Journal of Molecular Evolution

, Volume 67, Issue 3, pp 233–245 | Cite as

High Conservation of a 5′ Element Required for RNA Editing of a C Target in Chloroplast psbE Transcripts

Article

Abstract

C-to-U editing modifies 30–40 distinct nucleotides within higher-plant chloroplast transcripts. Many C targets are located at the same position in homologous genes from different plants; these either could have emerged independently or could share a common origin. The 5′ sequence GCCGUU, required for editing of C214 in tobacco psbE in vitro, is one of the few identified editing cis-elements. We investigated psbE sequences from many plant species to determine in what lineage(s) editing of psbE C214 emerged and whether the cis-element identified in tobacco is conserved in plants with a C214. The GCCGUU sequence is present at a high frequency in plants that carry a C214 in psbE. However, Sciadopitys verticillata (Pinophyta) edits C214 despite the presence of nucleotide differences compared to the conserved cis-element. The C214 site in psbE genes is represented in members of four branches of spermatophytes but not in gnetophytes, resulting in the parsimonious prediction that editing of psbE C214 was present in the ancestor of spermatophytes. Extracts from chloroplasts from a species that has a difference in the motif and lacks the C target are incapable of editing tobacco psbE C214 substrates, implying that the critical trans-acting protein factors were not retained without a C target. Because noncoding sequences are less constrained than coding regions, we analyzed sequences 5′ to two C editing targets located within coding regions to search for possible editing-related conserved elements. Putative editing cis-elements were uncovered in the 5′ UTRs near editing sites psbL C2 and ndhD C2.

Keywords

Plastid RNA processing Phylogeny psbE ndhD psbL 

Supplementary material

239_2008_9101_MOESM1_ESM.xls (290 kb)
[Editing Sites Present in Three Homologous Chloroplast Genes from a Collection of Diverse Species] (XLS 290 kb)
239_2008_9101_MOESM2_ESM.xls (40 kb)
[Editing Sites Present in Three Homologous Chloroplast Genes from a Collection of Diverse Species] (XLS 40 kb)
239_2008_9101_MOESM3_ESM.pdf (134 kb)
[An alignment of psbE sequences around the editing site in Sciadopitys verticillata and homologous sequences in other members of the Conifer II clade defined by Bowe, Coat, and dePamphilis (2000). The nucleotide at the editing site position is indicated by a character in a larger font. Nucleotides that are different from Araucaria bidwillii are represented by grey characters. The 6 nucleotide motif necessary for editing of a tobacco substrate in vitro is depicted by a black box and is underlined] (PDF 134 kb)

References

  1. Bock R, Hagemann R, Kossel H, Kudla J (1993) Tissue- and stage-specific modulation of RNA editing of the psbF and psbL transcript from spinach plastids—a new regulatory mechanism? Mol Gen Genet 240:238–244PubMedCrossRefGoogle Scholar
  2. Bowe LM, Coat G, dePamphilis CW (2000) Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proc Natl Acad Sci USA 97:4092–4097PubMedCrossRefGoogle Scholar
  3. Chateigner-Boutin AL, Hanson MR (2002) Cross-competition in transgenic chloroplasts expressing single editing sites reveals shared cis elements. Mol Cell Biol 22:8448–8456PubMedCrossRefGoogle Scholar
  4. Chaudhuri S, Maliga P (1996) Sequences directing C to U editing of the plastid psbL mRNA are located within a 22 nucleotide segment spanning the editing site. EMBO J 15:5958–5964PubMedGoogle Scholar
  5. Corneille S, Lutz K, Maliga P (2000) Conservation of RNA editing between rice and maize plastids: are most editing events dispensable? Mol Gen Genet 264:419–424PubMedCrossRefGoogle Scholar
  6. Covello PS, Gray MW (1993) On the evolution of RNA editing. Trends Genet 9:265–268PubMedCrossRefGoogle Scholar
  7. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  8. Freyer R, Kiefer-Meyer MC, Kossel H (1997) Occurrence of plastid RNA editing in all major lineages of land plants. Proc Natl Acad Sci USA 94:6285–6290PubMedCrossRefGoogle Scholar
  9. Funk HT, Berg S, Krupinska K, Maier UG, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 7:45PubMedCrossRefGoogle Scholar
  10. Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24:1068–1074PubMedCrossRefGoogle Scholar
  11. Hayes ML, Hanson MR (2007a) Assay of editing of exogenous RNAs in chloroplast extracts of Arabidopsis, maize, pea, and tobacco. Methods Enzymol 424:459–482PubMedCrossRefGoogle Scholar
  12. Hayes ML, Hanson MR (2007b) Identification of a sequence motif critical for editing of a tobacco chloroplast transcript. RNA 13:281–288PubMedCrossRefGoogle Scholar
  13. Hayes ML, Reed ML, Hegeman CE, Hanson MR (2006) Sequence elements critical for efficient RNA editing of a tobacco chloroplast transcript in vivo and in vitro. Nucleic Acids Res 34:3742–3754PubMedCrossRefGoogle Scholar
  14. Hegeman CE, Hayes ML, Hanson MR (2005) Substrate and cofactor requirements for RNA editing of chloroplast transcripts in Arabidopsis in vitro. Plant J 42:124–132PubMedCrossRefGoogle Scholar
  15. Hirose T, Kusumegi T, Tsudzuki T, Sugiura M (1999) RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity. Mol Gen Genet 262:462–467PubMedCrossRefGoogle Scholar
  16. Kahlau S, Aspinall S, Gray JC, Bock R (2006) Sequence of the tomato chloroplast DNA and evolutionary comparison of solanaceous plastid genomes. J Mol Evol 63:194–207PubMedCrossRefGoogle Scholar
  17. Kudla J, Bock R (1999) RNA editing in an untranslated region of the Ginkgo chloroplast genome. Gene 234:81–86PubMedCrossRefGoogle Scholar
  18. Lopez-Serrano M, Del Campo EM, Sabater B, Martin M (2001) Primary transcripts of ndhD of Liliaceae and Aloaceae require editing of the start and 20th codons. J Exp Bot 52:179–180PubMedCrossRefGoogle Scholar
  19. Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730PubMedCrossRefGoogle Scholar
  20. Maier RM, Neckermann K, Igloi GL, Kossel H (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251:614–628PubMedCrossRefGoogle Scholar
  21. Malek O, Lattig K, Hiesel R, Brennicke A, Knoop V (1996) RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J 15:1403–1411PubMedGoogle Scholar
  22. Miyamoto T, Obokata J, Sugiura M (2002) Recognition of RNA editing sites is directed by unique proteins in chloroplasts: biochemical identification of cis-acting elements and trans-acting factors involved in RNA editing in tobacco and pea chloroplasts. Mol Cell Biol 22:6726–6734PubMedCrossRefGoogle Scholar
  23. Miyamoto T, Obokata J, Sugiura M (2004) A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts. Proc Natl Acad Sci USA 101:48–52PubMedCrossRefGoogle Scholar
  24. Ng PC, Henikoff S (2006) Predicting the effects of amino acid substitutions on protein function. Annu Rev Genomics Hum Genet 7:61–80PubMedCrossRefGoogle Scholar
  25. Revill MJ, Stanley S, Hibberd JM (2005) Plastid genome structure and loss of photosynthetic ability in the parasitic genus Cuscuta. J Exp Bot 56:2477–2486PubMedCrossRefGoogle Scholar
  26. Sasaki T, Yukawa Y, Miyamoto T, Obokata J, Sugiura M (2003) Identification of RNA editing sites in chloroplast transcripts from the maternal and paternal progenitors of tobacco (Nicotiana tabacum): comparative analysis shows the involvement of distinct trans-factors for ndhB editing. Mol Biol Evol 20:1028–1035PubMedCrossRefGoogle Scholar
  27. Schmitz-Linneweber C, Regel R, Du TG, Hupfer H, Herrmann RG, Maier RM (2002) The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: the role of RNA editing in generating divergence in the process of plant speciation. Mol Biol Evol 19:1602–1612PubMedGoogle Scholar
  28. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM (2005) Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase alpha-subunit mRNA. Plant Cell 17:1815–1828PubMedCrossRefGoogle Scholar
  29. Shields DC, Wolfe KH (1997) Accelerated evolution of sites undergoing mRNA editing in plant mitochondria and chloroplasts. Mol Biol Evol 14:344–349PubMedGoogle Scholar
  30. Stefanovic S, Krueger L, Olmstead RG (2002) Monophyly of the Convolvulaceae and circumscription of their major lineages based on DNA sequences of multiple chloroplast loci. Am J Bot 89:1510–1522CrossRefGoogle Scholar
  31. Sugiura M (2008) RNA editing in chloroplasts. In: Göringer HU (ed) RNA editing. Nucleic acids and molecular biology. Springer-Verlag, Berlin, pp 123–142Google Scholar
  32. Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier RM (2005) Editing of plastid RNA in Arabidopsis thaliana ecotypes. Plant J 43:708–715PubMedCrossRefGoogle Scholar
  33. Tillich M, Lehwark P, Morton BR, Maier UG (2006) The evolution of chloroplast RNA editing. Mol Biol Evol 23:1912–1921PubMedCrossRefGoogle Scholar
  34. Tsudzuki T, Wakasugi T, Sugiura M (2001) Comparative analysis of RNA editing sites in higher plant chloroplasts. J Mol Evol 53:327–332PubMedCrossRefGoogle Scholar
  35. Wakasugi T, Hirose T, Horihata M, Tsudzuki T, Kossel H, Sugiura M (1996) Creation of a novel protein-coding region at the RNA level in black pine chloroplasts: the pattern of RNA editing in the gymnosperm chloroplast is different from that in angiosperms. Proc Natl Acad Sci USA 93:8766–8770PubMedCrossRefGoogle Scholar
  36. Wojciechowski M, Lavin M, Sanderson M (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862CrossRefGoogle Scholar
  37. Wolf PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:89–97PubMedCrossRefGoogle Scholar
  38. Wu CS, Wang YN, Liu SM, Chaw SM (2007) Chloroplast genome (cpDNA) of Cycas taitungensis and 56 Cp protein-coding genes of Gnetum parvifolium: insights into cpDNA evolution and phylogeny of extant seed plants. Mol Biol Evol 24:1366–1379PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of Molecular Biology and GeneticsCornell UniversityIthacaUSA

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