Abstract
Key message
Upon loss of either its chloroplast or mitochondrial target, a uniquely dual-targeted factor for C-to-U RNA editing in angiosperms reveals low evidence for improved molecular adaptation to its remaining target.
Abstract
RNA-binding pentatricopeptide repeat (PPR) proteins specifically recognize target sites for C-to-U RNA editing in the transcriptomes of plant chloroplasts and mitochondria. Among more than 80 PPR-type editing factors that have meantime been characterized, AEF1 (or MPR25) is a special case given its dual targeting to both organelles and addressing an essential mitochondrial (nad5eU1580SL) and an essential chloroplast (atpFeU92SL) RNA editing site in parallel in Arabidopsis. Here, we explored the angiosperm-wide conservation of AEF1 and its two organelle targets. Despite numerous independent losses of the chloroplast editing site by C-to-T conversion and at least four such conversions at the mitochondrial target site in other taxa, AEF1 remains consistently conserved in more than 120 sampled angiosperm genomes. Not a single case of simultaneous loss of the chloroplast and mitochondrial editing target or of AEF1 disintegration or loss could be identified, contrasting previous findings for editing factors targeted to only one organelle. Like in most RNA editing factors, the PPR array of AEF1 reveals potential for conceptually “improved fits” to its targets according to the current PPR-RNA binding code. Surprisingly, we observe only minor evidence for adaptation to the mitochondrial target also after deep losses of the chloroplast target among Asterales, Caryophyllales and Poales or, vice versa, for the remaining chloroplast target after a deep loss of the mitochondrial target among Malvales. The evolutionary observations support the notion that PPR-RNA mismatches may be essential for proper function of editing factors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Andrés-Colás N, Zhu Q, Takenaka M, De Rybel B, Weijers D, Van Der Straeten D (2017) Multiple PPR protein interactions are involved in the RNA editing system in Arabidopsis mitochondria and plastids. Proc Natl Acad Sci USA 114:8883–8888. https://doi.org/10.1073/pnas.1705815114
Angiosperm Phylogeny Group IV (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20. https://doi.org/10.1111/boj.12385
Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, Small I (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8:e1002910. https://doi.org/10.1371/journal.pgen.1002910
Bentolila S, Heller WP, Sun T, Babina AM, Friso G, van Wijk KJ, Hanson MR (2012) RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proc Natl Acad Sci USA 109:E1453–E1661. https://doi.org/10.1073/pnas.1121465109
Boussardon C, Salone V, Avon A, Berthome R, Hammani K, Okuda K, Shikanai T, Small I, Lurin C (2012) Two interacting proteins are necessary for the editing of the ndhD-1 site in Arabidopsis plastids. Plant Cell 24:3684–3694
Boussardon C, Avon A, Kindgren P, Bond CS, Challenor M, Lurin C, Small I (2014) The cytidine deaminase signature HxE(x)nCxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. New Phytol 203:1090–1095. https://doi.org/10.1111/nph.12928
Carrie C, Small I (2013) A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim Biophys Acta 1833:253–259. https://doi.org/10.1016/J.BBAMCR.2012.05.029
Cheng S, Gutmann B, Zhong X, Ye Y, Fisher MF, Bai F, Castleden I, Song Y, Song B, Huang J, Liu X, Xu X, Lim BL, Bond CS, Yiu S-M, Small I (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J 85:532–547. https://doi.org/10.1111/tpj.13121
Colcombet J, Lopez-Obando M, Heurtevin L, Bernard C, Martin K, Berthomé R, Lurin C (2013) Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles. RNA Biol 10:1557–1575. https://doi.org/10.4161/rna.26128
Daniell H, Wurdack KJ, Kanagaraj A, Lee S-B, Saski C, Jansen RK (2008) The complete nucleotide sequence of the cassava (Manihot esculenta) chloroplast genome and the evolution of atpF in Malpighiales: RNA editing and multiple losses of a group II intron. Theor Appl Genet 116:723–737. https://doi.org/10.1007/s00122-007-0706-y
Diaz MF, Bentolila S, Hayes ML, Hanson MR, Mulligan RM (2017) A protein with an unusually short PPR domain, MEF8, affects editing at over 60 Arabidopsis mitochondrial C targets of RNA editing. Plant J 92:638–649. https://doi.org/10.1111/tpj.13709
Doyle JLJJ, Doyle JLJJ (1990) Isolation of plant DNA from fresh tissue. Focus (Madison) 12:13–15
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. NatProtoc 2:953–971
Geiss KT, Abbas GM, Makaroff CA (1994) Intron loss from the nadh dehydrogenase subunit 4 gene of lettuce mitochondrial DNA - evidence for homologous recombination of a cDNA intermediate. Mol Gen Genet 243:97–105
Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104
Grewe F, Zhu A, Mower JP (2016) Loss of a Trans-Splicing nad1 Intron from Geraniaceae and Transfer of the Maturase Gene matR to the Nucleus in Pelargonium. Genome Biol Evol 8:3193–3201. https://doi.org/10.1093/gbe/evw233
Guillaumot D, Lopez-Obando M, Baudry K, Avon A, Rigaill G, Falcon de Longevialle A, Broche B, Takenaka M, Berthomé R, De Jaeger G, Delannoy E, Lurin C (2017) Two interacting PPR proteins are major Arabidopsis editing factors in plastid and mitochondria. Proc Natl Acad Sci USA 114:8877–8882. https://doi.org/10.1073/pnas.1705780114
Gutmann B, Royan S, Small I (2017) Protein complexes implicated in RNA editing in plant organelles. Mol Plant 10:1255–1257. https://doi.org/10.1016/J.MOLP.2017.09.011
Hayes ML, Giang K, Mulligan RM (2012) Molecular evolution of pentatricopeptide repeat genes reveals truncation in species lacking an editing target and structural domains under distinct selective pressures. BMC Evol Biol 12:66. https://doi.org/10.1186/1471-2148-12-66
Hayes ML, Dang KN, Diaz MF, Mulligan RM (2015) A conserved glutamate residue in the C-terminal deaminase domain of pentatricopeptide repeat proteins is required for RNA editing activity. J Biol Chem 290:10136–101342. https://doi.org/10.1074/jbc.M114.631630
He S, Sun Y, Yang Q, Zhang X, Huang Q, Zhao P, Sun M, Liu J, Qian W, Qin G, Gu H, Qu LJ (2017) A novel imprinted gene NUWA controls mitochondrial function in early seed development in Arabidopsis. PLoS Genet. https://doi.org/10.1371/journal.pgen.1006553
Hein A, Knoop V (2018) Expected and unexpected evolution of plant RNA editing factors CLB19, CRR28 and RARE1: retention of CLB19 despite a phylogenetically deep loss of its two known editing targets in Poaceae. BMC Evol Biol 18:85. https://doi.org/10.1186/s12862-018-1203-4
Hein A, Polsakiewicz M, Knoop V (2016) Frequent chloroplast RNA editing in early-branching flowering plants: pilot studies on angiosperm-wide coexistence of editing sites and their nuclear specificity factors. BMC Evol Biol 16:23. https://doi.org/10.1186/s12862-016-0589-0
Hein A, Brenner S, Knoop V (2019) Multifarious evolutionary pathways of a nuclear RNA editing factor: disjunctions in co-evolution of DOT4 and its chloroplast target rpoC1eU488SL. Genome Biol Evol 11:798–813. https://doi.org/10.1093/gbe/evz032
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587
Ichinose M, Sugita M (2016) RNA editing and its molecular mechanism in plant organelles. Genes (Basel) 8:5. https://doi.org/10.3390/genes8010005
Ichinose M, Tasaki E, Sugita C, Sugita M (2012) A PPR-DYW protein is required for splicing of a group II intron of cox1 pre-mRNA in Physcomitrella patens. Plant J Cell Mol Biol 70:271–278. https://doi.org/10.1111/j.1365-313X.2011.04869.x
Iyer LM, Zhang D, Rogozin IB, Aravind L (2011) Evolution of the deaminase fold and multiple origins of eukaryotic editing and mutagenic nucleic acid deaminases from bacterial toxin systems. Nucleic Acids Res 39:9473–9497. https://doi.org/10.1093/nar/gkr691
Jenkins BD, Kulhanek DJ, Barkan A (1997) Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9:283–296
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Knoop V, Rüdinger M (2010) DYW-type PPR proteins in a heterolobosean protist: plant RNA editing factors involved in an ancient horizontal gene transfer? FEBS Lett 584:4287–4291. https://doi.org/10.1016/j.febslet.2010.09.041
Knoop V, Schuster W, Wissinger B, Brennicke A (1991) Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J 10:3483–3493
Kobayashi T, Yagi Y, Nakamura T (2019) Comprehensive prediction of target RNA editing sites for PLS-class PPR proteins in Arabidopsis thaliana. Plant Cell Physiol 60:862–874. https://doi.org/10.1093/pcp/pcy251
Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lenz H, Hein A, Knoop V (2018) Plant organelle RNA editing and its specificity factors: enhancements of analyses and new database features in PREPACT 30. BMC Bioinform 19:255. https://doi.org/10.1186/s12859-018-2244-9
Liao Z, Chen M, Guo L, Gong Y, Tang F, Sun X, Tang K (2004) Rapid isolation of high-quality total RNA from taxus and ginkgo. Prep Biochem Biotechnol 34:209–214. https://doi.org/10.1081/PB-200026790
Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette M-L, Mireau H, Peeters N, Renou J-P, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103. https://doi.org/10.1105/tpc.104.022236
Mower JP, Touzet P, Gummow JS, Delph LF, Palmer JD (2007) Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol Biol 7:135. https://doi.org/10.1186/1471-2148-7-135
Oldenkott B, Yang Y, Lesch E, Knoop V, Schallenberg-Rüdinger M (2019) Plant-type pentatricopeptide repeat proteins with a DYW domain drive C-to-U RNA editing in Escherichia coli. Commun Biol 2:85. https://doi.org/10.1038/s42003-019-0328-3
Ostersetzer O, Cooke AM, Watkins KP, Barkan A (2005) CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell 17:241–255. https://doi.org/10.1105/tpc.104.027516
Park S, Grewe F, Zhu A, Ruhlman TA, Sabir J, Mower JP, Jansen RK (2015) Dynamic evolution of Geranium mitochondrial genomes through multiple horizontal and intracellular gene transfers. New Phytol 208:570–583. https://doi.org/10.1111/nph.13467
Ran JH, Gao H, Wang XQ (2010) Fast evolution of the retroprocessed mitochondrial rps3 gene in Conifer II and further evidence for the phylogeny of gymnosperms. Mol Phylogenet Evol 54:136–149
Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, Barry K, Boore JL, Zhang Y, DePamphilis CW, Knox EB, Palmer JD (2013) Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342:1468–1473. https://doi.org/10.1126/science.1246275
Rüdinger M, Polsakiewicz M, Knoop V (2008) Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat (PPR) proteins in jungermanniid but not in marchantiid liverworts. Mol Biol Evol 25:1405–1414
Rüdinger M, Szövényi P, Rensing SASA, Knoop V (2011) Assigning DYW-type PPR proteins to RNA editing sites in the funariid mosses Physcomitrella patens and Funaria hygrometrica. Plant J 67:370–380. https://doi.org/10.1111/j.1365-313X.2011.04600.x
Rüdinger M, Volkmar U, Lenz H, Groth-Malonek M, Knoop V (2012) Nuclear DYW-type PPR gene families diversify with increasing RNA editing frequencies in liverwort and moss mitochondria. J Mol Evol 74:37–51. https://doi.org/10.1007/s00239-012-9486-3
Ruwe H, Gutmann B, Schmitz-Linneweber C, Small I, Kindgren P, Schmitz-Linneweber C, Small I, Kindgren P (2019) The E domain of CRR2 participates in sequence-specific recognition of RNA in plastids. New Phytol 222:218–229. https://doi.org/10.1111/nph.15578
Salone V, Rüdinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, Szurek B, Small I, Knoop V, Lurin C (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581:4132–4138. https://doi.org/10.1016/j.febslet.2007.07.075
Schallenberg-Rüdinger M, Knoop V (2016) Coevolution of organelle RNA editing and nuclear specificity factors in early land plants. In: Rensing SA (ed) Genomes and evolution of charophytes, bryophytes and ferns. Advances in botanical research, vol 78. Elsevier, Amsterdam, pp 37–93
Schallenberg-Rüdinger M, Lenz H, Polsakiewicz M, Gott JM, Knoop V (2013) A survey of PPR proteins identifies DYW domains like those of land plant RNA editing factors in diverse eukaryotes. RNA Biol 10:1549–1556. https://doi.org/10.4161/rna.25755
Sharma M, Bennewitz B, Klösgen RB (2018) Rather rule than exception? How to evaluate the relevance of dual protein targeting to mitochondria and chloroplasts. Photosynth Res. https://doi.org/10.1007/s11120-018-0543-7
Shikanai T (2015) RNA editing in plants: machinery and flexibility of the site recognition. Biochim Biophys Acta 1874:779–785. https://doi.org/10.1016/j.bbabio.2014.12.010
Sloan DB, Barr CM, Olson MS, Keller SR, Taylor DR (2008) Evolutionary rate variation at multiple levels of biological organization in plant mitochondrial DNA. Mol Biol Evol 25:243–246
Sloan DB, MacQueen AH, Alverson AJ, Palmer JD, Taylor DR (2010) Extensive loss of RNA editing sites in rapidly evolving Silene mitochondrial genomes: selection vs. retroprocessing as the driving force. Genetics 185:1369–1380. https://doi.org/10.1534/genetics.110.118000
Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241. https://doi.org/10.1371/journal.pbio.1001241
Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590
Sperschneider J, Catanzariti A-M, DeBoer K, Petre B, Gardiner DM, Singh KB, Dodds PN, Taylor JM (2017) LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell. Sci Rep 7:44598. https://doi.org/10.1038/srep44598
Sun T, Bentolila S, Hanson MR (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21:926–973. https://doi.org/10.1016/j.tplants.2016.07.005
Takenaka M (2014) How complex are the editosomes in plant organelles? Mol Plant 7:582–585. https://doi.org/10.1093/mp/sst170
Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Härtel B, Brennicke A (2012) Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc Natl Acad Sci 109:5104–5109. https://doi.org/10.1073/pnas.1202452109
Takenaka M, Zehrmann A, Brennicke A, Graichen K (2013) Improved computational target site prediction for pentatricopeptide repeat RNA editing factors. PLoS ONE 8:e65343. https://doi.org/10.1371/journal.pone.0065343
Takenaka M, Jörg A, Burger M, Haag S (2019) RNA editing mutants as surrogates for mitochondrial SNP mutants. Plant Physiol Biochem 135:310–321. https://doi.org/10.1016/J.PLAPHY.2018.12.014
Till B, Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2001) CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7:1227–1238
Toda T, Fujii S, Noguchi K, Kazama T, Toriyama K (2012) Rice MPR25 encodes a pentatricopeptide repeat protein and is essential for RNA editing of nad5 transcripts in mitochondria. Plant J 72:450–460. https://doi.org/10.1111/j.1365-313X.2012.05091.x
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235. https://doi.org/10.1093/nar/gkw256
Xu L, Carrie C, Law SR, Murcha MW, Whelan J (2013) Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiol 161:644–662. https://doi.org/10.1104/pp.112.210997
Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T (2013) Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants. PLoS ONE 8:e57286
Yan J, Yao Y, Hong S, Yang Y, Shen C, Zhang Q, Zhang D, Zou T, Yin P (2019) Delineation of pentatricopeptide repeat codes for target RNA prediction. Nucleic Acids Res 47:3728–3738. https://doi.org/10.1093/nar/gkz075
Yap A, Kindgren P, Colas des Francs-Small C, Kazama T, Tanz SK, Toriyama K, Small I (2015) AEF1/MPR25 is implicated in RNA editing of plastid atpF and mitochondrial nad5 and also promotes atpF splicing in Arabidopsis and rice. Plant J 81:661–669. https://doi.org/10.1111/tpj.12756
Zehrmann A, Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21:558–567. https://doi.org/10.1105/tpc.108.064535
Zumkeller SM, Knoop V, Knie N (2016) Convergent evolution of fern-specific mitochondrial group II intron atp1i361g2 and its ancient source paralogue rps3i249g2 and independent losses of intron and RNA editing among Pteridaceae. Genome Biol Evol 8:2505–2519. https://doi.org/10.1093/gbe/evw173
Author information
Authors and Affiliations
Contributions
AH did analysis of sequence data and conducted phylogenetic analysis, SB and MP did nucleic acid preparations, PCR amplifications and molecular cloning, VK designed and supervised the study and wrote the manuscript, AH and VK prepared figures and edited the final manuscript.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hein, A., Brenner, S., Polsakiewicz, M. et al. The dual-targeted RNA editing factor AEF1 is universally conserved among angiosperms and reveals only minor adaptations upon loss of its chloroplast or its mitochondrial target. Plant Mol Biol 102, 185–198 (2020). https://doi.org/10.1007/s11103-019-00940-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-019-00940-9