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Many Independent Origins of trans Splicing of a Plant Mitochondrial Group II Intron

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Abstract

We examined the cis- vs. trans-splicing status of the mitochondrial group II intron nad1i728 in 439 species (427 genera) of land plants, using both Southern hybridization results (for 416 species) and intron sequence data from the literature. A total of 164 species (157 genera), all angiosperms, was found to have a trans-spliced form of the intron. Using a multigene land plant phylogeny, we infer that the intron underwent a transition from cis to trans splicing 15 times among the sampled angiosperms. In 10 cases, the intron was fractured between its 5′ end and the intron-encoded matR gene, while in the other 5 cases the fracture occurred between matR and the 3′ end of the intron. The 15 intron fractures took place at different time depths during the evolution of angiosperms, with those in Nymphaeales, Austrobaileyales, Chloranthaceae, and eumonocots occurring early in angiosperm evolution and those in Syringodium filiforme, Hydrocharis morsus-ranae, Najas, and Erodium relatively recently. The trans-splicing events uncovered in Austrobaileyales, eumonocots, Polygonales, Caryophyllales, Sapindales, and core Rosales reinforce the naturalness of these major clades of angiosperms, some of which have been identified solely on the basis of recent DNA sequence analyses.

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References

  • KL Adams DO Daley Y-L Qiu J Whelan JD Palmer (2000) ArticleTitleRepeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants Nature 408 354–357 Occurrence Handle10.1038/35042567 Occurrence Handle1:CAS:528:DC%2BD3cXosVektb0%3D Occurrence Handle11099041

    Article  CAS  PubMed  Google Scholar 

  • KL Adams Y-L Qiu M Stoutemyer JD Palmer (2002) ArticleTitlePunctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer during angiosperm evolution Proc Natl Acad Sci USA 99 9905–9912 Occurrence Handle10.1073/pnas.042694899 Occurrence Handle1:CAS:528:DC%2BD38XlslKgsb0%3D Occurrence Handle12119382

    Article  CAS  PubMed  Google Scholar 

  • DC Albach PS Soltis DE Soltis RG Olmstead (2001) ArticleTitlePhylogenetic analysis of asterids based on sequences of four genes Ann Mo Bot Gard 88 163–212 Occurrence Handle10.1006/anbo.2001.1429

    Article  Google Scholar 

  • C Andre A Levy V Walbot (1992) ArticleTitleSmall repeated sequences and the structure of plant mitochondrial genomes Trends Genet 8 128–132 Occurrence Handle10.1016/0168-9525(92)90370-J Occurrence Handle1:STN:280:By2A3snjslA%3D Occurrence Handle1631955

    Article  CAS  PubMed  Google Scholar 

  • S Beckert H Muhle D Pruchner V Knoop (2001) ArticleTitleThe mitochondrial nad2 gene as a novel marker locus for phylogenetic analysis among early land plants: A comparative analysis in mosses Mol Phylogenet Evol 18 117–126 Occurrence Handle10.1006/mpev.2000.0868 Occurrence Handle1:CAS:528:DC%2BD3MXmt1Wruw%3D%3D Occurrence Handle11161748

    Article  CAS  PubMed  Google Scholar 

  • H-D Behnke (1988) ArticleTitleSieve-element plastids, phloem protein, and evolution of flowering plants: III. Magnoliidae Taxon 37 699–732

    Google Scholar 

  • S Binder A Marchfelder A Brennicke B Wissinger (1992) ArticleTitleRNA editing in trans-splicing intron sequences of nad2 mRNAs in Oenothera mitochondria J Biol Chem 267 7615–7623 Occurrence Handle1:CAS:528:DyaK3sXhs1egtLs%3D Occurrence Handle1559998

    CAS  PubMed  Google Scholar 

  • Y Chapdelaine L Bonen (1991) ArticleTitleThe wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: A trans-splicing model for this gene-in-pieces Cell 65 465–472 Occurrence Handle1:CAS:528:DyaK3MXmt1Gjt7k%3D Occurrence Handle1902143

    CAS  PubMed  Google Scholar 

  • MW Chase DE Soltis RG Olmstead et al. (1993) ArticleTitlePhylogenetics of seed plants: An analysis of nucleotide sequences from the plastid gene rbcL Ann Mo Bot Gard 80 528–580

    Google Scholar 

  • MW Chase MR Duvall HG Hills et al. (1995a) Molecular phylogenetics of Lilianae PJ Rudall PJ Cribb DF Cutler CJ Humphries (Eds) Monocotyledons: Systematics and evolution Royal Botanic Gardens Kew 109–137

    Google Scholar 

  • MW Chase DW Stevenson P Wilkin PJ Rudall (1995b) Monocot systematics: A combined analysis PJ Rudall PJ Cribb DF Cutler CJ Humphries (Eds) Monocotyledons: Systematics and evolution Royal Botanic Gardens Kew 685–730

    Google Scholar 

  • MW Chase DE Soltis PS Soltis et al. (2000) Higher-level systematics of the monocotyledons: An assessment of current knowledge and a new classification KL Wilson DA Morrison (Eds) Monocots: Systematics and evolution CSIRO Melbourne 3–16

    Google Scholar 

  • S-M Chaw CL Parkinson Y Cheng TM Vincent JD Palmer (2000) ArticleTitleSeed plant phylogeny inferred from all three plant genomes: Monophyly of extant gymnosperms and origin of Gnetales from conifers Proc Natl Acad Sci USA 97 4086–4091 Occurrence Handle10.1073/pnas.97.8.4086 Occurrence Handle1:CAS:528:DC%2BD3cXislSgtb4%3D Occurrence Handle10760277

    Article  CAS  PubMed  Google Scholar 

  • Y Cho Y-L Qiu P Kuhlman JD Palmer (1998) ArticleTitleExplosive invasion of plant mitochondria by a group I intron Proc Natl Acad Sci USA 95 14244–14249 Occurrence Handle10.1073/pnas.95.24.14244 Occurrence Handle1:CAS:528:DyaK1cXns1Gmu7s%3D Occurrence Handle9826685

    Article  CAS  PubMed  Google Scholar 

  • PL Conklin RK Wilson MR Hanson (1991) ArticleTitleMultiple trans-splicing events are required to produce a mature nad1 transcript in a plant mitochondrion Genes Dev 5 1407–1415 Occurrence Handle1:CAS:528:DyaK38XksVWlsLs%3D Occurrence Handle1869047

    CAS  PubMed  Google Scholar 

  • P Cuenoud V Savolainen LW Chatrou M Powell RJ Grayer MW Chase (2002) ArticleTitleMolecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences Am J Bot 89 132–144 Occurrence Handle1:CAS:528:DC%2BD3sXjvFOksw%3D%3D

    CAS  Google Scholar 

  • L Dai S Zimmerly (2002) ArticleTitleCompilation and analysis of group II intron insertions in bacterial genomes: Evidence for retroelement behavior Nucleic Acids Res 30 1091–1102 Occurrence Handle10.1093/nar/30.5.1091 Occurrence Handle1:CAS:528:DC%2BD38XitVOisb8%3D Occurrence Handle11861899

    Article  CAS  PubMed  Google Scholar 

  • AP Souza Particlede M-F Jubier E Delcher D Lancelin B Lejeune (1991) ArticleTitleA trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria Plant Cell 3 1363–1378 Occurrence Handle10.1105/tpc.3.12.1363 Occurrence Handle1726722

    Article  PubMed  Google Scholar 

  • O Dombrovska Y-L Qiu (2004) ArticleTitleDistribution of introns in the mitochondrial gene nad1 in land plants: Phylogenetic and molecular evolutionary implications Mol Phylogenet Evol . .

    Google Scholar 

  • JJ Doyle JS Doyle (1987) ArticleTitleA rapid DNA isolation procedure for small quantities of fresh leaf tissue Phytochem Bull 19 11–15

    Google Scholar 

  • PK Endress A Igersheim (1997) ArticleTitleGynoecium diversity and systematics of the Laurales Bot J Linn Soc 125 93–168 Occurrence Handle10.1006/bojl.1997.0113

    Article  Google Scholar 

  • C Fauron M Casper Y Gao B Moore (1995) ArticleTitleThe maize mitochondrial genome: dynamic, yet functional Trends Genet 11 228–235 Occurrence Handle10.1016/S0168-9525(00)89056-3 Occurrence Handle1:CAS:528:DyaK2MXmtFSntLw%3D Occurrence Handle7638905

    Article  CAS  PubMed  Google Scholar 

  • JC French MG Chung YK Hur (1995) Chloroplast DNA phylogeny of the Ariflorae PJ Rudall PJ Cribb DF Cutler CJ Humphries (Eds) Monocotyledons: Systematics and evolution Royal Botanic Gardens Kew 255–275

    Google Scholar 

  • EM Friis K Pedersen PR Crane (2001) ArticleTitleFossil evidence of water lilies (Nymphaeales) in the Early Cretaceous Nature 410 357–360 Occurrence Handle10.1038/35066557 Occurrence Handle1:STN:280:DC%2BD3M7mvVaquw%3D%3D Occurrence Handle11268209

    Article  CAS  PubMed  Google Scholar 

  • H Fukuzawa T Kohchi H Shirai K Ohyama K Umesono H Inokuchi H Ozeki (1986) ArticleTitleCoding sequences for chloroplast ribosomal protein S-12 from the liverwort Marchantia polymorpha are separated far apart on the different DNA strands FEBS Lett 198 11–15 Occurrence Handle10.1016/0014-5793(86)81174-7 Occurrence Handle1:CAS:528:DyaL28XitF2ru74%3D

    Article  CAS  Google Scholar 

  • M Goldschmidt-Clermont Y Choquet J Girard-Bascou F Michel M Schirmer-Rahire J-D Rochaix (1991) ArticleTitleA small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii Cell 65 135–143 Occurrence Handle10.1016/0092-8674(91)90415-U Occurrence Handle1:CAS:528:DyaK3MXks1GrsL8%3D Occurrence Handle1707343

    Article  CAS  PubMed  Google Scholar 

  • SW Graham RG Olmstead (2000) ArticleTitleUtility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms Am J Bot 87 1712–1730 Occurrence Handle1:CAS:528:DC%2BD3cXosleit7k%3D Occurrence Handle11080123

    CAS  PubMed  Google Scholar 

  • F Gugerli C Sperisen U Büchler I Brunner S Brodbeck JD Palmer Y-L Qiu (2001) ArticleTitleThe evolutionary split of Pinaceae from other conifers: Evidence from an intron loss and a multigene phylogeny Mol Phylog Evol 21 167–175 Occurrence Handle10.1006/mpev.2001.1004 Occurrence Handle1:CAS:528:DC%2BD3MXotVynur8%3D

    Article  CAS  Google Scholar 

  • K Hashimoto N Sato (2001) ArticleTitleCharacterization of the mitochondrial nad7 gene in Physcomitrella patens: Similarity with angiosperm nad7 genes Plant Sci 160 807–815 Occurrence Handle10.1016/S0168-9452(00)00444-1 Occurrence Handle1:CAS:528:DC%2BD3MXisF2ktLc%3D Occurrence Handle11297777

    Article  CAS  PubMed  Google Scholar 

  • RK Jansen JD Palmer (1987) ArticleTitleA chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae) Proc Natl Acad Sci USA 84 5818–5822 Occurrence Handle1:CAS:528:DyaL2sXlt1ygtbg%3D

    CAS  Google Scholar 

  • S Joly L Brouillet A Bruneau (2001) ArticleTitlePhylogenetic implications of the multiple losses of the mitochondrial coxII.i3 intron in the angiosperms Int J Plant Sci 162 359–373 Occurrence Handle10.1086/319586 Occurrence Handle1:CAS:528:DC%2BD3MXjtFKgtbw%3D

    Article  CAS  Google Scholar 

  • V Knoop W Schuster B Wissinger A Brennicke (1991) ArticleTitle Trans-splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria EMBO J 10 3483–3493 Occurrence Handle1:CAS:528:DyaK3sXhtFyjsL8%3D Occurrence Handle1915303

    CAS  PubMed  Google Scholar 

  • V Knoop M Unseld J Marienfeld P Brandt S Sunkel H Ullrich A Brennicke (1996) ArticleTitleCopia-, gypsy and LINE-like retrotransposon fragments in the mitochondrial genome of Arabidopsis thaliana Genetics 142 579–585 Occurrence Handle1:CAS:528:DyaK28XhsFKjs7s%3D Occurrence Handle8852855

    CAS  PubMed  Google Scholar 

  • V Knoop M Altwasser A Brennicke (1997) ArticleTitleA tripartite group II intron in mitochondria of an angiosperm plant Mol Gen Genet 255 269–276 Occurrence Handle10.1007/s004380050497 Occurrence Handle1:CAS:528:DyaK2sXlsFers78%3D Occurrence Handle9268017

    Article  CAS  PubMed  Google Scholar 

  • B Koller H Fromm E Galun M Edelman (1987) ArticleTitleEvidence for in vivo trans splicing of premessenger-RNAs in tobacco chloroplasts Cell 48 111–119 Occurrence Handle10.1016/0092-8674(87)90361-8 Occurrence Handle1:CAS:528:DyaL1cXltVCjtQ%3D%3D Occurrence Handle3791410

    Article  CAS  PubMed  Google Scholar 

  • WJ Kress LM Prince WJ Hahn EA Zimmer (2001) ArticleTitleUnraveling the evolutionary radiation of the families of the Zingiberales using morphological and molecular evidence Syst Biol 50 926–944 Occurrence Handle10.1080/106351501753462885 Occurrence Handle1:STN:280:DC%2BD38zntVKltg%3D%3D Occurrence Handle12116641

    Article  CAS  PubMed  Google Scholar 

  • T Kubo S Nishizawa A Sugawara N Itchoda A Estiati T Mikami (2000) ArticleTitleThe complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys (GCA) Nucleic Acids Res 28 2571–2576 Occurrence Handle10.1093/nar/28.13.2571 Occurrence Handle1:CAS:528:DC%2BD3cXlvFWqsLg%3D Occurrence Handle10871408

    Article  CAS  PubMed  Google Scholar 

  • U Kück Y Choquet M Schneider M Dron P Bennoun (1987) ArticleTitleStructural and transcriptional analysis of two homologous genes for the P700 chlorophyll alpha apoproteins in Chlamydomonas reinhardtii: Evidence for in vivo trans-splicing EMBO J 6 2185–2196

    Google Scholar 

  • J Kudla FJ Albertazzi D Blazevic M Hermann R Bock (2002) ArticleTitleLoss of the mitochondrial cox2 intron 1 in a family of monocotyledonous plants and utilization of mitochondrial intron sequences for the construction of a nuclear intron Mol Genet Genom 267 223–230 Occurrence Handle10.1007/s00438-002-0657-6 Occurrence Handle1:CAS:528:DC%2BD38XkvVentbY%3D

    Article  CAS  Google Scholar 

  • DH Les MA Cleland M Waycott (1997) ArticleTitlePhylogenetic studies in Alismatidae. II: Evolution of marine angiosperms (seagrasses) and hydrophily Syst Bot 22 443–463

    Google Scholar 

  • KA Lew JR Manhart (1993) ArticleTitleThey rps12 gene in Spirogyra maxima (Chlorophyta) and its evolutionary significance J Phycol 29 500–505 Occurrence Handle1:CAS:528:DyaK2cXhvVChur0%3D

    CAS  Google Scholar 

  • DJ Mabberley (1987) The plant book Cambridge University Press Cambridge

    Google Scholar 

  • O Malek V Knoop (1998) ArticleTitleTrans-splicing group II introns in plant mitochondria: The complete set of cis-arranged homologs in ferns, fern allies, and a hornwort RNA 4 1599–1609 Occurrence Handle10.1017/S1355838298981262 Occurrence Handle1:CAS:528:DyaK1cXnvFOgs7s%3D Occurrence Handle9848656

    Article  CAS  PubMed  Google Scholar 

  • O Malek A Brennicke V Knoop (1997) ArticleTitleEvolution of trans-splicing plant mitochondrial introns in pre-Permian times Proc Natl Acad Sci USA 94 553–558 Occurrence Handle10.1073/pnas.94.2.553 Occurrence Handle1:CAS:528:DyaK2sXnslegtg%3D%3D Occurrence Handle9012822

    Article  CAS  PubMed  Google Scholar 

  • JR Manhart JD Palmer (1990) ArticleTitleThe gain of two chloroplast tRNA introns marks the green algal ancestors of land plants Nature 345 268–270 Occurrence Handle10.1038/345268a0 Occurrence Handle1:CAS:528:DyaK3MXhsVWg Occurrence Handle2333097

    Article  CAS  PubMed  Google Scholar 

  • S Mathews MJ Donoghue (1999) ArticleTitleThe root of angiosperm phylogeny inferred from duplicate phytochrome genes Science 286 947–950 Occurrence Handle10.1126/science.286.5441.947 Occurrence Handle1:CAS:528:DyaK1MXntFaktbg%3D Occurrence Handle10542147

    Article  CAS  PubMed  Google Scholar 

  • Y Notsu S Masood T Nishikawa N Kubo G Akiduki M Nakazono A Hirai K Kadowaki (2002) ArticleTitleThe complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants Mol Genet Genom 268 434–445 Occurrence Handle10.1007/s00438-002-0767-1 Occurrence Handle1:CAS:528:DC%2BD38XptlWltb0%3D Occurrence Handle12471441

    Article  CAS  PubMed  Google Scholar 

  • JD Palmer LA Herbon (1988) ArticleTitlePlant mitochondrial DNA evolves rapidly in structure, but slowly in sequence J Mol Evol 28 87–97 Occurrence Handle1:CAS:528:DyaL1MXhvFejuw%3D%3D Occurrence Handle3148746

    CAS  PubMed  Google Scholar 

  • CL Parkinson KL Adams JD Palmer (1999) ArticleTitleMultigene analyses identify the three earliest lineages of extant flowering plants Curr Biol 9 1481–1485 Occurrence Handle10.1016/S0960-9822(00)80119-0 Occurrence Handle10607595

    Article  PubMed  Google Scholar 

  • D Pruchner B Nassal M Schindler V Knoop (2001) ArticleTitleMosses share mitochondrial group II introns with flowering plants, not with liverworts Mol Genet Genom 266 608–613 Occurrence Handle10.1007/s004380100577 Occurrence Handle1:CAS:528:DC%2BD38XnsVGjuw%3D%3D

    Article  CAS  Google Scholar 

  • KM Pryer H Schneider AR Smith R Cranfill PG Wolf JS Hunt SD Sipes (2001) ArticleTitleHorsetails and ferns are a monophyletic group and the closest relatives to seed plants Nature 409 618–622 Occurrence Handle10.1038/35054555 Occurrence Handle1:STN:280:DC%2BD3M7islSntw%3D%3D Occurrence Handle11214320

    Article  CAS  PubMed  Google Scholar 

  • Y-L Qiu JD Palmer (1997) Mitochondrial genome evolution and land plant phylogeny SR Wessler M Freeling EM Meyerowitz (Eds) Proceedings of the Keystone Symposia on Molecular and Cellular Biology: Evolution of Plant Development Taos NM 21

    Google Scholar 

  • Y-L Qiu MW Chase DH Les CR Parks (1993) ArticleTitleMolecular phylogenetics of the Magnoliidae: cladistic analyses of nucleotide sequences of the plastid gene rbcL Ann Mo Bot Gard 80 587–606

    Google Scholar 

  • Y-L Qiu Y Cho JC Cox JD Palmer (1998a) ArticleTitleThe gain of three mitochondrial introns identifies liverworts as the earliest land plants Nature 394 671–674 Occurrence Handle10.1038/29286 Occurrence Handle1:CAS:528:DyaK1cXlsFKmsLY%3D

    Article  CAS  Google Scholar 

  • Y-L Qiu MW Chase SB Hoot E Conti PR Crane KJ Sytsma CR Parks (1998b) ArticleTitlePhylogenetics of the Hamamelidae and their allies: parsimony analyses of nucleotide sequences of the plastid gene rbcL Int J Plant Sci 159 891–905 Occurrence Handle10.1086/297611 Occurrence Handle1:CAS:528:DyaK1MXptlCr

    Article  CAS  Google Scholar 

  • Y-L Qiu J Lee F Bernasconi-Quadroni DE Soltis PS Soltis M Zanis EA Zimmer Z Chen V Savolainen MW Chase (1999) ArticleTitleThe earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes Nature 402 404–407 Occurrence Handle10.1038/46536 Occurrence Handle1:STN:280:DC%2BD3c%2Flt1WlsA%3D%3D Occurrence Handle10586879

    Article  CAS  PubMed  Google Scholar 

  • Y-L Qiu J Lee F Bernasconi-Quadroni DE Soltis PS Soltis M Zanis EA Zimmer Z Chen V Savolainen MW Chase (2000) ArticleTitlePhylogeny of basal angiosperms: Analyses of five genes from three genomes Int J Plant Sci 161 S3–S27 Occurrence Handle10.1086/317584 Occurrence Handle1:CAS:528:DC%2BD3cXos1Oqs74%3D

    Article  CAS  Google Scholar 

  • MF Rabbi KG Wilson (1993) ArticleTitleThe mitochondrial coxII intron has been lost in two different lineages of dicots and altered in others Am J Bot 80 1216–1223

    Google Scholar 

  • LA Raubeson RK Jansen (1992) ArticleTitleChloroplast DNA evidence on the ancient evolutionary split in vascular land plants Science 255 1697–1699 Occurrence Handle1:CAS:528:DyaK38XitFWhsb4%3D

    CAS  Google Scholar 

  • DE Soltis PS Soltis MW, Chase et al. (2000) ArticleTitleAngiosperm phylogeny inferred from 18S rDNA, rbcL and atpB sequences Bot J Linn Soc 133 381–461 Occurrence Handle10.1006/bojl.2000.0380

    Article  Google Scholar 

  • DW Stevenson H Loconte (1995) Cladistic analysis of monocot families PJ Rudall PJ Cribb DF Cutler CJ Humphries (Eds) Monocotyledons: Systematics and evolution Royal Botanic Gardens Kew 543–578

    Google Scholar 

  • MC Thomson JL MacFarlane CT Beagley DR Wolstenholme (1994) ArticleTitleRNA editing of mat-r transcripts in maize and soybean increases similarity of the encoded protein to fungal and bryophyte group II intron maturases: evidence that mat-r encodes a functional protein Nucleic Acids Res 22 5745–5752 Occurrence Handle1:CAS:528:DyaK2MXjtlGitrs%3D Occurrence Handle7838731

    CAS  PubMed  Google Scholar 

  • M Turmel C Otis C Lemieux (2002a) ArticleTitleThe complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and a highly compact mitochondrial genome in the ancestor of all green plants Mol Biol Evol 19 24–38 Occurrence Handle1:CAS:528:DC%2BD38XhtFCjuw%3D%3D

    CAS  Google Scholar 

  • M Turmel C Otis C Lemieux (2002b) ArticleTitleThe chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: Insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants Proc Natl Acad Sci USA 99 11275–11280 Occurrence Handle10.1073/pnas.162203299 Occurrence Handle1:CAS:528:DC%2BD38XmslSmtbs%3D

    Article  CAS  Google Scholar 

  • M Unseld JR Marienfeld P Brand A Brennicke (1997) ArticleTitleThe mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides Nature Genet 15 57–61 Occurrence Handle1:CAS:528:DyaK2sXjsFSiuw%3D%3D Occurrence Handle8988169

    CAS  PubMed  Google Scholar 

  • GRJ Upchurch (1984) ArticleTitleCuticle evolution in Early Cretaceous angiosperms from the Potomac Group of Virginia and Maryland Ann Mo Bot Gard 71 522–550

    Google Scholar 

  • JA Wahleithner JL MacFarlane DR Wolstenholme (1990) ArticleTitleA sequence encoding a maturase-related protein in a group II intron of a plant mitochondrial nad1 gene Proc Natl Acad Sci USA 87 548–552 Occurrence Handle1:CAS:528:DyaK3cXhslegtbs%3D Occurrence Handle2300546

    CAS  PubMed  Google Scholar 

  • N Wikstrom V Savolainen MW Chase (2001) ArticleTitleEvolution of the angiosperms: Calibrating the family tree Proc Roy Soc Lond B 268 2211–2220 Occurrence Handle10.1098/rspb.2001.1782 Occurrence Handle1:STN:280:DC%2BD3MrmvVKmtQ%3D%3D

    Article  CAS  Google Scholar 

  • JH Williams WE Friedman (2002) ArticleTitleIdentification of diploid endosperm in an early angiosperm lineage Nature 415 522–526 Occurrence Handle10.1038/415522a Occurrence Handle11823859

    Article  PubMed  Google Scholar 

  • B Wissinger W Schuster A Brennicke (1991) ArticleTitleTrans-splicing in Oenothera mitochondria: nad1 mRNA are edited in exon and trans-splicing group II intron sequences Cell 65 473–482 Occurrence Handle1:CAS:528:DyaK3MXmt1Gjt7Y%3D Occurrence Handle1850322

    CAS  PubMed  Google Scholar 

  • N Zaita K Torazawa K Shinozaki M Sugiura (1987) ArticleTitle Trans splicing in vivo joining of transcripts from the divided gene for ribosomal protein S12 in the chloroplasts of tobacco FEBS Lett 210 153–156 Occurrence Handle10.1016/0014-5793(87)81326-1 Occurrence Handle1:CAS:528:DyaL2sXpslansw%3D%3D

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Keming Song for technical help, Joe Peters for making a test version of the Immobilon-Ny+ transfer membranes available to us, and Olena Dombrovska for providing us a preprint. This work was supported by an NIH postdoctoral fellowship (GM17923-01), an NSF Career Award (DEB 0093012) to Y.-L.Q., and an NIH research grant to J.D.P. (GM-35087).

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  1. Department of Biology, Indiana University, Bloomington, IN, 47405, USA

    Yin-Long Qiu & Jeffrey D. Palmer

  2. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109, USA

    Yin-Long Qiu

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Correspondence to Yin-Long Qiu.

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Qiu, YL., Palmer, J.D. Many Independent Origins of trans Splicing of a Plant Mitochondrial Group II Intron. J Mol Evol 59, 80–89 (2004). https://doi.org/10.1007/s00239-004-2606-y

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