Recent advances and biotechnological applications of RNA metabolism in plant chloroplasts and mitochondria

References

• Zhao X, Huang J, Chory J. Unraveling the linkage between retrograde signaling and RNA metabolism in plants. Trends Plant Sci. 2020;25:141–147. doi: 10.1016/j.tplants.2019.10.009.
   PubMed Web of Science ®Google Scholar
• Timmis JN, Ayliffe MA, Huang CY, et al. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 2004;5:123–135. doi: 10.1038/nrg1271.
   PubMed Web of Science ®Google Scholar
• Barkan A, Small I. Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol. 2014;65:415–442. doi: 10.1146/annurev-arplant-050213-040159.
   PubMed Web of Science ®Google Scholar
• Liere K, Weihe A, Börner T. The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol. 2011;168:1345–1360. doi: 10.1016/j.jplph.2011.01.005.
   PubMed Web of Science ®Google Scholar
• Kanamaru K, Nagashima A, Fujiwara M, et al. An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol. 2001;42:1034–1043. doi: 10.1093/pcp/pce155.
   PubMed Web of Science ®Google Scholar
• Ishizaki Y, Tsunoyama Y, Hatano K, et al. A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J. 2005;42:133–144. doi: 10.1111/j.1365-313X.2005.02362.x.
   PubMed Web of Science ®Google Scholar
• Hedtke B, Börner T, Weihe A. Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science. 1997;277:809–811. doi: 10.1126/science.277.5327.809.
   PubMed Web of Science ®Google Scholar
• Zhelyazkova P, Sharma CM, Förstner KU, et al. The primary transcriptome of Barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell. 2012;24:123–136. doi: 10.1105/tpc.111.089441.
   PubMed Web of Science ®Google Scholar
• Pfalz J, Liere K, Kandlbinder A, et al. pTAC2, -6, and -12 Are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell. 2006;18:176–197. doi: 10.1105/tpc.105.036392.
   PubMed Web of Science ®Google Scholar
• Cheng S, Gutmann B, Zhong X, et al. Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J. 2016;85:532–547. doi: 10.1111/tpj.13121.
   PubMed Web of Science ®Google Scholar
• Gutmann B, Royan S, Schallenberg-Rüdinger M, et al. The expansion and diversification of pentatricopeptide repeat RNA-editing factors in plants. Mol Plant. 2020;13:215–230. doi: 10.1016/j.molp.2019.11.002.
   PubMed Web of Science ®Google Scholar
• Small I, Melonek J, Bohne A-V, et al. Plant organellar RNA maturation. Plant Cell. 2023;35:1727–1751. doi: 10.1093/plcell/koad049.
   PubMed Web of Science ®Google Scholar
• Sosso D, Canut M, Gendrot G, et al. PPR8522 encodes a chloroplast-targeted pentatricopeptide repeat protein necessary for maize embryogenesis and vegetative development. J Exp Bot. 2012;63:5843–5857. doi: 10.1093/jxb/ers232.
   PubMed Web of Science ®Google Scholar
• Wang X, An Y, Qi Z, et al. PPR protein early chloroplast development 2 is essential for chloroplast development at the early stage of Arabidopsis development. Plant Sci. 2021;308:110908. doi: 10.1016/j.plantsci.2021.110908.
   PubMed Web of Science ®Google Scholar
• Du Y, Mo W, Ma T, et al. A pentatricopeptide repeat protein DUA1 interacts with sigma factor 1 to regulate chloroplast gene expression in rice. Photosynth Res. 2021;147:131–143. doi: 10.1007/s11120-020-00793-0.
   PubMed Web of Science ®Google Scholar
• Kühn K, Bohne A-V, Liere K, et al. Arabidopsis phage-type RNA polymerases: accurate in vitro transcription of organellar genes. Plant Cell. 2007;19:959–971. doi: 10.1105/tpc.106.046839.
   PubMed Web of Science ®Google Scholar
• Babiychuk E, Vandepoele K, Wissing J, et al. Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc Natl Acad Sci USA. 2011;108:6674–6679. doi: 10.1073/pnas.1103442108.
   PubMed Web of Science ®Google Scholar
• Méteignier L-V, Ghandour R, Meierhoff K, et al. The Arabidopsis mTERF-repeat MDA1 protein plays a dual function in transcription and stabilization of specific chloroplast transcripts within the psbE and ndhH operons. New Phytol. 2020;227:1376–1391. doi: 10.1111/nph.16625.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Cui Y-L, Zhang X-L, et al. A nuclear-encoded protein, mTERF6, mediates transcription termination of rpoA polycistron for plastid-encoded RNA polymerase-dependent chloroplast gene expression and chloroplast development. Sci Rep. 2018;8:11929. doi: 10.1038/s41598-018-30166-6.
   PubMed Web of Science ®Google Scholar
• Xiong H-B, Wang J, Huang C, et al. mTERF8, a member of the mitochondrial transcription termination factor family, is involved in the transcription termination of chloroplast gene psbJ. Plant Physiol. 2020;182:408–423. doi: 10.1104/pp.19.00906.
   PubMed Web of Science ®Google Scholar
• Yang EJ, Yoo CY, Liu J, et al. NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches. Nat Commun. 2019;10:2630. doi: 10.1038/s41467-019-10517-1.
   PubMed Web of Science ®Google Scholar
• Yoo CY, Pasoreck EK, Wang H, et al. Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat Commun. 2019;10:2629. doi: 10.1038/s41467-019-10518-0.
   PubMed Web of Science ®Google Scholar
• Stern DB, Goldschmidt-Clermont M, Hanson MR. Chloroplast RNA metabolism. Annu Rev Plant Biol. 2010;61:125–155. doi: 10.1146/annurev-arplant-042809-112242.
   PubMed Web of Science ®Google Scholar
• Schein A, Sheffy-Levin S, Glaser F, et al. The RNase E/G-type endoribonuclease of higher plants is located in the chloroplast and cleaves RNA similarly to the E. coli enzyme. RNA. 2008;14:1057–1068. doi: 10.1261/rna.907608.
   PubMed Web of Science ®Google Scholar
• Stoppel R, Manavski N, Schein A, et al. RHON1 is a novel ribonucleic acid-binding protein that supports RNase E function in the Arabidopsis chloroplast. Nucleic Acids Res. 2012;40:8593–8606. doi: 10.1093/nar/gks613.
   PubMed Web of Science ®Google Scholar
• Walter M, Piepenburg K, Schöttler MA, et al. Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency. Plant J. 2010;64:851–863. doi: 10.1111/j.1365-313X.2010.04377.x.
   PubMed Web of Science ®Google Scholar
• de la Sierra-Gallay IL, Zig L, Jamalli A, et al. Structural insights into the dual activity of RNase J. Nat Struct Mol Biol. 2008;15:206–212. doi: 10.1038/nsmb.1376.
   PubMed Web of Science ®Google Scholar
• Bollenbach TJ, Stern DB. Secondary structures common to chloroplast mRNA 3′-untranslated regions direct cleavage by CSP41, an endoribonuclease belonging to the short chain dehydrogenase/reductase superfamily. J Biol Chem. 2003;278:25832–25838. doi: 10.1074/jbc.M303559200.
   PubMed Web of Science ®Google Scholar
• Walter M, Kilian J, Kudla J. PNPase activity determines the efficiency of mRNA 3′-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. Embo J. 2002;21:6905–6914. doi: 10.1093/emboj/cdf686.
   PubMed Web of Science ®Google Scholar
• Perrin R, Lange H, Grienenberger J-M, et al. AtmtPNPase is required for multiple aspects of the 18S rRNA metabolism in Arabidopsis thaliana mitochondria. Nucleic Acids Res. 2004;32:5174–5182. doi: 10.1093/nar/gkh852.
   PubMed Web of Science ®Google Scholar
• Kishine M, Takabayashi A, Munekage Y, et al. Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Mol Biol. 2004;55:595–606. doi: 10.1007/s11103-004-1507-1.
   PubMed Web of Science ®Google Scholar
• Germain A, Kim SH, Gutierrez R, et al. Ribonuclease II preserves chloroplast RNA homeostasis by increasing mRNA decay rates, and cooperates with polynucleotide phosphorylase in 3′ end maturation. Plant J. 2012;72:960–971. doi: 10.1111/tpj.12006.
   PubMed Web of Science ®Google Scholar
• Germain A, Hotto AM, Barkan A, et al. RNA processing and decay in plastids: RNA processing and decay in plastids. Wiley Interdiscip Rev RNA. 2013;4:295–316. doi: 10.1002/wrna.1161.
   PubMed Web of Science ®Google Scholar
• Sharwood R, Halpert M, Luro S, et al. Chloroplast RNase J compensates for inefficient transcription termination by removal of antisense RNA. RNA. 2011;17:2165–2176. doi: 10.1261/rna.028043.111.
   PubMed Web of Science ®Google Scholar
• Teubner M, Fuß J, Kühn K, et al. The RNA recognition motif protein CP33A is a global ligand of chloroplast mRNAs and is essential for plastid biogenesis and plant development. Plant J. 2017;89:472–485. doi: 10.1111/tpj.13396.
   PubMed Web of Science ®Google Scholar
• Pfalz J, Bayraktar OA, Prikryl J, et al. Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. Embo J. 2009;28:2042–2052. doi: 10.1038/emboj.2009.121.
   PubMed Web of Science ®Google Scholar
• Rojas M, Ruwe H, Miranda RG, et al. Unexpected functional versatility of the pentatricopeptide repeat proteins PGR3, PPR5 and PPR10. Nucleic Acids Res. 2018;46:10448–10459.
   PubMed Web of Science ®Google Scholar
• Hammani K, Cook WB, Barkan A. RNA binding and RNA remodeling activities of the half-a-tetratricopeptide (HAT) protein HCF107 underlie its effects on gene expression. Proc Natl Acad Sci USA. 2012;109:5651–5656. doi: 10.1073/pnas.1200318109.
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhou W, Che L, et al. PPR protein BFA2 is essential for the accumulation of the atpH/F transcript in chloroplasts. Front Plant Sci. 2019;10:446. doi: 10.3389/fpls.2019.00446.
   PubMed Web of Science ®Google Scholar
• Zoschke R, Watkins KP, Miranda RG, et al. The PPR-SMR protein PPR53 enhances the stability and translation of specific chloroplast RNAs in maize. Plant J. 2016;85:594–606. doi: 10.1111/tpj.13093.
   PubMed Web of Science ®Google Scholar
• Ebihara T, Matsuda T, Sugita C, et al. The P-class pentatricopeptide repeat protein PpPPR_21 is needed for accumulation of the psbI-ycf12 dicistronic mRNA in Physcomitrella chloroplasts. Plant J. 2019;97:1120–1131. doi: 10.1111/tpj.14187.
   PubMed Web of Science ®Google Scholar
• Perrin R, Meyer EH, Zaepfel M, et al. Two exoribonucleases act sequentially to process mature 3′-ends of atp9 mRNAs in Arabidopsis mitochondria. J Biol Chem. 2004;279:25440–25446. doi: 10.1074/jbc.M401182200.
   PubMed Web of Science ®Google Scholar
• Forner J, Weber B, Thuss S, et al. Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5′ and 3′ end formation. Nucleic Acids Res. 2007;35:3676–3692. doi: 10.1093/nar/gkm270.
   PubMed Web of Science ®Google Scholar
• Haïli N, Arnal N, Quadrado M, et al. The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res. 2013;41:6650–6663. doi: 10.1093/nar/gkt337.
   PubMed Web of Science ®Google Scholar
• Wang C, Aubé F, Planchard N, et al. The pentatricopeptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3´ end of its 5´-half intron. Nucleic Acids Res. 2017;45:6119–6134. doi: 10.1093/nar/gkx162.
   PubMed Web of Science ®Google Scholar
• Hölzle A, Jonietz C, Törjek O, et al. A RESTORER OF FERTILITY-like PPR gene is required for 5′-end processing of the nad4 mRNA in mitochondria of Arabidopsis thaliana. Plant J. 2011;65:737–744. doi: 10.1111/j.1365-313X.2010.04460.x.
   PubMed Web of Science ®Google Scholar
• Jonietz C, Forner J, Hölzle A, et al. RNA PROCESSING FACTOR2 is required for 5′ end processing of nad9 and cox3 mRNAs in mitochondria of Arabidopsis thaliana. Plant Cell. 2010;22:443–453. doi: 10.1105/tpc.109.066944.
   PubMed Web of Science ®Google Scholar
• Jonietz C, Forner J, Hildebrandt T, et al. RNA processing factor3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of Arabidopsis accession Columbia. Plant Physiol. 2011;157:1430–1439. doi: 10.1104/pp.111.181552.
   PubMed Web of Science ®Google Scholar
• Fujii S, Suzuki T, Giegé P, et al. The Restorer-of-fertility-like 2 pentatricopeptide repeat protein and RNase P are required for the processing of mitochondrial orf291 RNA in Arabidopsis. Plant J. 2016;86:504–513. doi: 10.1111/tpj.13185.
   PubMed Web of Science ®Google Scholar
• Stoll B, Binder S. Two NYN domain containing putative nucleases are involved in transcript maturation in Arabidopsis mitochondria. Plant J. 2016;85:278–288. doi: 10.1111/tpj.13111.
   PubMed Web of Science ®Google Scholar
• Miyata Y, Sugita M. Tissue- and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts. J Plant Physiol. 2004;161:113–115. doi: 10.1078/0176-1617-01220.
   PubMed Web of Science ®Google Scholar
• Takenaka M, Zehrmann A, Verbitskiy D, et al. RNA editing in plants and its evolution. Annu Rev Genet. 2013;47:335–352. doi: 10.1146/annurev-genet-111212-133519.
   PubMed Web of Science ®Google Scholar
• Sun T, Bentolila S, Hanson MR. The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci. 2016;21:962–973. doi: 10.1016/j.tplants.2016.07.005.
   PubMed Web of Science ®Google Scholar
• Ichinose M, Sugita M. RNA editing and its molecular mechanism in plant organelles. Genes. 2016;8:5. doi: 10.3390/genes8010005.
   PubMed Web of Science ®Google Scholar
• Chu D, Wei L. Reduced C-to-U RNA editing rates might play a regulatory role in stress response of Arabidopsis. J Plant Physiol. 2020;244:153081. doi: 10.1016/j.jplph.2019.153081.
   PubMed Web of Science ®Google Scholar
• Tian F, Yu J, Zhang Y, et al. MORF9 functions in plastid RNA editing with tissue specificity. Int J Mol Sci. 2019;20:4635. doi: 10.3390/ijms20184635.
   PubMed Web of Science ®Google Scholar
• Sun YK, Gutmann B, Yap A, et al. Editing of chloroplast rps14 by PPR editing factor EMB2261 is essential for Arabidopsis development. Front Plant Sci. 2018;9:841. doi: 10.3389/fpls.2018.00841.
   PubMed Web of Science ®Google Scholar
• Zhao X, Huang J, Chory J. GUN1 interacts with MORF2 to regulate plastid RNA editing during retrograde signaling. Proc Natl Acad Sci USA. 2019;116:10162–10167. doi: 10.1073/pnas.1820426116.
   PubMed Web of Science ®Google Scholar
• Yapa MM, Doroodian P, Gao Z, et al. MORF2-mediated plastidial retrograde signaling is involved in stress response and skotomorphogenesis beyond RNA editing. Front Plant Sci. 2023;14:1146922. doi: 10.3389/fpls.2023.1146922.
   PubMed Web of Science ®Google Scholar
• Rüdinger M, Funk HT, Rensing SA, et al. RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics. 2009;281:473–481. doi: 10.1007/s00438-009-0424-z.
   PubMed Web of Science ®Google Scholar
• Tasaki E, Hattori M, Sugita M. The moss pentatricopeptide repeat protein with a DYW domain is responsible for RNA editing of mitochondrial ccmFc transcript. Plant J. 2010;62:560–570. doi: 10.1111/j.1365-313X.2010.04175.x.
   PubMed Web of Science ®Google Scholar
• Kugita M, Yamamoto Y, Fujikawa T, et al. RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res. 2003;31:2417–2423. doi: 10.1093/nar/gkg327.
   PubMed Web of Science ®Google Scholar
• Bégu D, Castandet B, Araya A. RNA editing restores critical domains of a group I intron in fern mitochondria. Curr Genet. 2011;57:317–325. doi: 10.1007/s00294-011-0349-z.
   PubMed Web of Science ®Google Scholar
• Bonavita S, Regina TMR. The volutionary conservation of rps3 introns and rps19-rps3-rpl16 gene cluster in Adiantum capillus-veneris mitochondria. Curr Genet. 2016;62:173–184. doi: 10.1007/s00294-015-0512-z.
   PubMed Web of Science ®Google Scholar
• Ong HC, Palmer JD. Pervasive survival of expressed mitochondrial rps14 pseudogenes in grasses and their relatives for 80 million years following three functional transfers to the nucleus. BMC Evol Biol. 2006;6:55. doi: 10.1186/1471-2148-6-55.
   PubMed Web of Science ®Google Scholar
• Knie N, Grewe F, Fischer S, et al. Reverse U-to-C editing exceeds C-to-U RNA editing in some ferns – a monilophyte-wide comparison of chloroplast and mitochondrial RNA editing suggests independent evolution of the two processes in both organelles. BMC Evol Biol. 2016;16:134. doi: 10.1186/s12862-016-0707-z.
   PubMed Web of Science ®Google Scholar
• Gerke P, Szövényi P, Neubauer A, et al. Towards a plant model for enigmatic U-to-C RNA editing: the organelle genomes, transcriptomes, editomes and candidate RNA editing factors in the hornwort Anthoceros agrestis. New Phytol. 2020;225:1974–1992. doi: 10.1111/nph.16297.
   PubMed Web of Science ®Google Scholar
• Ichinose M, Kawabata M, Akaiwa Y, et al. U-to-C RNA editing by synthetic PPR-DYW proteins in bacteria and human culture cells. Commun Biol. 2022;5:968. doi: 10.1038/s42003-022-03927-3.
   PubMed Web of Science ®Google Scholar
• Lesch E, Schilling MT, Brenner S, et al. Plant mitochondrial RNA editing factors can perform targeted C-to-U editing of nuclear transcripts in human cells. Nucleic Acids Res. 2022;50:9966–9983. doi: 10.1093/nar/gkac752.
   PubMed Web of Science ®Google Scholar
• Hayes ML, Santibanez PI. A plant pentatricopeptide repeat protein with a DYW-deaminase domain is sufficient for catalyzing C-to-U RNA editing in vitro. J Biol Chem. 2020;295:3497–3505. doi: 10.1074/jbc.RA119.011790.
   PubMed Web of Science ®Google Scholar
• Boussardon C, Avon A, Kindgren P, et al. The cytidine deaminase signature HxE(x)nCxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. New Phytol. 2014;203:1090–1095. doi: 10.1111/nph.12928.
   PubMed Web of Science ®Google Scholar
• Takenaka M, Takenaka S, Barthel T, et al. DYW domain structures imply an unusual regulation principle in plant organellar RNA editing catalysis. Nat Catal. 2021;4:510–522. doi: 10.1038/s41929-021-00633-x.
   PubMed Web of Science ®Google Scholar
• Maeda A, Takenaka S, Wang T, et al. DYW deaminase domain has a distinct preference for neighboring nucleotides of the target RNA editing sites. Plant J. 2022;111:756–767.
   Web of Science ®Google Scholar
• Oldenkott B, Yang Y, Lesch E, et al. Plant-type pentatricopeptide repeat proteins with a DYW domain drive C-to-U RNA editing in Escherichia coli. Commun Biol. 2019;2:85. doi: 10.1038/s42003-019-0328-3.
   PubMed Web of Science ®Google Scholar
• Lurin C, Andrés C, Aubourg S, et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell. 2004;16:2089–2103. doi: 10.1105/tpc.104.022236.
   PubMed Web of Science ®Google Scholar
• Kotera E, Tasaka M, Shikanai T. A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature. 2005;433:326–330. doi: 10.1038/nature03229.
   PubMed Web of Science ®Google Scholar
• Zehrmann A, Verbitskiy D, van der Merwe JA, et al. A DYW domain–containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell. 2009;21:558–567. doi: 10.1105/tpc.108.064535.
   PubMed Web of Science ®Google Scholar
• Barkan A, Rojas M, Fujii S, et al. A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLOS Genet. 2012;8:e1002910. doi: 10.1371/journal.pgen.1002910.
   PubMed Web of Science ®Google Scholar
• Härtel B, Zehrmann A, Verbitskiy D, et al. MEF10 is required for RNA editing at nad2-842 in mitochondria of Arabidopsis thaliana and interacts with MORF8. Plant Mol Biol. 2013;81:337–346. doi: 10.1007/s11103-012-0003-2.
   PubMed Web of Science ®Google Scholar
• Ichinose M, Sugita C, Yagi Y, et al. Two DYW subclass PPR proteins are involved in RNA editing of ccmFc and atp9 transcripts in the moss Physcomitrella patens: first complete set of PPR editing factors in plant mitochondria. Plant Cell Physiol. 2013;54:1907–1916. doi: 10.1093/pcp/pct132.
   PubMed Web of Science ®Google Scholar
• Xie T, Chen D, Wu J, et al. Growing Slowly 1 locus encodes a PLS-type PPR protein required for RNA editing and plant development in Arabidopsis. J Exp Bot. 2016;67:5687–5698. doi: 10.1093/jxb/erw331.
   PubMed Web of Science ®Google Scholar
• Hammani K, Okuda K, Tanz SK, et al. A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites. Plant Cell. 2009;21:3686–3699. doi: 10.1105/tpc.109.071472.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Xu Y, Huang J, et al. The rice pentatricopeptide repeat protein PPR756 is involved in pollen development by affecting multiple RNA editing in mitochondria. Front Plant Sci. 2020;11:749. doi: 10.3389/fpls.2020.00749.
   PubMed Web of Science ®Google Scholar
• Cui X, Wang Y, Wu J, et al. The RNA editing factor DUA 1 is crucial to chloroplast development at low temperature in rice. New Phytol. 2019;221:834–849. doi: 10.1111/nph.15448.
   PubMed Web of Science ®Google Scholar
• Huang J, Lu G, Liu L, et al. The kernel size-related quantitative trait locus qKW9 encodes a pentatricopeptide repeat protein that affects photosynthesis and grain filling. Plant Physiol. 2020;183:1696–1709. doi: 10.1104/pp.20.00374.
   PubMed Web of Science ®Google Scholar
• Knoop V. C-to-U and U-to-C: RNA editing in plant organelles and beyond. J Exp Bot. 2023;74:2273–2294. doi: 10.1093/jxb/erac488.
   PubMed Web of Science ®Google Scholar
• Loiacono FV, Walther D, Seeger S, et al. Emergence of novel RNA-editing sites by changes in the binding affinity of a conserved PPR protein. Mol Biol Evol. 2022;39:222.
   Web of Science ®Google Scholar
• Boussardon C, Salone V, Avon A, et al. Two interacting proteins are necessary for the editing of the NdhD-1 site in Arabidopsis plastids. Plant Cell. 2012;24:3684–3694. doi: 10.1105/tpc.112.099507.
   PubMed Web of Science ®Google Scholar
• Verbitskiy D, Zehrmann A, Härtel B, et al. Two Related RNA-editing Proteins Target the Same Sites in Mitochondria of Arabidopsis thaliana. J Biol Chem. 2012;287:38064–38072.
   PubMed Web of Science ®Google Scholar
• Guillaumot D, Lopez-Obando M, Baudry K, et al. Two interacting PPR proteins are major Arabidopsis editing factors in plastid and mitochondria. Proc Natl Acad Sci USA. 2017;114:8877–8882. doi: 10.1073/pnas.1705780114.
   PubMed Web of Science ®Google Scholar
• Andrés-Colás N, Zhu Q, Takenaka M, et al. Multiple PPR protein interactions are involved in the RNA editing system in Arabidopsis mitochondria and plastids. Proc Natl Acad Sci USA. 2017;114:8883–8888. doi: 10.1073/pnas.1705815114.
   PubMed Web of Science ®Google Scholar
• Malbert B, Burger M, Lopez-Obando M, et al. The analysis of the editing defects in the dyw2 mutant provides new clues for the prediction of RNA targets of Arabidopsis E+-class PPR proteins. Plants. 2020;9:280. doi: 10.3390/plants9020280.
   Google Scholar
• Zhang J, Guo Y, Fang Q, et al. The PPR-SMR protein ATP4 is required for editing the chloroplast rps8 mRNA in rice and maize. Plant Physiol. 2020;184:2011–2021. doi: 10.1104/pp.20.00849.
   PubMed Web of Science ®Google Scholar
• Yang Y-Z, Liu X-Y, Tang J-J, et al. GRP23 plays a core role in E-type editosomes via interacting with MORFs and atypical PPR-DYWs in Arabidopsis mitochondria. Proc Natl Acad Sci USA. 2022;119:e2210978119.
   PubMed Web of Science ®Google Scholar
• Wang Y, Li H, Huang Z-Q, et al. Maize PPR-E proteins mediate RNA C-to-U editing in mitochondria by recruiting the trans deaminase PCW1. Plant Cell. 2022;35:529–551. doi: 10.1093/plcell/koac298.
   Web of Science ®Google Scholar
• Bentolila S, Heller WP, Sun T, et al. RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proc Natl Acad Sci USA. 2012;109:e1453–e1461.
   PubMed Web of Science ®Google Scholar
• Takenaka M, Zehrmann A, Verbitskiy D, et al. Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc Natl Acad Sci USA. 2012;109:5104–5109. doi: 10.1073/pnas.1202452109.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Cui X, Wang Y, et al. The RNA editing factor WSP1 is essential for chloroplast development in rice. Mol Plant. 2017;10:86–98. doi: 10.1016/j.molp.2016.08.009.
   PubMed Web of Science ®Google Scholar
• Sun T, Germain A, Giloteaux L, et al. An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize. Proc Natl Acad Sci USA. 2013;110:e1169–e1178.
   PubMed Web of Science ®Google Scholar
• Yang Y, Liu X, Wang K, et al. Molecular and functional diversity of organelle RNA editing mediated by RNA recognition motif-containing protein ORRM4 in tomato. New Phytol. 2020;228:570–585. doi: 10.1111/nph.16714.
   PubMed Web of Science ®Google Scholar
• Sun T, Shi X, Friso G, et al. A zinc finger motif-containing protein is essential for chloroplast RNA editing. PLOS Genet. 2015;11:e1005028. doi: 10.1371/journal.pgen.1005028.
   PubMed Web of Science ®Google Scholar
• Zhang F, Tang W, Hedtke B, et al. Tetrapyrrole biosynthetic enzyme protoporphyrinogen IX oxidase 1 is required for plastid RNA editing. Proc Natl Acad Sci USA. 2014;111:2023–2028. doi: 10.1073/pnas.1316183111.
   PubMed Web of Science ®Google Scholar
• Zehrmann A, Härtel B, Glass F, et al. Selective homo- and heteromer interactions between the multiple organellar RNA editing factor (MORF) proteins in Arabidopsis thaliana. J Biol Chem. 2015;290:6445–6456. doi: 10.1074/jbc.M114.602086.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang Y, Ren Y, et al. white panicle2 encoding thioredoxin z, regulates plastid RNA editing by interacting with multiple organellar RNA editing factors in rice. New Phytol. 2021;229:2693–2706. doi: 10.1111/nph.17047.
   PubMed Web of Science ®Google Scholar
• Yuan J, Ma T, Ji S, et al. Two chloroplast-localized MORF proteins act as chaperones to maintain tetrapyrrole biosynthesis. New Phytol. 2022;235:1868–1883. doi: 10.1111/nph.18273.
   PubMed Web of Science ®Google Scholar
• Bayer-Császár E, Haag S, Jörg A, et al. The conserved domain in MORF proteins has distinct affinities to the PPR and E elements in PPR RNA editing factors. Biochim Biophys Acta Gene Regul Mech. 2017;1860:813–828. doi: 10.1016/j.bbagrm.2017.05.004.
   PubMed Web of Science ®Google Scholar
• Haag S, Schindler M, Berndt L, et al. Crystal structures of the Arabidopsis thaliana organellar RNA editing factors MORF1 and MORF9. Nucleic Acids Res. 2017;45:4915–4928. doi: 10.1093/nar/gkx099.
   PubMed Web of Science ®Google Scholar
• Yan J, Zhang Q, Guan Z, et al. MORF9 increases the RNA-binding activity of PLS-type pentatricopeptide repeat protein in plastid RNA editing. Nat Plants. 2017;3:17037.
   PubMed Web of Science ®Google Scholar
• Shi X, Castandet B, Germain A, et al. ORRM5, an RNA recognition motif-containing protein, has a unique effect on mitochondrial RNA editing. J Exp Bot. 2017;68:2833–2847. doi: 10.1093/jxb/erx139.
   PubMed Web of Science ®Google Scholar
• Shi X, Bentolila S, Hanson MR. Organelle RNA recognition motif-containing (ORRM) proteins are plastid and mitochondrial editing factors in Arabidopsis. Plant Signal Behav. 2016;11:e1167299. doi: 10.1080/15592324.2016.1167299.
   PubMed Web of Science ®Google Scholar
• Huang C, Yu Q-B, Li Z-R, et al. Porphobilinogen deaminase HEMC interacts with the PPR-protein AtECB2 for chloroplast RNA editing. Plant J. 2017;92:546–556. doi: 10.1111/tpj.13672.
   PubMed Web of Science ®Google Scholar
• Bobik K, McCray TN, Ernest B, et al. The chloroplast RNA helicase ISE 2 is required for multiple chloroplast RNA processing steps in Arabidopsis thaliana. Plant J. 2017;91:114–131. doi: 10.1111/tpj.13550.
   PubMed Web of Science ®Google Scholar
• de Longevialle AF, Small ID, Lurin C. Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant. 2010;3:691–705. doi: 10.1093/mp/ssq025.
   PubMed Web of Science ®Google Scholar
• Haugen P, Simon DM, Bhattacharya D. The natural history of group I introns. Trends Genet. 2005;21:111–119. doi: 10.1016/j.tig.2004.12.007.
   PubMed Web of Science ®Google Scholar
• Hammani K, Giegé P. RNA metabolism in plant mitochondria. Trends Plant Sci. 2014;19:380–389. doi: 10.1016/j.tplants.2013.12.008.
   PubMed Web of Science ®Google Scholar
• Schmitz-Linneweber C, Lampe M-K, Sultan L, et al. Organellar maturases: a window into the evolution of the spliceosome. Biochim Biophys Acta BBA Bioenerg. 2015;1847:798–808.
   PubMed Web of Science ®Google Scholar
• Asakura Y, Bayraktar OA, Barkan A. Two CRM protein subfamilies cooperate in the splicing of group IIb introns in chloroplasts. RNA. 2008;14:2319–2332. doi: 10.1261/rna.1223708.
   PubMed Web of Science ®Google Scholar
• de Longevialle AF, Hendrickson L, Taylor NL, et al. The pentatricopeptide repeat gene OTP51 with two LAGLIDADG motifs is required for the cis-splicing of plastid ycf3 intron 2 in Arabidopsis thaliana. Plant J. 2008;56:157–168. doi: 10.1111/j.1365-313X.2008.03581.x.
   PubMed Web of Science ®Google Scholar
• Asakura Y, Galarneau E, Watkins KP, et al. Chloroplast RH3 dead box RNA helicases in maize and Arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome biogenesis. Plant Physiol. 2012;159:961–974. doi: 10.1104/pp.112.197525.
   PubMed Web of Science ®Google Scholar
• Barkan A, Klipcan L, Ostersetzer O, et al. The CRM domain: an RNA binding module derived from an ancient ribosome-associated protein. RNA. 2007;13:55–64. doi: 10.1261/rna.139607.
   PubMed Web of Science ®Google Scholar
• Till B, Schmitz-Linneweber C, Williams-Carrier R, et al. CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA. 2001;7:1227–1238. doi: 10.1017/s1355838201010445.
   PubMed Web of Science ®Google Scholar
• Lee K, Park SJ, Park Y-I, et al. CFM9, a mitochondrial CRM protein, is crucial for mitochondrial intron splicing, mitochondria function and arabidopsis growth and stress responses. Plant Cell Physiol. 2019;60:2538–2548. doi: 10.1093/pcp/pcz147.
   PubMed Web of Science ®Google Scholar
• Kroeger TS, Watkins KP, Friso G, et al. A plant-specific RNA-binding domain revealed through analysis of chloroplast group II intron splicing. Proc Natl Acad Sci USA. 2009;106:4537–4542. doi: 10.1073/pnas.0812503106.
   PubMed Web of Science ®Google Scholar
• Watkins KP, Kroeger TS, Cooke AM, et al. A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. Plant Cell. 2007;19:2606–2623. doi: 10.1105/tpc.107.053736.
   PubMed Web of Science ®Google Scholar
• Nawaz G, Kang H. Chloroplast- or mitochondria-targeted dead-box RNA helicases play essential roles in organellar RNA metabolism and abiotic stress responses. Front. Plant Sci. 2017;8:871. doi: 10.3389/fpls.2017.00871.
   PubMed Web of Science ®Google Scholar
• Bentolila S, Gipson AB, Kehl AJ, et al. A RanBP2-type zinc finger protein functions in intron splicing in Arabidopsis mitochondria and is involved in the biogenesis of respiratory complex I. Nucleic Acids Res. 2021;49:3490–3506. doi: 10.1093/nar/gkab066.
   PubMed Web of Science ®Google Scholar
• Hammani K, Barkan A. An mTERF domain protein functions in group II intron splicing in maize chloroplasts. Nucleic Acids Res. 2014;42:5033–5042. doi: 10.1093/nar/gku112.
   PubMed Web of Science ®Google Scholar
• Lee K, Park SJ, Colas Des Francs-Small C, et al. The coordinated action of PPR4 and EMB2654 on each intron half mediates trans-splicing of rps12 transcripts in plant chloroplasts. Plant J. 2019;100:1193–1207. doi: 10.1111/tpj.14509.
   PubMed Web of Science ®Google Scholar
• Chateigner-Boutin A-L, Des Francs-Small CC, Delannoy E, et al. OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoc1. Plant J. 2011;65:532–542. doi: 10.1111/j.1365-313X.2010.04441.x.
   PubMed Web of Science ®Google Scholar
• Liu X, Zhang X, Cao R, et al. CDE4 encodes a pentatricopeptide repeat protein involved in chloroplast RNA splicing and affects chloroplast development under low-temperature conditions in rice. J Integr Plant Biol. 2021;63:1724–1739.
   Web of Science ®Google Scholar
• de Longevialle AF, Meyer EH, Andrés C, et al. The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell. 2007;19:3256–3265. doi: 10.1105/tpc.107.054841.
   PubMed Web of Science ®Google Scholar
• Lee K, Han JH, Park Y-I, et al. The mitochondrial pentatricopeptide repeat protein PPR19 is involved in the stabilization of NADH dehydrogenase 1 transcripts and is crucial for mitochondrial function and Arabidopsis thaliana development. New Phytol. 2017;215:202–216. doi: 10.1111/nph.14528.
   PubMed Web of Science ®Google Scholar
• Beick S, Schmitz-Linneweber C, Williams-Carrier R, et al. The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol. 2008;28:5337–5347. doi: 10.1128/MCB.00563-08.
   PubMed Web of Science ®Google Scholar
• Goto S, Kawaguchi Y, Sugita C, et al. P-class pentatricopeptide repeat protein PTSF1 is required for splicing of the plastid pre-tRNAIle in Physcomitrella patens. Plant J. 2016;86:493–503. doi: 10.1111/tpj.13184.
   PubMed Web of Science ®Google Scholar
• Sun F, Zhang X, Shen Y, et al. The pentatricopeptide repeat protein EMPTY PERICARP8 is required for the splicing of three mitochondrial introns and seed development in maize. Plant J. 2018;95:919–932. doi: 10.1111/tpj.14030.
   Web of Science ®Google Scholar
• Yang H, Xiu Z, Wang L, et al. Two pentatricopeptide repeat proteins are required for the splicing of nad5 introns in maize. Front Plant Sci. 2020;11:732. doi: 10.3389/fpls.2020.00732.
   PubMed Web of Science ®Google Scholar
• Wang C, Aubé F, Quadrado M, et al. Three new pentatricopeptide repeat proteins facilitate the splicing of mitochondrial transcripts and complex I biogenesis in Arabidopsis. J Exp Bot. 2018;69:5131–5140. doi: 10.1093/jxb/ery275.
   PubMed Web of Science ®Google Scholar
• An H, Ke X, Li L, et al. ALBINO EMBRYO AND SEEDLING is required for RNA splicing and chloroplast homeostasis in Arabidopsis. Plant Physiol. 2023;193:483–501. doi: 10.1093/plphys/kiad341.
   PubMedGoogle Scholar
• Ichinose M, Ishimaru A, Sugita C, et al. Two novel PLS-class pentatricopeptide repeat proteins are involved in the group II intron splicing of mitochondrial transcripts in the moss Physcomitrella patens. Plant Cell Physiol. 2020;61:1687–1698. doi: 10.1093/pcp/pcaa070.
   PubMed Web of Science ®Google Scholar
• Dasso M. RCC1 in the cell cycle: the regulator of chromosome condensation takes on new roles. Trends Biochem Sci. 1993;18:96–101. doi: 10.1016/0968-0004(93)90161-f.
   PubMed Web of Science ®Google Scholar
• Kühn K, Carrie C, Giraud E, et al. The RCC1 family protein RUG3 is required for splicing of nad2 and complex I biogenesis in mitochondria of Arabidopsis thaliana. Plant J. 2011;67:1067–1080. doi: 10.1111/j.1365-313X.2011.04658.x.
   PubMed Web of Science ®Google Scholar
• Su C, Zhao H, Zhao Y, et al. RUG3 and ATM synergistically regulate the alternative splicing of mitochondrial nad2 and the DNA damage response in Arabidopsis thaliana. Sci Rep. 2017;7:43897. doi: 10.1038/srep43897.
   PubMed Web of Science ®Google Scholar
• Waltz F, Soufari H, Bochler A, et al. Cryo-EM structure of the RNA-rich plant mitochondrial ribosome. Nat Plants. 2020;6:377–383. doi: 10.1038/s41477-020-0631-5.
   PubMed Web of Science ®Google Scholar
• Cottilli P, Itoh Y, Nobe Y, et al. Cryo-EM structure and rRNA modification sites of a plant ribosome. Plant Commun. 2022;3:100342. doi: 10.1016/j.xplc.2022.100342.
   PubMedGoogle Scholar
• Scharff LB, Childs L, Walther D, et al. Local absence of secondary structure permits translation of mRNAs that lack ribosome-binding sites. PLOS Genet. 2011;7:e1002155. doi: 10.1371/journal.pgen.1002155.
   PubMed Web of Science ®Google Scholar
• Zoschke R, Kroeger T, Belcher S, et al. The pentatricopeptide repeat-SMR protein ATP4 promotes translation of the chloroplast atpB/E mRNA. Plant J. 2012;72:547–558. doi: 10.1111/j.1365-313X.2012.05081.x.
   PubMed Web of Science ®Google Scholar
• Zoschke R, Qu Y, Zubo YO, et al. Mutation of the pentatricopeptide repeat-SMR protein SVR7 impairs accumulation and translation of chloroplast ATP synthase subunits in Arabidopsis thaliana. J Plant Res. 2013;126:403–414. doi: 10.1007/s10265-012-0527-1.
   PubMed Web of Science ®Google Scholar
• Prikryl J, Rojas M, Schuster G, et al. Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc Natl Acad Sci USA. 2011;108:415–420. doi: 10.1073/pnas.1012076108.
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Tasaka M, Shikanai T. PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J. 2004;38:152–163. doi: 10.1111/j.1365-313X.2004.02035.x.
   PubMed Web of Science ®Google Scholar
• Higashi H, Kato Y, Fujita T, et al. The pentatricopeptide repeat protein PGR3 is required for the translation of petL and ndhG by binding their 5′ UTRs. Plant Cell Physiol. 2021;62:1146–1155. doi: 10.1093/pcp/pcaa180.
   PubMed Web of Science ®Google Scholar
• Williams-Carrier R, Brewster C, Belcher SE, et al. The Arabidopsis pentatricopeptide repeat protein LPE1 and its maize ortholog are required for translation of the chloroplast psbJ RNA. Plant J. 2019;99:56–66. doi: 10.1111/tpj.14308.
   PubMed Web of Science ®Google Scholar
• Link S, Engelmann K, Meierhoff K, et al. The atypical short-chain dehydrogenases HCF173 and HCF244 are jointly involved in translational initiation of the psbA mRNA of Arabidopsis. Plant Physiol. 2012;160:2202–2218. doi: 10.1104/pp.112.205104.
   PubMed Web of Science ®Google Scholar
• Schult K, Meierhoff K, Paradies S, et al. The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell. 2007;19:1329–1346. doi: 10.1105/tpc.106.042895.
   PubMed Web of Science ®Google Scholar
• Barkan A, Walker M, Nolasco M, et al. A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. Embo J. 1994;13:3170–3181. doi: 10.1002/j.1460-2075.1994.tb06616.x.
   PubMed Web of Science ®Google Scholar
• Fisk DG, Walker MB, Barkan A. Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. Embo J. 1999;18:2621–2630. doi: 10.1093/emboj/18.9.2621.
   PubMed Web of Science ®Google Scholar
• Jiang J, Chai X, Manavski N, et al. An RNA chaperone–like protein plays critical roles in chloroplast mRNA stability and translation in Arabidopsis and maize. Plant Cell. 2019;31:1308–1327. doi: 10.1105/tpc.18.00946.
   PubMed Web of Science ®Google Scholar
• Méteignier L-V, Ghandour R, Zimmerman A, et al. Arabidopsis mTERF9 protein promotes chloroplast ribosomal assembly and translation by establishing ribonucleoprotein interactions in vivo. Nucleic Acids Res. 2021;49:1114–1132. doi: 10.1093/nar/gkaa1244.
   PubMed Web of Science ®Google Scholar
• Manavski N, Guyon V, Meurer J, et al. An essential pentatricopeptide repeat protein facilitates 5′ maturation and translation initiation of rps3 mRNA in maize mitochondria. Plant Cell. 2012;24:3087–3105. doi: 10.1105/tpc.112.099051.
   PubMed Web of Science ®Google Scholar
• Hammani K, Gobert A, Hleibieh K, et al. An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation. Plant Cell. 2011;23:730–740. doi: 10.1105/tpc.110.081638.
   PubMed Web of Science ®Google Scholar
• Uyttewaal M, Mireau H, Rurek M, et al. PPR336 is associated with polysomes in plant mitochondria. J Mol Biol. 2008;375:626–636. doi: 10.1016/j.jmb.2007.11.011.
   PubMed Web of Science ®Google Scholar
• Waltz F, Nguyen T-T, Arrivé M, et al. Small is big in Arabidopsis mitochondrial ribosome. Nat Plants. 2019;5:106–117. doi: 10.1038/s41477-018-0339-y.
   PubMed Web of Science ®Google Scholar
• Haïli N, Planchard N, Arnal N, et al. The MTL1 pentatricopeptide repeat protein is required for both translation and splicing of the mitochondrial NADH dehydrogenase subunit7 mRNA in Arabidopsis. Plant Physiol. 2016;170:354–366. doi: 10.1104/pp.15.01591.
   PubMed Web of Science ®Google Scholar
• Lange H, Sement FM, Canaday J, et al. Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci. 2009;14:497–504. doi: 10.1016/j.tplants.2009.06.007.
   PubMed Web of Science ®Google Scholar
• Hirayama T, Matsuura T, Ushiyama S, et al. A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis. Nat Commun. 2013;4:2247. doi: 10.1038/ncomms3247.
   PubMed Web of Science ®Google Scholar
• Kanazawa M, Ikeda Y, Nishihama R, et al. Regulation of the poly(A) status of mitochondrial mRNA by poly(A)-specific ribonuclease is conserved among land plants. Plant Cell Physiol. 2020;61:470–480. doi: 10.1093/pcp/pcz212.
   PubMed Web of Science ®Google Scholar
• Otsuka K, Mamiya A, Konishi M, et al. Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis. eLife. 2021;10:e61611. doi: 10.7554/eLife.61611.
   PubMed Web of Science ®Google Scholar
• Hartmann RK, Gössringer M, Späth B, et al. The making of tRNAs and more - RNase P and tRNase Z. Prog Mol Biol Transl Sci. 2009;85:319–368.
   PubMed Web of Science ®Google Scholar
• Bollenbach TJ, Lange H, Gutierrez R, et al. RNR1, a 3’-5’ exoribonuclease belonging to the RNA superfamily, catalyzes 3’ maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res. 2005;33:2751–2763. doi: 10.1093/nar/gki576.
   PubMed Web of Science ®Google Scholar
• Takahashi A, Sugita C, Ichinose M, et al. Moss PPR-SMR protein PpPPR_64 influences the expression of a psaA-psaB-rps14 gene cluster and processing of the 23S–4.5S rRNA precursor in chloroplasts. Plant Mol Biol. 2021;107:417–429. doi: 10.1007/s11103-020-01090-z.
   PubMed Web of Science ®Google Scholar
• Schiffer S, Rösch S, Marchfelder A. Assigning a function to a conserved group of proteins: the tRNA 3′-processing enzymes. Embo J. 2002;21:2769–2777. doi: 10.1093/emboj/21.11.2769.
   PubMed Web of Science ®Google Scholar
• Canino G, Bocian E, Barbezier N, et al. Arabidopsis encodes four tRNase Z enzymes. Plant Physiol. 2009;150:1494–1502. doi: 10.1104/pp.109.137950.
   PubMed Web of Science ®Google Scholar
• Duchêne A-M, Pujol C, Maréchal-Drouard L. Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet. 2009;55:1–18. doi: 10.1007/s00294-008-0223-9.
   PubMed Web of Science ®Google Scholar
• Zhou W, Karcher D, Bock R. Identification of enzymes for adenosine-to-inosine editing and discovery of cytidine-to-uridine editing in nucleus-encoded transfer RNAs of Arabidopsis. Plant Physiol. 2014;166:1985–1997. doi: 10.1104/pp.114.250498.
   PubMed Web of Science ®Google Scholar
• Delannoy E, Le Ret M, Faivre-Nitschke E, et al. Arabidopsis tRNA adenosine deaminase arginine edits the wobble nucleotide of chloroplast tRNA Arg(ACG) and is essential for efficient chloroplast translation. Plant Cell. 2009;21:2058–2071. doi: 10.1105/tpc.109.066654.
   PubMed Web of Science ®Google Scholar
• Manavski N, Vicente A, Chi W, et al. The chloroplast epitranscriptome: factors, sites, regulation, and detection methods. Genes. 2021;12:1121. doi: 10.3390/genes12081121.
   PubMed Web of Science ®Google Scholar
• Wang Z, Tang K, Zhang D, et al. High-throughput m6A-seq reveals RNA m6A methylation patterns in the chloroplast and mitochondria transcriptomes of Arabidopsis thaliana. PLOS One. 2017;12:e0185612. doi: 10.1371/journal.pone.0185612.
   PubMed Web of Science ®Google Scholar
• Murik O, Chandran SA, Nevo-Dinur K, et al. Topologies of N6 -adenosine methylation (m6 A) in land plant mitochondria and their putative effects on organellar gene expression. Plant J. 2020;101:1269–1286. doi: 10.1111/tpj.14589.
   PubMed Web of Science ®Google Scholar
• Tokuhisa JG, Vijayan P, Feldmann KA, et al. Chloroplast development at low temperatures requires a homolog of DIM1, a yeast gene encoding the 18S rRNA dimethylase. Plant Cell. 1998;10:699–711. doi: 10.1105/tpc.10.5.699.
   PubMed Web of Science ®Google Scholar
• Richter U, Kühn K, Okada S, et al. A mitochondrial rRNA dimethyladenosine methyltransferase in Arabidopsis. Plant J. 2010;61:558–569. doi: 10.1111/j.1365-313X.2009.04079.x.
   PubMed Web of Science ®Google Scholar
• Tieu Ngoc LN, Jung Park S, Thi Huong T, et al. N4-methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis. J Integr Plant Biol. 2021;63:570–582. doi: 10.1111/jipb.13009.
   PubMed Web of Science ®Google Scholar
• Ngoc LNT, Park SJ, Cai J, et al. RsmD, a chloroplast rRNA m2G methyltransferase, plays a role in cold stress tolerance by possibly affecting chloroplast translation in Arabidopsis. Plant Cell Physiol. 2021;62:948–958. doi: 10.1093/pcp/pcab060.
   PubMed Web of Science ®Google Scholar
• Adachi H, Zoysa MDD, Yu Y-T. Post-transcriptional pseudouridylation in mRNA as well as in some major types of noncoding RNAs. Biochim Biophys Acta Gene Regul Mech. 2019;1862:230–239. doi: 10.1016/j.bbagrm.2018.11.002.
   PubMed Web of Science ®Google Scholar
• Wang Z, Sun J, Zu X, et al. Pseudouridylation of chloroplast ribosomal RNA contributes to low temperature acclimation in rice. New Phytol. 2022;236:1708–1720. doi: 10.1111/nph.18479.
   PubMed Web of Science ®Google Scholar
• Yu F, Liu X, Alsheikh M, et al. Mutations in suppressor of variegation1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell. 2008;20:1786–1804. doi: 10.1105/tpc.107.054965.
   PubMed Web of Science ®Google Scholar
• Niu Y, Zheng Y, Zhu H, et al. The Arabidopsis mitochondrial pseudouridine synthase homolog FCS1 plays critical roles in plant development. Plant Cell Physiol. 2022;63:955–966. doi: 10.1093/pcp/pcac060.
   PubMed Web of Science ®Google Scholar
• Zhang J, Khan SA, Hasse C, et al. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science. 2015;347:991–994. doi: 10.1126/science.1261680.
   PubMed Web of Science ®Google Scholar
• Maliga P, Bock R. Plastid biotechnology: food, fuel, and medicine for the 21st century1. Plant Physiol. 2011;155:1501–1510. doi: 10.1104/pp.110.170969.
   PubMed Web of Science ®Google Scholar
• Long BM, Hee WY, Sharwood RE, et al. Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts. Nat Commun. 2018;9:3570. doi: 10.1038/s41467-018-06044-0.
   PubMed Web of Science ®Google Scholar
• Hanson MR, Lin MT, Carmo-Silva AE, et al. Towards engineering carboxysomes into C3 plants. Plant J. 2016;87:38–50. doi: 10.1111/tpj.13139.
   PubMed Web of Science ®Google Scholar
• Colas Des Francs-Small C, Vincis Pereira Sanglard L, Small I. Targeted cleavage of nad6 mRNA induced by a modified pentatricopeptide repeat protein in plant mitochondria. Commun Biol. 2018;1:166. doi: 10.1038/s42003-018-0166-8.
   PubMed Web of Science ®Google Scholar
• Shen C, Wang X, Liu Y, et al. Specific RNA recognition by designer pentatricopeptide repeat protein. Mol Plant. 2015;8:667–670. doi: 10.1016/j.molp.2015.01.001.
   PubMed Web of Science ®Google Scholar
• Royan S, Gutmann B, Colas Des Francs-Small C, et al. A synthetic RNA editing factor edits its target site in chloroplasts and bacteria. Commun Biol. 2021;4:545. doi: 10.1038/s42003-021-02062-9.
   PubMed Web of Science ®Google Scholar
• Yu Q, Barkan A, Maliga P. Engineered RNA-binding protein for transgene activation in non-green plastids. Nat Plants. 2019;5:486–490. doi: 10.1038/s41477-019-0413-0.
   PubMed Web of Science ®Google Scholar
• Rojas M, Yu Q, Williams-Carrier R, et al. Engineered PPR proteins as inducible switches to activate the expression of chloroplast transgenes. Nat Plants. 2019;5:505–511. doi: 10.1038/s41477-019-0412-1.
   PubMed Web of Science ®Google Scholar