RNA Editing: Evolutionary Implications

Abstract

The term ‘ribonucleic acid (RNA) editing’ describes a variety of mechanistically unrelated biochemical activities that alter RNA molecules after transcription by addition, deletion or substitution of nucleotides. Examples include insertion and deletion of uridine residues in the mitochondrial messenger RNAs (mRNAs) of kinetoplastid protozoa; cytidine‐to‐uridine deamination of specific residues in the mitochondrial mRNAs and transfer RNAs (tRNAs) of land plants; conversion of adenosine to inosine via deamination in the nuclear transcripts of metazoan animals; and replacement of nonbase‐paired nucleotides at the 5′ and 3′ ends of certain mitochondrial tRNAs. A three‐stage ‘constructive neutral evolution’ (CNE) model, illustrated by specific examples, can explain in a general way how RNA‐editing systems might arise and become fixed. The CNE model proposes that potential editing systems arise before there is an actual requirement for editing, thereby serving to relax functional constraints at the genome level because harmful/lethal mutations are able to be reversed at the level of the corresponding transcript.

Key Concepts:

  • RNA editing is a process (typically post‐transcriptional) that alters the nucleotide sequence of an RNA molecule relative to the corresponding gene sequence.

  • Two general types of RNA editing are recognised: (1) insertional, in which nucleotides are added to (and also deleted from) internal positions and (2) substitutional, in which one nucleotide type replaces another at particular positions.

  • All types of cellular RNA (messenger, transfer and ribosomal) may undergo editing, as well as intron, noncoding and viral sequences.

  • RNA‐editing systems are almost exclusively restricted to eukaryotes, and are especially prominent in chloroplasts and mitochondria.

  • RNA‐editing systems are clearly derived traits, arising relatively recently within particular eukaryotic lineages.

  • RNA‐editing systems are mechanistically diverse and biochemically distinct, pointing to numerous separate evolutionary origins.

  • A ‘constructive neutral evolution’ (CNE) model provides a general explanation for the emergence of diverse RNA‐editing systems.

  • A basic tenet of the CNE model is that potential RNA‐editing systems arise before there is a need for editing.

  • The emergence of an RNA‐editing system allows fixation of otherwise deleterious mutations that can be ‘repaired’ by RNA editing.

Keywords: RNA editing; evolution; coevolution; genetic drift; selection; insertional editing; substitutional editing; deamination; tRNA editing

Figure 1.

Editing of a portion of the messenger RNA encoding subunit 2 of cytochrome oxidase (COX2). (a) Insertional editing by U addition in the mitochondria of Trypanosoma brucei, a kinetoplastid protozoan. (b) Substitutional editing involving C‐to‐U changes in the mitochondria of wheat, a flowering plant. Nucleotides added (in (a)) or changed (in (b)) by editing are shown in green. Red arrows indicate differences between the nucleotide sequences of the gene and the corresponding edited RNA. Differences between the amino acid sequences inferred from the gene (‘unedited’) and from the mature mRNA (‘edited’) are shown in blue bold.

close

References

Abad MG, Long Y, Willcox A et al. (2011) A role for tRNAHis guanylyltransferase (Thg1)‐like proteins from Dictyostelium discoideum in mitochondrial 5′ tRNA editing. RNA 17: 613–623.

Abad MG, Rao BS and Jackman JE (2010) Template‐dependent 3′‐5′ nucleotide addition is a shared feature of tRNAHis guanylyltransferase enzymes from multiple domains of life. Proceedings of the National Academy of Sciences of the USA 107: 674–679.

Bock R (2001) RNA editing in plant mitochondria and chloroplasts. In: Bass BL (ed.) RNA Editing, pp. 38–60. Oxford: Oxford University Press.

Bullerwell CE and Gray MW (2005) In vitro characterization of a tRNA editing activity in the mitochondria of Spizellomyces punctatus, a chytridiomycete fungus. Journal of Biological Chemistry 280: 2463–2470.

Castandet B and Araya A (2012) The nucleocytoplasmic conflict, a driving force for the emergence of plant organellar RNA editing. IUBMB Life 64: 120–125.

Cavalier‐Smith T (1997) Cell and genome coevolution: facultative anaerobiosis, glycosomes and kinetoplastan RNA editing. Trends in Genetics 13: 6–9.

Chan L, Chang BH‐J, Nakamuta M, Li W‐H and Smith LC (1997) Apobec‐1 and apolipoprotein B mRNA editing. Biochimica et Biophysica Acta 1345: 11–26.

Covello PS and Gray MW (1993) On the evolution of RNA editing. Trends in Genetics 9: 265–268.

Driscoll DM and Innerarity TL (2001) RNA editing by cytidine deamination in mammals. In: Bass BL (ed.) RNA Editing, pp. 61–76. Oxford: Oxford University Press.

Emeson RB and Singh M (2001) Adenosine‐to‐inosine RNA editing: substrates and consequences. In: Bass BL (ed.) RNA Editing, pp. 109–138. Oxford: Oxford University Press.

Fujii S and Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. New Phytologist 191: 37–47.

Gerber A, Grosjean H, Melcher T and Keller W (1998) Tad1p, a yeast tRNA‐specific adenosine deaminase, is related to the mammalian pre‐mRNA editing enzymes ADAR1 and ADAR2. EMBO Journal 17: 4780–4789.

Gerber AP and Keller W (1999) An adenosine deaminase that generates inosine at the wobble position of tRNAs. Science 286: 1146–1149.

Gott JM (2001) RNA editing in Physarum polycephalum. In: Bass BL (ed.) RNA Editing, pp. 20–37. Oxford: Oxford University Press.

Gott JM and Visomirski‐Robic LM (1998) RNA editing in Physarum mitochondria. In: Grosjean H and Benne R (eds) Modification and Editing of RNA, pp. 395–411. Washington DC: ASM Press.

Gott JM, Somerlot BH and Gray MW (2010) Two forms of RNA editing are required for tRNA maturation in Physarum mitochondria. RNA 16: 482–488.

Gray MW and Covello PS (1993) RNA editing in plant mitochondria and chloroplasts. FASEB Journal 7: 64–71.

Hajduk SL and Sabatini RS (1998) Mitochondrial mRNA editing in kinetoplastid protozoa. In: Grosjean H and Benne R (eds) Modification and Editing of RNA, pp. 377–393. Washington DC: ASM Press.

Jackman JE, Gott JM and Gray MW (2012) Doing it in reverse: 3′‐to‐5′ polymerization by the Thg1 superfamily. RNA 18: 886–899.

Jobson RW and Qiu Y‐L (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biology Direct 3: 43.

Keegan L, Leroy A, Sproul D and O'Connell M (2004) Adenosine deaminases acting on RNA (ADARs): RNA‐editing enzymes. Genome Biology 5: 209.

Kiethega GN, Turcotte M and Burger G (2011) Evolutionarily conserved cox1 trans‐splicing without cis‐motifs. Molecular Biology and Evolution 28: 2425–2428.

Laforest M‐J, Roewer I and Lang BF (1997) Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus: tRNA editing and UAG ‘stop’ codons recognized as leucine. Nucleic Acids Research 25: 626–632.

Lavrov DV, Brown WM and Boore JL (2000) A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proceedings of the National Academy of Sciences of the USA 97: 13738–13742.

Lin S, Zhang H, Spencer DF, Norman JE and Gray MW (2002) Widespread and extensive editing of mitochondrial mRNAs in dinoflagellates. Journal of Molecular Biology 320: 727–739.

Lukeš J, Archibald JM, Keeling PJ, Doolittle WF and Gray MW (2011) How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life 63: 528–537.

Marchfelder A, Binder S, Brennicke A and Knoop V (1998) RNA editing by base conversion in plant organellar RNAs. In: Grosjean H and Benne R (eds) Modification and Editing of RNA, pp. 307–323. Washington DC: ASM Press.

Navaratnam N, Bhattacharya S, Fujino T et al. (1995) Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA‐binding motif at its active site. Cell 81: 187–195.

Price DH and Gray MW (1998) Editing of tRNA. In: Grosjean H and Benne R (eds) Modification and Editing of RNA, pp. 289–305. Washington DC: ASM Press.

Price DH and Gray MW (1999) A novel nucleotide incorporation activity implicated in the editing of mitochondrial tRNAs in Acanthamoeba castellanii. RNA 5: 302–317.

Randau L, Stanley BJ, Kohlway A et al. (2009) A cytidine deaminase edits C to U in transfer RNAs in Archaea. Science 324: 657–659.

Rao BS, Maris EL and Jackman JE (2011) tRNA 5′‐repair activities of tRNAHis guanylyltransferase (Thg1)‐like proteins from Bacteria and Archaea. Nucleic Acids Research 39: 1833–1842.

Rueter SM and Emeson RB (1998) Adenosine‐to‐inosine conversion in mRNA. In: Grosjean H and Benne R (eds) Modification and Editing of RNA, pp. 343–361. Washington DC: ASM Press.

Schmitz‐Linneweber C and Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends in Plant Science 13: 663–670.

Speijer D (2006) Is kinetoplastid pan‐editing the result of an evolutionary balancing act? IUBMB Life 58: 91–96.

Spencer DF and Gray MW (2011) Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome. Molecular Genetics and Genomics 285: 19–31.

Stoltzfus A (1999) On the possibility of constructive neutral evolution. Journal of Molecular Evolution 49: 169–181.

Stuart KD, Panigrahi AK and Salavati R (2001) RNA editing in kinetoplastid mitochondria. In: Bass BL (ed) RNA Editing, pp. 1–19. Oxford: Oxford University Press.

Further Reading

Gray MW (2001) Speculations on the origin and evolution of editing. In: Bass BL (eds) RNA Editing, pp. 160–184. Oxford: Oxford University Press.

Gray MW (2003) Diversity and evolution of mitochondrial RNA editing systems. IUBMB Life 55: 227–233.

Gray MW (2012) Evolutionary origin of RNA editing. Biochemistry 51: 5235–5242.

Gray MW, Lukeš J, Archibald JA, Keeling PJ and Doolittle WF (2010) Irremediable complexity? Science 330: 920–921.

Hayes ML and Mulligan RM (2011) Pentatricopeptide repeat proteins constrain genome evolution in chloroplasts. Molecular Biology and Evolution 28: 2029–2049.

Knoop V (2011) When you can't trust the DNA: RNA editing changes transcript sequences. Cellular and Molecular Life Sciences 68: 567–586.

Simpson L (1999) RNA editing – an evolutionary perspective. In: Gesteland R, Cech T and Atkins JF (eds) The RNA World, 2nd edn, pp. 585–608. New York: Cold Spring Harbor Laboratory Press.

Simpson L and Maslov DA (1999) Evolution of the U‐insertion/deletion RNA editing in mitochondria of kinetoplastid protozoa. Annals of the New York Academy of Sciences 870: 190–205.

Stoltzfus A (2012) Constructive neutral evolution: exploring evolutionary theory's curious disconnect. Biology Direct 7: 35.

Tillich M, Lehwark P, Morton BR and Maier UG (2006) The evolution of chloroplast RNA editing. Molecular Biology and Evolution 23: 1912–1921.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Gray, Michael W(Jun 2013) RNA Editing: Evolutionary Implications. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0003069.pub3]