Li L.H., Jin C., Zhang Q.L., Chen C.B., Song W.Q., Wang C.G. Small RNA Sequencing Reveals Differential miRNA Expression in the Early Development of Broccoli (Brassica oleracea var. italica) Pollen. Front. Plant Sci. 2017;8:404. doi: 10.3389/fpls.2017.00404. PubMed DOI PMC

Yang J.H., Liu X.Y., Xu B.C., Zhao N., Yang X.D., Zhang M.F. 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 Genom. 2013;14:9. doi: 10.1186/1471-2164-14-9. PubMed DOI PMC

Fang Y.N., Zheng B.B., Wang L., Wu X.M., Xu Q., Guo W.W. High-throughput sequencing and degradome analysis reveal altered expression of miRNAs and their targets in a male-sterile cybrid pummelo (Citrus grandis) BMC Genom. 2016;17:591. doi: 10.1186/s12864-016-2882-0. PubMed DOI PMC

Wei X.C., Zhang X.H., Yao Q.J., Yuan Y.X., Li X.X., We F., Zhao Y.Y., Zhang Q., Wang Z.Y., Jiang W.S., et al. 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. 2015;6:894. doi: 10.3389/fpls.2015.00894. PubMed DOI PMC

Ding X.L., Li J.J., Zhang H., He T.T., Han S.H., Li Y.W., Yang S.P., Gai J.Y. 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 Genom. 2016;17:24. doi: 10.1186/s12864-015-2352-0. PubMed DOI PMC

Shen Y., Zhang Z.M., Lin H.J., Liu H.J., Chen J., Peng H., Cao M.J., Rong T.Z., Pan G.T. Cytoplasmic male sterility-regulated novel microRNAs from maize. Funct. Integr. Genom. 2011;11:179–191. doi: 10.1007/s10142-010-0202-3. PubMed DOI

Li J.J., Han S.H., Ding X.L., He T.T., Dai J.Y., Yang S.P., Gai J.Y. Comparative Transcriptome Analysis between the Cytoplasmic Male Sterile Line NJCMS1A and Its Maintainer NJCMS1B in Soybean (Glycine max (L.) Merr.) PLoS ONE. 2015;10:e0126771. doi: 10.1371/journal.pone.0126771. PubMed DOI PMC

Li J.J., Yang S.P., Gai J.Y. Transcriptome comparative analysis between the cytoplasmic male sterile line and fertile line in soybean (Glycine max (L.) Merr.) Genes Genom. 2017;39:1117–1127. doi: 10.1007/s13258-017-0578-8. DOI

Ng S., Ivanova A., Duncan O., Law S.R., van Aken O., de Clercq I., Wang Y., Carrie C., Xu L., Kmiec B., et al. A membrane-Bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell. 2013;25:3450–3471. doi: 10.1105/tpc.113.113985. PubMed DOI PMC

Van Aken O., Ford E., Lister R., Huang S.B., Millar A.H. Retrograde signalling caused by heritable mitochondrial dysfunction is partially mediated by ANAC017 and improves plant performance. Plant J. 2016;88:542–558. doi: 10.1111/tpj.13276. PubMed DOI

Castel S.E., Martienssen R.A. RNA interference in the nucleus: Roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 2013;14:100–112. doi: 10.1038/nrg3355. PubMed DOI PMC

Allen E., Xie Z.X., Gustafson A.M., Carrington J.C. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell. 2005;121:207–221. doi: 10.1016/j.cell.2005.04.004. PubMed DOI

Yoshikawa M., Peragine A., Park M.Y., Poethig R.S. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 2005;19:2164–2175. doi: 10.1101/gad.1352605. PubMed DOI PMC

Howell M.D., Fahlgren N., Chapman E.J., Cumbie J.S., Sullivan C.M., Givan S.A., Kasschau K.D., Carrington J.C. Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. Plant Cell. 2007;19:926–942. doi: 10.1105/tpc.107.050062. PubMed DOI PMC

Xia R., Meyers B.C., Liu Z.C., Beers E.P., Ye S.Q., Liu Z.R. MicroRNA Superfamilies Descended from miR390 and Their Roles in Secondary Small Interfering RNA Biogenesis in Eudicots. Plant Cell. 2013;25:1555–1572. doi: 10.1105/tpc.113.110957. PubMed DOI PMC

Heo J.B., Lee Y.S. Molecular functions of long noncoding transcripts in plants. J. Plant Biol. 2015;58:361–365. doi: 10.1007/s12374-015-0476-z. DOI

Liu J., Wang H., Chua N.H. Long noncoding RNA transcriptome of plants. Plant Biotechnol. J. 2015;13:319–328. doi: 10.1111/pbi.12336. PubMed DOI

Lu T., Zhu C., Lu G., Guo Y., Zhou Y., Zhang Z., Zhao Y., Li W., Lu Y., Tang W., et al. Strand-specific RNA-seq reveals widespread occurrence of novel cis-natural antisense transcripts in rice. BMC Genom. 2012;13:721. doi: 10.1186/1471-2164-13-721. PubMed DOI PMC

Wu X.H., Liu M., Downie B., Liang C., Ji G., Li Q.Q., Hunt A.G. Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation. Proc. Natl. Acad. Sci. USA. 2011;108:12533–12538. doi: 10.1073/pnas.1019732108. PubMed DOI PMC

Wang Y., Wang X., Deng W., Fan X., Liu T.T., He G., Chen R., Terzaghi W., Zhu D., Deng X.W. Genomic Features and Regulatory Roles of Intermediate-Sized Non-Coding RNAs in Arabidopsis. Mol. Plant. 2014;7:514–527. doi: 10.1093/mp/sst177. PubMed DOI

Swiezewski S., Liu F., Magusin A., Dean C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature. 2009;462:799–802. doi: 10.1038/nature08618. PubMed DOI

Bardou F., Ariel F., Simpson C.G., Romero-Barrios N., Laporte P., Balzergue S., Brown J.W.S., Crespi M. Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev. Cell. 2014;30:166–176. doi: 10.1016/j.devcel.2014.06.017. PubMed DOI

Heo J.B., Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science. 2011;331:76–79. doi: 10.1126/science.1197349. PubMed DOI

Ma J.X., Yan B.X., Qu Y.Y., Qin F.F., Yang Y.T., Hao X.J., Yu J.J., Zhao Q., Zhu D.Y., Ao G.M. Zm401, a short-open reading-frame mRNA or noncoding RNA, is essential for tapetum and microspore development and can regulate the floret formation in maize. J. Cell Biochem. 2008;105:136–145. doi: 10.1002/jcb.21807. PubMed DOI

Wang M., Wu H.J., Fang J., Chu C.C., Wang X.J. A long noncoding RNA involved in rice reproductive development by negatively regulating osa-miR160. Sci. Bull. 2017;62:470–475. doi: 10.1016/j.scib.2017.03.013. PubMed DOI

Wu H.J., Wang Z.M., Wang M., Wang X.J. Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol. 2013;161:1875–1884. doi: 10.1104/pp.113.215962. PubMed DOI PMC

Komiya R., Nonomura K.I. PIWI-Interacting RNAs. Methods in Molecular Biology. Volume 1093. Humana Press; Totowa, NJ, USA: 2014. Isolation and bioinformatic analyses of small RNAs interacting with germ cell-specific Argonaute in rice; pp. 1–249. PubMed DOI

Ou L.J., Liu Z.B., Zhang Z.Q., Wei G., Zhang Y.P., Kang L.Y., Yang B.Z., Yang S., Lv J.H., Liu Y.H. Noncoding and coding transcriptome analysis reveals the regulation roles of long noncoding RNAs in fruit development of hot pepper (Capsicum annuum L.) Plant Growth Regul. 2017;83:141–156. doi: 10.1007/s10725-017-0290-3. DOI

Dietrich A., Wallet C., Iqbal R.K., Gualberto J.M., Lotfi F. Organellar non-coding RNAs: Emerging regulation mechanisms. Biochimie. 2015;117:48–62. doi: 10.1016/j.biochi.2015.06.027. PubMed DOI

Rurek M. Participation of non-coding RNAs in plant organelle biogenesis. Acta Biochim. Pol. 2016;63:653–663. doi: 10.18388/abp.2016_1346. PubMed DOI

Wu Z.Q., Stone J.D., Štorchová H., Sloan D.B. High transcript abundance, RNA editing, and small RNAs originating from intergenic regions in the massive mitochondrial genome of the angiosperm Silene noctiflora. BMC Genom. 2015;16:938. doi: 10.1186/s12864-015-2155-3. PubMed DOI PMC

Richly E., Leister D. NUMTs in sequenced eukaryotic genomes. Mol. Biol. Evol. 2004;21:1081–1084. doi: 10.1093/molbev/msh110. PubMed DOI

Ruwe H., Wang G.W., Gusewski S., Schmitz-Linneweber C. Systematic analysis of plant mitochondrial and chloroplast small RNAs suggests organelle-specific mRNA stabilization mechanisms. Nucleic Acids Res. 2016;44:7406–7417. doi: 10.1093/nar/gkw466. PubMed DOI PMC

Holec S., Lange H., Kuhn K., Alioua M., Borner T., Gagliardi D. Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell. Biol. 2006;26:2869–2876. doi: 10.1128/MCB.26.7.2869-2876.2006. PubMed DOI PMC

Stone J.D., Koloušková P., Sloan D.B., Štorchová H. Non-coding RNA may be associated with cytoplasmic male sterility in Silene vulgaris. J. Exp. Bot. 2017;68:1599–1612. doi: 10.1093/jxb/erx057. PubMed DOI PMC

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