RNA Editing in Plants and Its Evolution

GE47CH15-Takenaka ARI 29 October 2013 14:23
ANNUAL
REVIEWS Further
RNA Editing in Plants
Click here for quick links to
Annual Reviews content online,
including:
and Its Evolution
Other articles in this volume
Top cited articles Mizuki Takenaka, Anja Zehrmann, Daniil Verbitskiy,
Access provided by Universidade Federal de Vicosa on 12/12/14. For personal use only.
Top downloaded articles

Our comprehensive search Barbara Hartel, and Axel Brennicke
Annu. Rev. Genet. 2013.47:335-352. Downloaded from www.annualreviews.org
Molekulare Botanik, Universitat Ulm, 89069 Ulm, Germany;

email: mizuki.takenaka@uni-ulm.de, anja.zehrmann@uni-ulm.de,
daniil.verbitskiy@uni-ulm.de, barbara.haertel@uni-ulm.de, mo.bo@uni-ulm.de
Annu. Rev. Genet. 2013. 47:33552 Keywords

The Annual Review of Genetics is online at
genet.annualreviews.org mitochondria, plastids, PPR proteins, MORF proteins, cytidine
deamination, RNA-protein interaction
This articles doi:
10.1146/annurev-genet-111212-133519
Abstract
Copyright c 2013 by Annual Reviews.
All rights reserved RNA editing alters the identity of nucleotides in RNA molecules such
that the information for a protein in the mRNA differs from the predic-
tion of the genomic DNA. In chloroplasts and mitochondria of ow-
ering plants, RNA editing changes C nucleotides to U nucleotides; in
ferns and mosses, it also changes U to C. The approximately 500 editing
sites in mitochondria and 40 editing sites in plastids of owering plants
are individually addressed by specic proteins, genes for which are am-
plied in plant species with organellar RNA editing. These proteins
contain repeat elements that bind to cognate RNA sequence motifs just
5 to the edited nucleotide. In owering plants, the site-specic proteins
interact selectively with individual members of a different, smaller fam-
ily of proteins. These latter proteins may be connectors between the
site-specic proteins and the as yet unknown deaminating enzymatic
activity.
335
INTRODUCTION Another species-specic feature is the dis-

tribution of the U-to-C reverse reaction RNA
The term RNA editing describes processes
editing, which occurs only in ferns, mosses,
RNA editing: that alter the identity of nucleotides in RNA
posttranscriptional and Lycopodiaceae in addition to many C-to-
molecules or that add or delete nucleotides so
modication of RNA U changes (Figure 1b) (24, 42). In ower-
that the information in the mature RNA dif-
that changes the ing plants, posttranscriptional mRNA editing
fers from that dened in the genome. Diverse
information content is performed generally as C-to-U alterations of
processes of RNA editing are found in viruses,
nucleotide identity (22).
primitive eukaryotes, vertebrates, fungi, and
Most of the RNA-editing events occur at
plants. RNA-editing processes are used as con-
the rst or second positions of codons and thus
trol checkpoints, can restore the function of the
usually alter the codon given in the genome
encoded protein, and can create different pro-
and transcribed into the precursor mRNA (pre-
teins. Excellent reviews of the various processes
mRNA) (Figure 1a). Consequently, the ma-
in different organisms have recently appeared
ture RNA species a different amino acid than

and describe their mechanistic and functional
that encoded by the genomic DNA. To pre-

aspects and their origins (1, 23, 40, 56, 64, 88).
dict the nal protein sequence synthesized from
Here, we focus on the RNA-editing process in
a given gene, it is therefore not sufcient to
land plants in which this is an essential step of
determine the genomic sequence because only
RNA maturation in the two organelles with res-
the mature mRNA sequence contains this in-
ident genomes: mitochondria and plastids (14,
formation. The C-to-U RNA editing can alter
21, 37, 70).
any codon containing a C nucleotide, including
the generation of initiation codons by changing
RNA EDITING IN PLANTS ACG to AUG and the introduction of transla-
In owering plants (angiosperms), RNA editing tion termination signals by changing CGA to
was rst recognized in mitochondria in 1989 as UGA or CAA to UAA. Conversely, the U-to-
sequence differences between DNA and RNA C RNA editing found in mosses and ferns can
(16, 27, 32). These differences of U nucleotides convert translational stop codons, such as UAA
in the RNA in positions of C nucleotides in termination signals, to a CAA triplet coding for
the DNA were found to be caused by substitu- the amino acid glycine. The nal open reading
tional C-to-U changes in the RNA (Figure 1a). frames can thus not only become different from
The amino acid codons specied after editing those originally encoded by the genome but can
are more similar to those present at the re- also be extended or shortened.
spective positions of orthologous proteins in RNA editing in plant organelles is a post-
other organisms. Three years later, the same transcriptional process. The competence of
type of RNA editing involving C-to-U changes lysates from mitochondria or plastids to faith-
was also documented in plastids (33). Editing fully edit an in vitro synthesized and added RNA
in both organelles was subsequently reported molecule shows that this editing does not de-
in all land plants, including all major plant lin- pend on a close link to the transcription ma-
eages from the bryophytes to gymnosperms and chinery (7, 30, 55, 63, 76, 84, 85). However,
in all angiosperms (73, 74, 78, 91). The notable only a few sites can be edited in vitro, suggest-
exceptions are some species of liverworts in the ing that often the editing activity may require
branch of the Marchantiales, in which the mes- a complex machinery of several proteins that is
senger RNAs (mRNAs) remain as specied by not readily assembled on in vitroadded RNA
the genomes in plastids as well as in mitochon- molecules.
dria (Figure 1b) (66). At present, no RNA edit- The C-to-U and the U-to-C types of RNA
ing has been observed in cytoplasmic RNAs of editing occur in plastids and in plant mi-
plants. The process seems to be conned to the tochondria in not only mRNAs but also in
two organelles. transfer RNAs (tRNAs), introns, and 5 - and
336 Takenaka et al.

a Primary Ala Thr Arg Gln

transcript GCU ACG CGC CAG
RNA editing
RN
Mature RNA GCU AUG UGC UAG

Ala Met Cys STOP
b 0 Chara (stonewort) 0
GREEN ALGAE
0 Chaetosphaeridium 0 C to U
U to C
ext. Haplomitrium ext.
LIVERWORTS
0 Marchantia 0
ext. Takakia ext.

MOSSES
1 Physcomitrella 11
433 509 Anthoceros HORNWORTS ext.
ext. Isoetes (quillwort) 1,560 222

LYCOPODS
104 Selaginella 2,139
35 315 Adiantum FERNS ext.
35 Oryza 481
43 Nicotiana SEED PLANTS 536
41 Arabidopsis 430
1,000 500 0 0 500 1,000 1,500 2,000 2,500

Chloroplast editing sites Mitochondrial editing sites
Figure 1
Plant organellar RNA editing alters nucleotide identities in almost all land plants. (a) The C-to-U alteration can change amino acid
codons and introduce translational start and stop codons. This results in different amino acids being incorporated into the mature RNA
than were predicted from the genomic DNA. Plants shown in the photographs are from left to right: the liverwort Marchantia
polymorpha, a representative fern, and two angiosperms (owering plants). (b) In all land plant lineages, RNA editing changes C
nucleotide identities to U in mitochondria and plastids. In green algae, no editing has been reported to date. In the branch of the
liverworts that contains the species Marchantia polymorpha, editing has been lost secondarily. Numbers of editing sites are given for
species in which the full complement has been analyzed. In some species, extensive editing has been reported, although the full extent
still needs to be determined.
3 -untranslated sequences (6, 12, 24, 49). In ri- organelles, RNA editing is most prevalent in
bosomal RNAs, editing appears to be absent the coding regions of mRNAs. The amino acids
or very infrequent. The reason for this sup- specied by the codons generated by editing in
pression of editing can only be speculated; it the mRNA are generally better conserved in
may be connected to a rapid compartmental- evolution than the amino acids encoded by the
ization of the rRNAs by protein coverage. In genomic DNA (27). This observation suggests
introns, editing seems to be required in some in- that RNA editing in plants restores codons al-
stances for efcient splicing. In tRNAs, editing tered by mutation to (again) encode the amino
events can be required for processing of pre- acids that are optimal or even required for func-
cursor RNA molecules (6). However, in both tion of the respective protein. RNA editing can
www.annualreviews.org RNA Editing in Plants 337

then be considered to act as an indirect repair ing the inference that different trans-factors are
mechanism that corrects DNA mutations on involved at different editing events. Indeed, sev-
the RNA level. eral site-specic trans-factors have been identi-
PPR proteins:
pentatricopeptide ed in recent years that conrm that the unique
repeat proteins RNA sequence motifs upstream of editing sites
THE RNA: CIS ELEMENTS are individually recognized by specic proteins
The nucleotide to be edited must be recognized encoded in the nuclear genome.
and targeted within the multitude of C nu-
cleotides in the population of RNA molecules.
In recent years, in vivo [trans-plastidic (911, THE PROTEINS:
47)], in vitro (55, 84, 85), and in organello (7, 19, TRANS-FACTORS
36) investigations have identied the crucial cis
Pentatricopeptide Repeat Proteins
elements in the polynucleotide RNA chain for
a number of editing sites. There is no common

Are the Specificity Factors
denominator distinguishing a C to be edited The rst such trans-factor was identied in

from an unedited C, implying that editing sites 2005 for an RNA-editing event in plastids by
are addressed individually through a unique se- tracing a rather unspecic mutant phenotype
quence pattern. In all instances, stretches of 20 to the nuclear gene responsible (41). The phys-
to 25 nucleotides in the RNA mostly upstream iological defect identied as a disturbed func-
(5 ) of the editing site provide a specic se- tion of the plastid NADH dehydrogenase is
quence context that is recognized by the editing caused by a single RNA-editing defect in the
activity (9, 15, 85). RNA for a specic subunit of this protein
When mutations of these sequence regions complex. The affected editing event creates an
from several editing sites were tested in in vitro AUG translational start from the genomic ACG
and in organello assays, the crucial nucleotides codon. Consequently, without this editing
were found to reside in a window between 5 event, the NADH dehydrogenase subunit pro-
and 15 nucleotides upstream of the edited C (9, tein is not synthesized and the complex cannot
15, 19, 36, 55, 84, 85). The gap to the edited C be functionally assembled in the mutant of the
suggests that the site-specic trans-factors do RNA-editing specicity factor.
not actually discriminate the nucleotides adja- Analysis of other mutants incapacitated in
cent to the edited nucleotide. Mechanistically, various plastid functions led to further similar
either the site-specic factors stretch across this proteins, all of them uniquely addressing one
gap or one or more other proteins are recruited or a very few editing sites in plastid mRNAs
for the deamination reaction. Such spatial con- (29, 44, 57, 59). The rst factor for editing
straints may also be responsible in selecting the events in mitochondrial mRNAs was identied
nucleotide identity just upstream of the edited by genomic mapping of ecotype-specic editing
C. At this 1 position, G and A nucleotides are variants and tracing these to the altered genes
highly underrepresented and can be found only (93). More recently, a direct screening approach
at a very few editing sites (22). has been developed to identify specic RNA-
In some instances, nucleotide identities far- editing aberrations in a randomly mutated plant
ther from this central motif appear to inuence population and to trace the respective mutation
attachment of the respective specicity factors to an individual plant and therein to the gene
(85). Nucleotides more than 30 moieties up- affected (28, 75, 77, 86, 87, 93).
stream from the edited C or closer to this posi- The nuclear-encoded factors required for
tion and even downstream in the mRNA inu- editing of one to as many as eight to ten sites in
ence RNA editing in vitro. These very variable mitochondria and plastids belong to the family
parameters suggest that individual recognition of the pentatricopeptide repeat (PPR) proteins.
patterns are used at each site, further support- This protein family is specically amplied in
338 Takenaka et al.

plants, whereas the nuclear genomes of fungi, an E domain. These approximately 200 pro-
protists, and animals code for only few members teins are not enough to individually specify the
of this class of proteins (2, 38, 46, 57, 58, 60, 69, 450500 editing sites in mitochondria and plas-
E (extension)
71). Almost all of the PPR proteins are targeted tids. Indeed, many of these proteins are found domain: the extension
to mitochondria or plastids (the two organelles to target several sites. Although several of the domain evolved from
with genomes), where they are involved in var- assigned RNA-editing PPR proteins appear to an ancient PPR
ious RNA-processing steps, including intron address individual sites, some are required for element; only found in
RNA-editing PPR
splicing, endonucleolytic processing, RNA sta- as many as six or even eight editing events. Sur-
proteins
bility, and access to translation. prisingly, the common targets of a given PPR
DYW domain:
The RNA-editing factors in plants belong protein sometimes show very little sequence
another extension
to an approximately 200-member-strong sub- similarity in their cis elements upstream of the beyond the E domain
group of the PPR proteins, which is character- edited nucleotides, suggesting that different nu- with signature amino
ized by a mixture of 35-mer amino acid repeats cleotide combinations may confer recognition acids of cytidine
(P) and PPR repeats that are slightly longer (L), and binding of the same PPR protein (79). deaminases and
containing the three

with as many as 37 amino acids, or shorter (S), In some instances, such exible connections
highly conserved
with 31 to 34 amino acids (46, 69, 71). At their between the PPR proteins and the RNA se- amino acids D
C termini, following the last PPR motif, these quence lead to overlapping specicities, result- (aspartic acid),
RNA-editing proteins are extended by an E (ex- ing in two PPR proteins able to target the same Y (tyrosine), and
tension) domain. The E region displays some editing site. Evidence for such redundancies is W (tryptophan) at the
C terminus
features of PPR elements, suggesting that such mostly indirect from those cases in which a
an element was part of the E-domain ances- complete knockout of one PPR protein only re- PLS repeats: PPR
repeats that consist of
tor and that some properties may have been re- duces editing at a given site but does not lead to a
P (normal PPR), L
tained (Figure 2). complete loss of the nucleotide conversion (93). (longer PPR), and S
About half of the E-type PPR proteins At these sites, another PPR protein presumably (shorter PPR) motifs.
are further extended by an approximately must be able to provide the residual activity, al- This pattern is
100-amino-acid-long DYW region. This ele- beit less efciently. Direct evidence has so far generally present in
PPR-type
ment is named after the three highly conserved been reported for the two rather similar PPR
RNA-editing factors in
C-terminal amino acids: aspartic acid (D), tyro- proteins MEF8 and MEF8S (87). The acronym plant organelles
sine (Y), and tryptophan (W) (Figure 2). The MEF designates the PPR proteins identied as
DYW region is essential in some of the DYW mitochondrial RNA-editing factors. The target
PPR proteins but is not required for functional sites of MEF8 and MEF8S seem to be identi-
activity in others, at least in complementation cal, and the editing levels at the sites are di-
assays of mutants (17, 57). One protein in Ara- rectly correlated with the expression pattern of
bidopsis, DYW1, consists of a well-conserved the resident intact PPR protein in a knockout
DYW domain and of a region with rudimen- plant of the respective other protein.
tary similarity to a partial E domain (Figure 2) The overlapping specicities and target se-
(13). The DYW1 protein interacts in plastids quences of different RNA-editing PPR proteins
with the rst identied RNA-editing specicity have consequences for our view of the speci-
factor CRR4, which lacks a DYW region, to city of the RNA-PPR interaction. There may
edit the ACG codon to an AUG. Both proteins actually be a large number of such redundan-
are required here, suggesting that a DYW cies and hidden targets, which could imply a
domain is essential but may be provided in trans more degenerate and exible RNA-PPR code
if not present in cis on the PPR editing factor. interaction.
The nuclear genome of Arabidopsis thaliana
codes for 194 E-type PPR proteins. Six addi-
tional genes code for PPR proteins that consist The PPR Protein to RNA Code
of the PLS repeat elements that are character- RNA binding of PPR proteins has been
istic for this subgroup but do not encompass shown for several RNA-editing proteins but

Arabidopsis cp
CRR22 cp S P L S P L S P L S P L S P L2 S E DYW
CLB19 cp P L S S P L S P L2 S E
CRR4 cp L P P L S S S S S P L S P L2 S E
DYW1 cp DYW
Arabidopsis mt
MEF11 mt L S P L S P L S P L S P L2 S E DYW
MEF21 mt S P L S S P L S P L2 S E
MEF19 mt S P L S P L S P L S P L2 S E
MEF8 mt L S P L2 S E DYW
Physcomitrella mt
PpPPR_56 mt L S P L S P L S P L S P L2 S E DYW
Figure 2
Structure of pentatricopeptide repeat (PPR) proteins involved in plant organellar RNA editing. The proteins
that recognize a specic RNA sequence just upstream of an RNA-editing site belong to the superfamily of
PPR proteins. Aligned here are several representative editing factors from plastids (cp; CRR22, CLB19, and
CRR4) and mitochondria (mt; MEF11, MEF21, and MEF19). These examples display the principle of the
structure and the variations in the numbers of the three different types of repeats (S, small; P, medium sized;
L, long repeats). The RNA-editing subfamily of the PPR proteins is characterized by a modular structure
within which each of the PLS repeats presumably contacts one nucleotide. The function of the extension (E)
domain is not yet clear, and the optional C-terminal DYW domain may provide deaminase activity for the
C-to-U nucleotide conversion in the RNA. In both compartments, proteins with a DYW domain and few if
any PPR elements can be found. As examples, DYW1 in plastids and MEF8 in mitochondria are depicted.
All RNA-editing PPR proteins in the moss Physcomitrella patens contain E and DYW domains. On the left of
the respective protein structure, the N-terminal elements labeled cp or mt denote the predicted respective
target sequences. The N-terminal part of the MEF8 E domain shows relatively low similarity to other E
domains (light green).
is most intensively documented for PPR needs to be readily accessible to the ribosome
proteins involved in other RNA-processing for protein synthesis. Nevertheless, attach-
reactions (59, 69, 90). For PPR proteins ment of some PPR proteins to their specic
protecting against endo- or exonucleases, tight RNA targets has been observed in several
contact to the RNA is expected and indeed instances. The main problem encountered
found to be very sequence specic. However, with these assays is the difculty of obtaining
RNA-editing PPR proteins are expected to PPR proteins by expression of their coding
bind reversibly because the mature RNA sequences (20) in bacterial cells. In bacteria,
340 Takenaka et al.

the PPR proteins are synthesized but usually ported into both organelles (5, 81). One protein
aggregate or are sequestered into inclusion bod- contains only half of the only conserved region
ies and are not soluble. This holds true for the and may be a pseudogene. These proteins are
Multiple organellar
expression of single PPR repeats as well as for each required for numerous editing sites and RNA-editing factors
the E and DYW domains without any repeat. have been designated accordingly as multiple (MORF) proteins:
Although no direct structural data of the organellar RNA-editing factors (MORFs) (81). individual MORF
PPR proteins could be obtained, predictions Mutation of one such MORF results in loss proteins are involved
in RNA editing at
of their 3D structures generally suggest two of RNA editing at several sites and reduction of
numerous sites in
helical structures within each repeat unit (20, editing at many sites. In the plastid, mutation of owering plants
39, 53, 69, 71). Starting from the presumption either of the two MORFs targeted exclusively
Editosome: the
that each repeat attaches to one nucleotide in to this compartment affects almost all editing hypothetical protein
the RNA, amino acid coincidences with nu- sites, suggesting that both proteins are involved complex that associates
cleotide identities in the target RNA can be cal- in editing at a given site. At some sites, editing with mitochondrial or
culated. These presumptions seem to be valid, is completely lost when only one of the two fac- plastid RNA to alter a
C or U nucleotide to
given that the parameters identied through tors is absent (81). Both plastid MORF proteins
the respective other
such alignments yield reasonably accurate com- are therefore predicted to form homomers and identity
putational correlation tools, which have been heteromers, implying that they may, in some
used to correctly predict the target sites for instances, be able to provide their function in
previously unassigned RNA-editing PPR pro- editing as homomers. At other sites heteromers
teins (3, 29, 39, 53, 80). These assignments may be required, but at most of the editing
even allow the intelligent manipulation of the sites either the homomer or heteromer seems
RNA target sites to eventually generate PPR to be functional, although the heteromers ap-
proteins, which can be designed to bind to pear to be more prevalent. This inference is sug-
any given RNA sequence. This fact has been gested by the reduced editing observed at most
proven in assays of PPR proteins in which of the plastid editing sites when either of the
only the crucial nucleotide determinator amino two MORFs is missing (81).
acid identities were altered. The recoded PPR The actual function of the MORF proteins
proteins bind specically to the correspond- in the hypothetical editosome in plastids and
ingly altered RNA sequence (3). Such designed mitochondria is as yet unknown. Because they
RNA-binding proteins complement the DNA- show no similarity to known functional pro-
binding TAL proteins, which likewise use a tein domains (specically, they do not carry
34-meramino acid repeat structure to dene a any cytidine deaminase signatures), they may
specic sequence pattern as a target for binding provide a function as connectors between the
in double-stranded DNA nucleotide polymers RNA-binding PPR proteins and the actual en-
(8). zymatic activity (Figure 4). This notion is sup-
ported by the observation that MORF proteins
can interact with the PPR proteins involved in
Multiple Site-Specific Proteins: RNA editing. The mitochondrial MORF pro-
Multiple Organellar RNA-Editing teins discriminate between different PPR pro-
Factors teins in yeast two-hybrid assays (81). In some
Along with the RNA sequence-specic PPR instances, the MORF protein required for edit-
proteins, another group of proteins is required ing a given site indeed interacts with the specic
for RNA editing at all sites in owering plant PPR protein, which is also essential for pro-
mitochondria as well as plastids (Figure 3). In cessing this site. The MORF proteins may be
the genome of Arabidopsis, ten members of this involved in bridging the distance of four nu-
small family of proteins are encoded; two are cleotides between the nucleotides contacted by
targeted to plastids and ve or six are targeted the PPR proteins and the actually edited C moi-
to mitochondria, with one or two possibly im- ety to guide the enzyme.

MORF6
MORF5
Arabidopsis_AT2G35240_
F2
Vit
Arabido
M
R
is_
_
OR
MO
081566
GSV
Ory
F4
IVG
psis_AT
Po
za_
0
Ar
43
pu
NE3.00
01
ab
lus
33
OS1
02
_
id
_ FG
.1.1
2G
op
33
1G3258
EN
1G1
sis
_
AT
46
Pop opulus_EUGE
01
_G Ara 1.1593
ES
_
G0 psis_
H4
00
AT
00
70
102
Pop _P 26
5G
38
ulu G. 1_ 0
0_
28
6G
44
o
0_
s_E C_
_GW
1_
SV bid
0
10
UG
78
SC
EN AF OS 200
0
E3.
016 F O L a_ 7 87
ulus
z 2
IV
y 0 _
Or IVG01 1280
P
3 00 D
MO 40 _ G S V _OS04G5
RF1 s_ yza
t is
Viti Or
Vi
LG_X45
Ar abid Pop WISE1_V1.C_
o psis ulus Populus_GENE
_AT _GW
4G 2 1.III
002 .231
0 2.1_
1G11430
MORF9 Arabidopsis_AT Popu Vitis_GSVIVG01
_XI2 _
.C_LG 47001 lu s_GW 035101001_
E _V1 1..X
ENE W IS 14 5
0_ Ara X.3771.1
lus_G 010 445 Or bid _
Popu VG yz ops
G SVI 8G0 a_
OS is_A
s_ 0 T3G
V iti OS 03 067
a_ G3
r yz 84 90
O 90 MO
Populus_
_ R F3
Ar
ab
480_
S09G33 70
Pop
_
id
01
op
46
GW1.14
30
00
ulus
sis
9G0
74
25
_A
Vitis_GSVIVG01014223001_
16
G7
_FG
T3
OS0
10
G1
T1
6.72.1_
G0
Ara
ENE
50
_A
za_
O
IV
bid
00
SV
Oryza_
sis
S H4
Ory
_G
op
op
M
tis
sis
bi d
_PG
OR
Vi
_A
A ra
F8
.C_L
T1
G5
7
G_X
RF
32
60
MO
I09
MO
RF
10
Figure 3
Multiple organellar RNA-editing factor (MORF) proteins are required for RNA editing in plastids and mitochondria of owering
plants in addition to the pentatricopeptide repeat (PPR) proteins. The small family of MORF proteins is only found in owering plants,
suggesting these are a recent addition to the RNA-editing process. In Arabidopsis thaliana, nine genes encode proteins with full-length
conserved central domains; MORF10 contains only part of this region. Two of the nine full-length genes are specic for the plastid
(MORF2 and MORF9; shaded green), MORF8 is dual targeted to both organelles, and the other MORFs are specic to mitochondria.
This unrooted tree visualizes the species-specic variation of genes for MORF proteins between the owering plants rice (Oryza),
poplar (Populus), grape (Vitis), and thale cress (Arabidopsis). This suggests that similar species-specic MORF proteins are recent
derivates and may at least partially substitute for each other. Different numbers of genes for MORF proteins are encoded in other
owering plant species. MORFs are not found in nonowering plants.
342 Takenaka et al.

MORF Cytidine
proteins deaminase?
E domain DYW domain

PPR domains
Figure 4
Model of the presently identied composition of the hypothetical editosome in owering plant organelles. A
pentatricopeptide repeat (PPR) protein binds to a specic combination of nucleotides in the RNA. One or
more multiple organellar RNA-editing factor (MORF) proteins interact with the PPR protein and attract
the enzymatic activity. This most likely deaminase activity may be a DYW domain from a respective
(second) PPR protein or an entirely different moiety. Bullets represent nucleotides in the RNA. Cartridges
in the PPR proteins denote the degenerate repeats of approximately 35 amino acids. The E and DYW
domains of the respective PPR proteins are indicated.
The only discernible feature present in all step analogous to the single nucleotide con-
nine members of the MORF family is the version in the pathway of uridine and cytidine
so-called MORF box, which is centrally located biosynthesis. Here, a classic cytidine deaminase
in most MORF proteins. The function of this enzyme is involved, of which seven are encoded
conserved MORF box domain is unknown; it in the Arabidopsis genome (18). However, none
may be a point of contact to the PPR proteins of them appears to be active in organellar
(5, 81). RNA editing. Precedence for the adaptation
of such a mononucleotide deaminase to be
able to act on polynucleotide chains is found
The Enzyme in the mammalian apolipoprotein C-to-U
The enzyme catalyzing the actual C-to-U RNA editing (54). This, as well as the classic
conversion reaction for RNA editing in plant mononucleotide-specic cytidine deaminases,
mitochondria and plastids has not yet been requires bound zinc atoms for its active center.
identied. So far, several conditions have been Zinc chelators, however, do not reduce or
characterized that are only partially compatible block the plant mitochondrial activity in
with either of the classic deamination or in vitro assays (76). Analogous assays with
transamination reactions. plastid extracts did detect an inhibition by the
Functional in vitro assays and the absence chelators, leaving a classic cytidine deaminase
of any in vivo intermediates with termini at activity as a possibility (31).
editing sites suggest that the sugar-phosphate As a plausible alternative, it has been
backbone remains intact during editing (7, 30, suggested that the PPR proteinintegral DYW
31, 76). The C nucleotide is not excised and domains (in which the crucial amino acid pat-
substituted by a U, but the C is modied in terns of classic cytidine deaminases appear to be
place in the RNA chain. This conclusion is conserved) supply the cytidine deaminase activ-
supported by in vitro assays that show that an ity (67). This very attractive hypothesis implies
-phosphate-labeled cytosine integrated in a that for editing sites recognized by E-class PPR
substrate RNA is recovered as an -labeled proteins without their own DYW domain, an
uridine (7, 63). These observations suggest that additional DYW class PPR protein or a protein
the reaction proceeds as a C-to-U deamination consisting of little more than a DYW region

is recruited. Support comes from the identi- pendently from RNA processes in distant evo-
cation that the DYW1 protein is required lutionary lineages of animals, fungi, and pro-
together with the E-class PPR protein CRR4 tozoans when the rst plants moved from the
for the editing at one plastid site, from the aquatic environment onto the land and devel-
in vivo interaction of these two proteins, and oped into the ancestors of the Lycopodiaceae
from the correct function of a chimeric fusion (21, 24, 38, 65, 73, 74, 83, 91). No editing has
protein of both entities (13). In most instances, been observed in any alga, whereas it is preva-
PPRPPR DYW protein interactions may be lent in all land plants. The only exceptions are
mediated by the MORF proteins, which may several species of the Marchantiales, which pre-
supply the linker between the two PPR-like sumably lost RNA editing secondarily (25, 26,
proteins (Figure 4). However, a C-to-U 66, 89).
deaminating activity of the DYW domains still Within the liverwort branch, several fea-
needs to be shown. tures other than the loss of editing have changed
Yet another alternative source of the en- during the evolution of the land plants. For ex-
zyme could be a modied transaminase activ- ample, the frequency of editing events per RNA
ity. Transaminases are involved in amino acid unit varies greatly between different lineages. In
biosynthesis pathways and require an acceptor owering plants, 400600 RNA-editing events
molecule for the amino group. Several accep- occur in mitochondria, and 3040 such alter-
tor molecules known from the amino acid path- ations occur in plastids (Figure 1) (51, 62). In
ways have been tested in vitro, but none were basal vascular plants, such as Isoetes engelmanii
found to inuence the reaction (76). The very or Lycopodium, 1,000 to 1,500 nucleotides are
selective in vitro assays suggest that additional altered in mitochondria (24). On the other end
as-yet-unassigned proteins may play a role in of the spectrum is the moss Physcomitrella patens,
RNA editing in plants. The positive effect of in which two RNA-editing events occur in plas-
added ATP on the in vitro assays is on accessory tids and eleven C nucleotides are changed to U
functions rather than the reaction itself (76). in mitochondria (65).
The ATP enhancement implies that a step is in- The number of the genes for RNA editing
volved that requires the energy supply. The re- type PPR proteins in a given plant species often
action step could be traced to the release of the roughly matches the number of editing sites
RNA from an attached protein, such as gluta- in the organelles. The 400500 editing sites in
mate dehydrogenase, which is abundant in mi- owering plants are served by 200 editing-type
tochondria. The protein was found to inhibit PPR proteins; in the moss Physcomitrella, the
RNA editing in vitro but is specically blocked 13 sites are recognized by 10 editing-type
from binding to the RNA by the presence of PPR proteins, and in the liverwort Marchantia,
ATP (76). Furthermore, the ATP can be largely where no editing is observed, there are no
substituted by NTP and even dNTP, suggest- genes for editing-type PPR proteins found
ing that for the RNA-editing step an RNA heli- in the genome. In Lycopodium, the number
case may be activated, which unwinds and clears of editing PPR proteins is slightly increased
the target RNAs from attached nonediting pro- compared with their number in owering
teins. All proteins involved must be identied plants, although the number of editing sites
and analyzed to understand and to eventually is two to three times larger. It is possible
rebuild the plant plastid and mitochondrial ed- that more sites are addressed by a single PPR
itosomes in vitro. protein in Lycopodium than in higher plants,
or maybe the entire editing machinery has
EVOLUTION OF RNA EDITING evolved differently. This scenario is a distinct
IN PLANTS option, considering that in Lycopodium no
The evidence gathered to date suggests that MORF proteins are encoded in the genome.
RNA editing in plant organelles evolved inde- Many E-type PPR proteins, which require a
344 Takenaka et al.

deaminase in trans and an adaptor molecule RNA. In addition, the direction of the reaction
analogous to the MORF proteins, are found in needs to be tightly controlled by accessory
the Lycopodium genome. Similarly, no genes for proteins, such as distinct types of PPR proteins.
MORF proteins are found in Physcomitrella. In
the moss and also in the protist Naegleria, this
may be correlated with the presence of only Evolution of the Pentatricopeptide
DYW-domain-containing PPR proteins, but Repeat Proteins
the functional signicance of the coincidence Similar to the U-to-C editing that arose during
will probably become apparent only after the the evolution of the vascular plants and was lost
actual contribution of the MORF proteins to in the branch that led to the owering plant
the editing machinery has been claried. species, individual RNA-editing sites seem to
appear and disappear during evolution (4, 68,
82, 92). The most striking example is the com-
Evolution of the U-to-C-Type plete loss of all editing sites in the Marchantia
RNA Editing clade of liverworts. But even between closely

Another difference between the land plant lin- related species, such as Arabidopsis and Brassica,
eages is the occurrence of the reverse RNA- differences in individual editing sites are ob-
editing reaction, which alters a U nucleotide served. For example, in the nad3 mRNA, site
to a C nucleotide. This type of editing occurs nad3-64 is edited in Arabidopsis thaliana but not
in hornworts, lycopods, and ferns but is absent in Brassica napus. This rather fast evolution of
from liverworts, mosses, and owering plants appearing and disappearing editing sites sug-
(24, 73, 91). This distribution suggests that this gests that the specicity factors of editing, the
type of editing arose after the split of the mosses PPR proteins, can mutate rapidly to alter their
and the hornworts and later was lost or greatly target restrictions.
reduced in the branch that led to the seed plants. Concomitantly with the loss of an editing
The presence of U-to-C-type RNA editing site by its conversion to a genomic T, the
requires a specic enzymatic activity. With only respective specicity conferring PPR protein is
circumstantial information about the enzyme free to mutate or even to become lost from the
involved in the C-to-U type of reaction, two nuclear genome. The remaining constraints
major scenarios are presently feasible. Either on this PPR protein depend on its requirement
two distinct enzymes perform the two opposing for editing at other target sites. These sites
reactions or one protein molecule catalyzes may be contacted through a different set of
both directions of the reaction. In the rst the repeats in this PPR protein that would
instance, the C-to-U reaction could be acceler- consequently need to be maintained. This
ated by a deaminase as discussed above and the idea may be difcult to analyze experimentally
amination of the U to a C could be performed because along with the sites for which a given
by a specic enzyme adapted, for example, PPR protein is essential, there are usually other
from the nucleotide metabolism-catabolism targets requiring this factor. As detailed above,
repertoire. The most likely precedence for these may be hidden by also being targets
the second scenario, a single enzyme for both of other PPR proteins and therefore cannot
reactions, would be a transaminase activity be recognized as such in mutants of a single
recruited from one of those involved in amino gene. For example, the PPR protein MEF10 is
acid biosynthesis/degradation pathways. As assigned to one target site in Arabidopsis, but its
outlined above, this would require an acceptor homolog in grape, which may or may not be an
molecule on which the amino group can be ortholog, is not required for this site because
deposited in the C-to-U reaction and from this nucleotide is already encoded as a T in the
where the amino group could be retrieved in grape mitochondrial genome (28). Although
the U-to-C amination of the nucleotide in the this grape PPR protein is the most similar to

MEF10 in Arabidopsis, it has accumulated so Selection and Maintenance of

many amino acid differences in evolution that RNA-Editing Sites
its actual function is likely to have shifted to a
The general if small advantage of individual
different editing site. At present, only one true
editing events also becomes apparent by the in-
pair of orthologous proteins has been identi-
ferred selection pressure on the persistence of
ed, the PPR2263 protein in maize and MEF29
these sites. Such a positive selective force can
in Arabidopsis, which are similar in sequence and
be postulated from the observation that most
structure and target the same editing sites (72).
editing events occur in coding regions and in
The above example also demonstrates the
positions where RNA editing changes codon
rule rather than the exception in editing: RNA-
identities. In addition, editing events in silent
editing sites are necessary for optimal mito-
codon positions tend to be edited in only some
chondrial and plastid (protein) function and
molecules in the steady-state organellar mRNA
survival of the plant. Generally, the amino acid
population. The partial conversion of such pre-
encoded by the edited codon is much better

sumably neutral sites suggests that these may
conserved with the respective proteins from

be side effects of PPR proteins primarily act-
other species. Furthermore, as in MEF10, if
ing at other sites. This fact and the nonrandom
an editing event is lost, usually the genomic
distribution of edited nucleotides suggest that
sequence has preempted the requirement for
a selective pressure acts on nonsilent sites to
this reaction by already encoding the T at the
maintain their editing.
respective position. This nding suggests that
Similar positive selection seems to apply to
editing is important and, with the sum of its
RNA-editing events in introns that most fre-
many sites, required for the plant. Direct ev-
quently occur in domains V and VI of the con-
idence for the requirement of editing at indi-
served group II intron structures. These are the
vidual sites is seen in mitochondria when ho-
best-conserved regions and are essential for the
mozygous knockout plants of respective PPR
splicing reaction. Their secondary and tertiary
proteins are not viable and is seen in plastids
structures can only fold properly after editing in
when such mutants can grow only on sugar-
some instances, and when inserted into yeast in-
supplementing media.
trons, only the edited intron version promotes
Although in many instances the knockout
splicing (12). In tRNAs, editing events are re-
mutation of a given PPR protein and the con-
quired for proper folding of the tRNA 3D struc-
sequential loss of this editing event have no
ture, and processing of the tRNA from its re-
detectable phenotype in the greenhouse, their
spective precursor RNA is compromised before
true positive value may only become apparent
editing has occurred at some sites. However,
in the competitive native environment. Many
RNA editing is not necessarily the rst process-
of these editing events without any overt effect
ing step. Intron splicing, mRNA end-trimming,
in the pampered conditions of the greenhouse
and RNA editing can occur in various orders;
may be crucial under certain environmental
some sites near exon borders are edited
challenges. In particular, the loss of editing re-
only after splicing of the nearby intron (6,
actions at several sites in mitochondria pro-
49).
duce pleiotropic phenotypes that are often con-
The examples of editing required for
nected to altered responses and even to survival
other processing steps prompt speculation
under various stress conditions, such as drought
about a potential regulatory function of RNA
or salt challenges (29, 44, 72, 94). Whether this
editing in controlling the available pool
is a secondary effect or whether RNA editing
of mature functional RNA molecules. In
can be regulated to adapt the physiological re-
mRNAs, this could be achieved most econom-
sponse of the plant still needs to be investigated
ically through the control of an AUG transla-
(35, 43, 50, 52).
tion initiation codon from an ACG triplet. This
346 Takenaka et al.

change is observed in a single plastid mRNA considering the establishment of RNA editing
and in a single mitochondrial mRNA. The af- only in the rst land plants and its absence in
fected plastid mRNA codes for the NdhD sub- the alga. However, the potential connection is
unit of the NADH dehydrogenase, a protein presently not discernible because the most ex-
complex that improves the efciency of photo- posed nucleotide connections of TT dimers in
synthesis but is not essential for survival of the the organellar DNA are not statistically more
plant. In mitochondria, an AUG translational highly represented in the RNA-editing target
start codon is generated in the nad1 mRNA sites than at unedited positions in the genomes.
coding for a subunit of the respiratory chain Furthermore, RNA editing is very frequent in
NADH dehydrogenase. Isoetes, but these plants have moved back to life
Editing events that create AUG codons, that underwater, where they are better protected
help to fold introns and tRNAs, and that remove from UV irradiation.
translational stops in ferns and Lycopodium may Plastids and mitochondria possibly benet
be employed in regulatory functions. At other from RNA editing, which could protect their
sites, partial or slow RNA editing may create genes and eventually their entire genomes from
protein variants for optimal functions in differ- being transferred into the nucleus. This raison
ent physiological requirements (45, 61). Con- detre could be on the level of the divergent
sidering the most likely evolutionary order of genetic code being used, for example, in mam-
events, these regulatory effects are likely to have malian mitochondria. Any direct translocation
been secondarily recruited. of a gene encoded in the mitochondrial genome
into the nuclear genome could not be function-
ally translated. The different nuclear decoding
ORIGIN OF EDITING: system in mammalia and the absence of RNA
SPECULATIONS editing in plants will result in different, less well
The potential sense of RNA editing in terms of adapted proteins.
a payoff for the plant has been debated without
a clear outcome. Any such interpretation and
justication requires the framework of the The Cost of RNA Editing
origin of this editing process and the questions Energetically, RNA editing seems a waste of
of why it was started and how it was initially resources and is outrageously expensive. Also,
established. Most likely, this process started the sheer number of nuclear genes being de-
by mutation of an enzyme able to perform the voted to this process in plastids and mitochon-
deamination or transamination reaction (34, dria are extremely costly in terms of genomic
48). With this ability established, thymidine space. Furthermore, considerable energy must
nucleotides in the genome could be substituted be spent on rst synthesizing and incorporating
by cytidines with the information content being C ribonucleotides and then converting these to
corrected in the RNA. The number of editing U ribonucleotides in the RNA. RNA editing
sites increased up to the present-day numbers is certainly not essential for land plants, as the
with the amplication of the site-specic PPR loss of editing in Marchantia proves. So why is
proteins. This amplication is possibly limited RNA editing still rampant in plants, and why is
by the burden of eventually carrying an excess it maintained in spite of being so expensive? Is
of genes for the PPR, the MORF, and other RNA editing in plant organelles used for reg-
RNA-editing proteins. ulation of organellar processes? Even if such
One selective factor for RNA editing might a use was secondarily acquired, the control of
have been protection against the increased ex- the two energy generating organelles by the nu-
posure to UV light when plants moved from cleus may justify the expenses. Answers to these
water to land. This connection is attractive questions still require an evolutionary rationale.

CONCLUSION ated through, for example, a regulatory func-

Recent progress, mostly via genetic studies, tion of organellar genes, needs to be clari-
revealed two types of key players in RNA ed. At present, there is little evidence to sup-
editing in plant organelles: PPR proteins and port such a function. The modular nature of
MORF proteins. However, how these proteins sequence-specic RNA binding by the PPR
cooperate is still unclear. Identication of the proteins opens a new eld of RNA biotechnol-
deaminase enzyme activity remains one of the ogy in which proteins analogous to the TALEN
main open questions in RNA editing in plants. DNA-binding technology are built. The PPR
The biological signicance of RNA editing proteins identied in RNA editing in plant or-
in plant organelles, beyond just being toler- ganelles open applications up to interference
with RNA virus infections.
SUMMARY POINTS
1. Individual RNA-editing sites are recognized by specic PPR proteins.

2. In owering plants, approximately 200 of the 400 PPR proteins are involved in RNA
editing, and the rest promote various other RNA-processing steps.
3. PPR proteins consist of approximately 35-mer amino acidrepeat units, each of which
can contact a nucleotide in the RNA.
4. The PPR proteinRNA code has been solved to rely on two combinatorial amino acids.
5. In owering plants, another group of proteins, the MORFs, are essential components of
the RNA editosome and interact with PPR proteins.
FUTURE ISSUES
1. The actual editing enzyme needs to be identied.
2. The functions of the MORF proteins need to be investigated.
3. The connection between PPR specicity factors and MORF proteins should be analyzed.
DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We thank Dagmar Pruchner, Bianca Wolf, and Angelika Muller for excellent experimental
help. This work was supported by grants from the Deutsche Forschungsgemeinschaft to Mizuki
Takenaka and Axel Brennicke. Mizuki Takenaka is a Heisenberg Fellow.
LITERATURE CITED
1. Aphasizhev R, Aphasizheva I. 2011. Uridine insertion/deletion editing in trypanosomes: a playground for
RNA-guided information transfer. Wiley Interdiscip. Rev. RNA 2:66985
348 Takenaka et al.

2. Aubourg S, Boudet N, Kreis M, Lecharny A. 2000. In Arabidopsis thaliana, 1% of the genome codes for a
novel protein family unique to plants. Plant Mol. Biol. 42:60313
3. Barkan A, Rojas M, Fujii S, Yap A, Chong YS, et al. 2012. A combinatorial amino acid code for RNA
recognition by pentatricopeptide repeat proteins. PLoS Genet. 8:e1002910
4. Bentolila S, Elliott LE, Hanson MR. 2008. Genetic architecture of mitochondrial editing in Arabidopsis
thaliana. Genetics 178:1693708
5. Bentolila S, Heller WP, Sun T, Babina AM, Friso G, et al. 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:E145361
6. Binder S, Marchfelder A, Brennicke A. 1994. RNA editing of tRNA(Phe) and tRNA(Cys) in mitochondria
of Oenothera berteriana is initiated in precursor molecules. Mol. Gen. Genet. 244:6774
7. Blanc V, Litvak S, Araya A. 1995. RNA editing in wheat mitochondria proceeds by a deamination mech-
anism. FEBS Lett. 373:5660
8. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, et al. 2009. Breaking the code of DNA-binding
specicity of TAL-type III effectors. Science 326:150912

9. Bock R, Hermann M, Kossel H. 1996. In vivo dissection of cis-acting determinants for plastid RNA editing.
EMBO J. 15:505259
10. Bock R, Kossel
H, Maliga P. 1994. Introduction of a heterologous editing site into the tobacco plastid
genome: the lack of RNA editing leads to a mutant phenotype. EMBO J. 13:462328
11. Bock R, Koop HU. 1997. Extraplastidic site-specic factors mediate RNA editing in chloroplasts. EMBO
J. 16:328288
12. Borner
GV, Morl M, Wissinger B, Brennicke A, Schmelzer C. 1995. RNA editing of a group II intron in
Oenothera as a prerequisite for splicing. Mol. Gen. Genet. 246:73944
13. Boussardon C, Salone V, Avon A, Berthome R, Hammani K, et al. 2012. Two interacting proteins are
necessary for the editing of the NdhD-1 site in Arabidopsis plastids. Plant Cell 24:368494
14. Chateigner-Boutin AL, Small I. 2010. Plant RNA editing. RNA Biol. 7:21319
15. 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. 15:595864
16. Covello PS, Gray MW. 1989. RNA editing in plant mitochondria. Nature 341:66266
17. de Longevialle AF, Meyer EH, Andres C, Taylor NL, Lurin C, et al. 2007. The pentatricopeptide repeat
gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant
Cell 19:325665
18. Faivre-Nitschke SE, Grienenberger JM, Gualberto JM. 1999. A prokaryotic-type cytidine deaminase from
Arabidopsis thaliana gene expression and functional characterization. Eur. J. Biochem. 263:896903
19. Farre JC, Leon G, Jordana X, Araya A. 2001. Cis recognition elements in plant mitochondrion RNA
editing. Mol. Cell. Biol. 21:673137
20. Fujii S, Bond CS, Small I. 2010. Selection patterns on restorer-like genes reveal a conict between nuclear
and mitochondrial genomes throughout angiosperm evolution. Proc. Natl. Acad. Sci. USA 108:172328
21. Fujii S, Small I. 2011. The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol.
191:3747
22. Giege P, Brennicke A. 1999. RNA editing in Arabidopsis mitochondria effects 441 C to U changes in
ORFs. Proc. Natl. Acad. Sci. USA 96:1532429
23. Goringer
HU, Katari VS, Bohm C. 2011. The structural landscape of native editosomes in African
trypanosomes. Wiley Interdiscip. Rev. RNA 2:395407
24. 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
104
25. Groth-Malonek M, Pruchner D, Grewe F, Knoop V. 2005. Ancestors of trans-splicing mitochondrial
introns support serial sister group relationships of hornworts and mosses with vascular plants. Mol. Biol.
Evol. 22:11725
26. 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. 24:106874

27. Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM. 1989. RNA editing in wheat
mitochondria results in the conservation of protein sequences. Nature 341:66062
28. Hartel B, Zehrmann A, Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M. 2013. MEF10 is
required for RNA editing at nad2-842 in mitochondria of Arabidopsis thaliana and interacts with MORF8.
Plant Mol. Biol. 81:33746
29. Hammani K, Okuda K, Tanz SK, Chateigner-Boutin AL, Shikanai T, Small I. 2009. General features
of chloroplast RNA editing factors and their target sites gained from a study of new Arabidopsis editing
mutants. Plant Cell 21:368689
30. Hayes ML, Hanson MR. 2007. Assay of editing of exogenous RNAs in chloroplast extracts of Arabidopsis,
maize, pea and tobacco. Methods Enzymol. 424:45982
31. Hegeman CE, Hayes ML, Hanson MR. 2005. Substrate and cofactor requirements for RNA editing of
chloroplast transcripts in Arabidopsis in vitro. Plant J. 42:12432
32. Hiesel R, Wissinger B, Schuster W, Brennicke A. 1989. RNA editing in plant mitochondria. Science
246:163234
33. Hoch B, Maier RM, Appel K, Igloi GL, Kossel H. 1991. Editing of a chloroplast mRNA by creation of
an initiation codon. Nature 353:17880

34. Jobson RW, Qiu YL. 2008. Did RNA editing in plant organellar genomes originate under natural selection
or through genetic drift? Biol. Direct 3:43
35. Karcher D, Bock R. 1998. Site-selective inhibition of plastid RNA editing by heat shock and antibiotics:
a role for plastid translation in RNA editing. Nucleic Acids Res. 26:118590
36. Kempken F, Bolle N, Bruhs A. 2009. Higher plant in organello systems as a model for RNA editing.
Endocytobiosis Cell Res. 19:110
37. Knoop V. 2011. When you cant trust the DNA: RNA editing changes transcript sequences. Cell. Mol.
Life Sci. 68:56786
38. Knoop V, Rudinger
M. 2010. DYW-type PPR proteins in a heterolobosean protist: plant RNA editing
factors involved in an ancient horizontal gene transfer? FEBS Lett. 584:428791
39. Kobayashi K, Kawabata M, Hisano K, Kazama T, Matsuoka K, et al. 2012. Identication and characteri-
zation of the RNA binding surface of the pentatricopeptide repeat protein. Nucleic Acids Res. 40:271223
40. Koito A, Ikeda T. 2012. Apolipoprotein B mRNA: editing, catalytic polypeptide cytidine deaminases and
retroviral restriction. Wiley Interdiscip. Rev. RNA 3:52941
41. Kotera E, Tasaka M, Shikanai T. 2005. A pentatricopeptide repeat protein is essential for RNA editing
in chloroplasts. Nature 433:32630
42. Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K. 2003. RNA editing in hornwort
chloroplasts makes more than half the genes functional. Nucleic Acids Res. 31:241723
43. Kurihara-Yonemoto S, Handa H. 2001. Low temperature affects the processing pattern and RNA editing
status of the mitochondrial cox2 transcripts in wheat. Curr. Genet. 40:2038
44. Liu Y, He J, Chen Z, Ren X, Hong X, Gong Z. 2010. ABA overly sensitive 5 (ABO5), encoding a pen-
tatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the
abscisic acid response in Arabidopsis. Plant J. 63:74965
45. Lu B, Wilson RK, Phreaner CG, Mulligan RM, Hanson MR. 1996. Protein polymorphism generated by
differential RNA editing of a plant mitochondrial rps12 gene. Mol. Cell. Biol. 16:154349
46. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, et al. 2004. Genome-wide analysis of Arabidopsis
pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089
103
47. Lutz KA, Maliga P. 2007. Transformation of the plastid genome to study RNA editing. Methods Enzymol.
424:50118
48. Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, et al. 2008. Complex chloroplast RNA
metabolism: just debugging the genetic programme? BMC Biol. 6:36
49. Marechal-Drouard L, Ramamonjisoa D, Cosset A, Weil JH, Dietrich A. 1993. Editing corrects mispairing
in the acceptor stem of bean and potato mitochondrial phenylalanine transfer RNAs. Nucleic Acids Res.
21:490914
50. Miyata Y, Sugita M. 2004. Tissue- and stage-specic RNA editing of rps 14 transcripts in moss
(Physcomitrella patens) chloroplasts. J. Plant Physiol. 161:11315
350 Takenaka et al.

51. Mower JP. 2009. The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast
genes and user-dened alignments. Nucleic Acids Res. 37:25359
52. Nakajima Y, Mulligan RM. 2001. Heat stress results in incomplete C-to-U editing of maize chloroplast
mRNAs and correlates with changes in chloroplast transcription rate. Curr. Genet. 40:20913
53. Nakamura T, Yagi Y, Kobayashi K. 2012. Mechanistic insight into pentatricopeptide repeat proteins as
sequence-specic RNA-binding proteins for organellar RNAs in plants. Plant Cell Physiol. 53:117179
54. Navaratnam N, Fujino T, Bayliss J, Jarmuz A, How A, et al. 1998. Escherichia coli cytidine deaminase
provides a molecular model for ApoB RNA editing and a mechanism for RNA substrate recognition.
J. Mol. Biol. 275:695714
55. Neuwirt J, Takenaka M, van der Merwe JA, Brennicke A. 2005. An in vitro RNA editing system from
cauliower mitochondria: Editing site recognition parameters can vary in different plant species. RNA
11:156370
56. Nishikura K. 2010. Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem.
79:32149
57. Okuda K, Chateigner-Boutin A-L, Nakamura T, Delannoy E, Sugita M. 2009. Pentatricopeptide repeat
proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in
Arabidopsis chloroplasts. Plant Cell 21:14656
58. Okuda K, Myouga R, Motohashi K, Shinozaki K, Shikanai T. 2007. Conserved domain structure of penta-
tricopeptide repeat proteins involved in chloroplast RNA editing. Proc. Natl. Acad. Sci. USA 104:817883
59. Okuda K, Nakamura T, Sugita M, Shimizu T, Shikanai T. 2006. A pentatricopeptide repeat protein is a
site recognition factor in chloroplast RNA editing. J. Biol. Chem. 281:3766167
60. OToole N, Hattori M, Andres C, Iida K, Lurin C, et al. 2008. On the expansion of the pentatricopeptide
repeat gene family in plants. Mol. Biol. Evol. 25:112028
61. Phreaner CG, Williams MA, Mulligan RM. 1996. Incomplete editing of rps12 transcripts results in the
synthesis of polymorphic polypeptides in plant mitochondria. Plant Cell 8:10717
62. Picardi E, Regina T, Verbitskiy D, Brennicke A, Quagliariello C. 2011. REDIdb: an upgraded bioinfor-
matics resource for organellar RNA editing sites. Mitochondrion 11:36065
63. Rajasekhar VK, Mulligan RM. 1993. RNA editing in plant mitochondria: -phosphate is retained during
C-to-U conversion in mRNAs. Plant Cell 5:184352
64. Rhee AC, Somerlot BH, Parimi N, Gott JM. 2009. Distinct roles for sequences upstream of and down-
stream from Physarum editing sites. RNA 15:175365
65. Rudinger
M, Funk HT, Rensing SA, Maier UG, Knoop V. 2009. RNA editing: only eleven sites are
present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal.
Mol. Genet. Genomics 281:47381
66. Rudinger
M, Polsakiewicz M, Knoop V. 2008. Organellar RNA editing and plant-specic extensions of
pentatricopeptide repeat proteins in jungermanniid but not in marchantiid liverworts. Mol. Biol. Evol.
25:140514
67. Salone V, Rudinger
M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, et al. 2007. A hypothesis on
the identication of the editing enzyme in plant organelles. FEBS Lett. 581:413238
68. Schmitz-Linneweber C, Kushnir S, Babiychuk E, Poltnigg P, Herrmann RG, Maier RM. 2005. Pigment
deciency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase -subunit
mRNA. Plant Cell 17:181528
69. Schmitz-Linneweber C, Small I. 2008. Pentatricopeptide repeat proteins: a socket set for organelle gene
expression. Trends Plant Sci. 13:66370
70. Shikanai T. 2006. RNA editing in plant organelles: machinery, physiological function and evolution. Cell.
Mol. Life Sci. 63:689708
71. Small ID, Peeters N. 2000. The PPR motif: a TPR-related motif prevalent in plant organellar proteins.
Trends Biochem. Sci. 25:4647
72. Sosso S, Mbelo S, Vernoud V, Gendrot G, Dedieu A, et al. 2012. PPR2263, a DYW-subgroup penta-
tricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion
biogenesis and maize growth. Plant Cell 24:67691
73. Steinhauser S, Beckert S, Capesius I, Malek O, Knoop V. 1999. Plant mitochondrial RNA editing. J. Mol.
Evol. 48:30312

74. Sugita M, Miyata Y, Maruyama K, Sugiura C, Arikawa T, Higuchi M. 2006. Extensive RNA editing in
transcripts from the PsbB operon and RpoA gene of plastids from the enigmatic moss Takakia lepidozioides.
Biosci. Biotechnol. Biochem. 70:226874
75. Takenaka M. 2009. MEF9, an E-subclass pentatricopeptide repeat protein, is required for an RNA editing
event in the nad7 transcript in mitochondria of Arabidopsis. Plant Physiol. 152:93947
76. Takenaka M, Brennicke A. 2003. In vitro RNA editing in pea mitochondria requires NTP or dNTP,
suggesting involvement of an RNA helicase. J. Biol. Chem. 278:4752633
77. Takenaka M, Brennicke A. 2012. Using multiplex single base extension typing to screen for mutants
defective in RNA editing. Nat. Protoc. 7:193145
78. Takenaka M, Verbitskiy D, van der Merwe JA, Zehrmann A, Brennicke A. 2008. The process of RNA
editing in plant mitochondria. Mitochondrion 8:3546
79. Takenaka M, Verbitskiy D, Zehrmann A, Brennicke A. 2010. Reverse genetic screening identies ve
E-class PPR proteins involved in RNA editing in mitochondria of Arabidopsis thaliana. J. Biol. Chem.
285:2712229
80. Takenaka M, Zehrmann A, Brennicke A, Graichen K. 2013. Improved computational target site prediction
for pentatricopeptide repeat RNA editing factors. PLoS ONE 8(6):e65343

81. Takenaka M, Zehrmann A, Hartel B, Kugelmann M, Verbitskiy D, Brennicke A. 2012. MORF family
proteins are required for RNA editing in mitochondria and plastids of plants. Proc. Natl. Acad. Sci. USA
109:51049
82. Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, et al. 2005. Editing of plastid RNA
in Arabidopsis thaliana ecotypes. Plant J. 43:70815
83. Tillich M, Lehwark P, Morton BR, Maier UG. 2006. The evolution of chloroplast RNA editing. Mol.
Biol. Evol. 23:191221
84. Verbitskiy D, Takenaka M, Neuwirt J, van der Merwe JA, Brennicke A. 2006. Partially edited RNAs are
intermediates of RNA editing in plant mitochondria. Plant J. 47:40816
85. Verbitskiy D, van der Merwe JA, Zehrmann A, Brennicke A, Takenaka M. 2008. Multiple specicity
recognition motifs enhance plant mitochondrial RNA editing in vitro. J. Biol. Chem. 283:2437481
86. Verbitskiy D, Zehrmann A, Hartel B, Brennicke A, Takenaka M. 2011. The DYW-E-PPR protein MEF14
is required for RNA editing at site matR-1895 in mitochondria of Arabidopsis thaliana. FEBS Lett. 585:700
4
87. Verbitskiy D, Zehrmann A, Hartel B, Brennicke A, Takenaka M. 2012. Two related RNA editing proteins
target the same sites in mitochondria of Arabidopsis thaliana. J. Biol. Chem. 287:3806472

88. Wahlstedt H, Ohman M. 2011. Site-selective versus promiscuous A-to-I editing. Wiley Interdiscip. Rev.
RNA 2:76171
89. Wahrmund U, Quandt D, Knoop V. 2010. The phylogeny of mosses: addressing open issues with a new
mitochondrial locus: group I intron cobi420. Mol. Phylogenet. Evol. 54:41726
90. Williams-Carrier R, Kroeger T, Barkan A. 2008. Sequence-specic binding of a chloroplast pentatri-
copeptide repeat protein to its native group II intron ligand. RNA 14:193041
91. 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 339:8997
92. Zehrmann A, van der Merwe JA, Verbitskiy D, Brennicke A, Takenaka M. 2008. Seven large varia-
tions in the extent of RNA editing in plant mitochondria between three ecotypes of Arabidopsis thaliana.
Mitochondrion 8:31927
93. Zehrmann A, van der Merwe JA, Verbitskiy D, Brennicke A, Takenaka M. 2009. A DYW domain con-
taining pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of
Arabidopsis thaliana. Plant Cell 21:55867
94. Zhu Q, Dugardeyn J, Zhang C, Takenaka M, Kuhn K, et al. 2012. SLO2, a mitochondrial PPR protein
affecting several RNA editing sites, is required for energy metabolism. Plant J. 71:83649
352 Takenaka et al.

GE47-FrontMatter ARI 2 November 2013 9:9
Contents Annual Review of

Genetics
Volume 47, 2013

Causes of Genome Instability
Andres Aguilera and Tatiana Garca-Muse p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Radiation Effects on Human Heredity
Nori Nakamura, Akihiko Suyama, Asao Noda, and Yoshiaki Kodama p p p p p p p p p p p p p p p p p p p33
Dissecting Social Cell Biology and Tumors Using Drosophila Genetics

Jose Carlos Pastor-Pareja and Tian Xu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p51

Estimation and Partition of Heritability in Human Populations Using
Whole-Genome Analysis Methods
Anna A.E. Vinkhuyzen, Naomi R. Wray, Jian Yang, Michael E. Goddard,
and Peter M. Visscher p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
Detecting Natural Selection in Genomic Data
Joseph J. Vitti, Sharon R. Grossman, and Pardis C. Sabeti p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p97
Adaptive Translation as a Mechanism of Stress Response
and Adaptation
Tao Pan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 121
Organizing Principles of Mammalian Nonsense-Mediated
mRNA Decay
Maximilian Wei-Lin Popp and Lynne E. Maquat p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 139
Control of Nuclear Activities by Substrate-Selective
and Protein-Group SUMOylation
Stefan Jentsch and Ivan Psakhye p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 167
Genomic Imprinting: Insights From Plants
Mary Gehring p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 187
Regulation of Bacterial Metabolism by Small RNAs
Using Diverse Mechanisms
Maksym Bobrovskyy and Carin K. Vanderpool p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Bacteria and the Aging and Longevity of Caenorhabditis elegans
Dennis H. Kim p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 233
The Genotypic View of Social Interactions in Microbial Communities
Sara Mitri and Kevin Richard Foster p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 247
SIR Proteins and the Assembly of Silent Chromatin in Budding Yeast
Stephanie Kueng, Mariano Oppikofer, and Susan M. Gasser p p p p p p p p p p p p p p p p p p p p p p p p p p p p 275
v
GE47-FrontMatter ARI 2 November 2013 9:9
New Gene Evolution: Little Did We Know

Manyuan Long, Nicholas W. VanKuren, Sidi Chen, Maria D. Vibranovski p p p p p p p p p p p 307
RNA Editing in Plants and Its Evolution
Mizuki Takenaka, Anja Zehrmann, Daniil Verbitskiy, Barbara Hartel,
and Axel Brennicke p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 335
Expanding Horizons: Ciliary Proteins Reach Beyond Cilia
Shiaulou Yuan and Zhaoxia Sun p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 353
The Digestive Tract of Drosophila melanogaster
Bruno Lemaitre and Irene Miguel-Aliaga p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 377
RNase III: Genetics and Function; Structure and Mechanism
Donald L. Court, Jianhua Gan, Yu-He Liang, Gary X. Shaw, Joseph E. Tropea,
Nina Costantino, David S. Waugh, and Xinhua Ji p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 405

Modernizing the Nonhomologous End-Joining Repertoire:
Alternative and Classical NHEJ Share the Stage
Ludovic Deriano and David B. Roth p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 433
Enterococcal Sex Pheromones: Signaling, Social Behavior,
and Evolution
Gary M. Dunny p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 457
Control of Transcriptional Elongation
Hojoong Kwak and John T. Lis p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 483
The Genomic and Cellular Foundations of Animal Origins
Daniel J. Richter and Nicole King p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 509
Genetic Techniques for the Archaea
Joel A. Farkas, Jonathan W. Picking, and Thomas J. Santangelo p p p p p p p p p p p p p p p p p p p p p p p 539
Initation of Meiotic Recombination: How and Where? Conservation
and Specicities Among Eukaryotes
Bernard de Massy p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 563
Biology and Genetics of Prions Causing Neurodegeneration
Stanley B. Prusiner p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 601
Bacterial Mg2+ Homeostasis, Transport, and Virulence
Eduardo A. Groisman, Kerry Hollands, Michelle A. Kriner, Eun-Jin Lee,
Sun-Yang Park, and Mauricio H. Pontes p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 625
Errata
An online log of corrections to Annual Review of Genetics articles may be found at
http://genet.annualreviews.org/errata.shtml
vi Contents
Annual Reviews
Its about time. Your time. Its time well spent.
New From Annual Reviews:

Annual Review of Statistics and Its Application
Volume 1 Online January 2014 http://statistics.annualreviews.org
Editor: Stephen E. Fienberg, Carnegie Mellon University

Associate Editors: Nancy Reid, University of Toronto
Stephen M. Stigler, University of Chicago
The Annual Review of Statistics and Its Application aims to inform statisticians and quantitative methodologists, as
well as all scientists and users of statistics about major methodological advances and the computational tools that
allow for their implementation. It will include developments in the field of statistics, including theoretical statistical
underpinnings of new methodology, as well as developments in specific application domains such as biostatistics
and bioinformatics, economics, machine learning, psychology, sociology, and aspects of the physical sciences.
Complimentary online access to the first volume will be available until January 2015.
table of contents:
What Is Statistics? Stephen E. Fienberg High-Dimensional Statistics with a View Toward Applications
A Systematic Statistical Approach to Evaluating Evidence in Biology, Peter Bhlmann, Markus Kalisch, Lukas Meier
from Observational Studies, David Madigan, Paul E. Stang, Next-Generation Statistical Genetics: Modeling, Penalization,
Jesse A. Berlin, Martijn Schuemie, J. Marc Overhage, and Optimization in High-Dimensional Data, Kenneth Lange,
Marc A. Suchard, Bill Dumouchel, Abraham G. Hartzema, Jeanette C. Papp, Janet S. Sinsheimer, Eric M. Sobel
Patrick B. Ryan Breaking Bad: Two Decades of Life-Course Data Analysis
The Role of Statistics in the Discovery of a Higgs Boson, in Criminology, Developmental Psychology, and Beyond,
David A. van Dyk Elena A. Erosheva, Ross L. Matsueda, Donatello Telesca
Brain Imaging Analysis, F. DuBois Bowman Event History Analysis, Niels Keiding
Statistics and Climate, Peter Guttorp Statistical Evaluation of Forensic DNA Profile Evidence,
Climate Simulators and Climate Projections, Christopher D. Steele, David J. Balding
Jonathan Rougier, Michael Goldstein Using League Table Rankings in Public Policy Formation:
Probabilistic Forecasting, Tilmann Gneiting, Statistical Issues, Harvey Goldstein
Matthias Katzfuss Statistical Ecology, Ruth King
Bayesian Computational Tools, Christian P. Robert Estimating the Number of Species in Microbial Diversity
Bayesian Computation Via Markov Chain Monte Carlo, Studies, John Bunge, Amy Willis, Fiona Walsh
Radu V. Craiu, Jeffrey S. Rosenthal Dynamic Treatment Regimes, Bibhas Chakraborty,
Build, Compute, Critique, Repeat: Data Analysis with Latent Susan A. Murphy
Variable Models, David M. Blei Statistics and Related Topics in Single-Molecule Biophysics,
Structured Regularizers for High-Dimensional Problems: Hong Qian, S.C. Kou
Statistical and Computational Issues, Martin J. Wainwright Statistics and Quantitative Risk Management for Banking
and Insurance, Paul Embrechts, Marius Hofert
Access this and all other Annual Reviews journals via your institution at www.annualreviews.org.
Annual Reviews | Connect With Our Experts

Tel: 800.523.8635 (us/can) | Tel: 650.493.4400 | Fax: 650.424.0910 | Email: service@annualreviews.org

RNA Editing in Plants and Its Evolution

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

RNA Editing in Plants and Its Evolution

Uploaded by

Copyright:

Available Formats

GE47CH15-Takenaka ARI 29 October 2013 14:23

Top downloaded articles

Molekulare Botanik, Universitat Ulm, 89069 Ulm, Germany;

Annu. Rev. Genet. 2013. 47:33552 Keywords

INTRODUCTION Another species-specic feature is the dis-

ture RNA species a different amino acid than

that encoded by the genomic DNA. To pre-

336 Takenaka et al.

a Primary Ala Thr Arg Gln

Mature RNA GCU AUG UGC UAG

ext. Takakia ext.

433 509 Anthoceros HORNWORTS ext.

ext. Isoetes (quillwort) 1,560 222

35 315 Adiantum FERNS ext.

43 Nicotiana SEED PLANTS 536

1,000 500 0 0 500 1,000 1,500 2,000 2,500

www.annualreviews.org RNA Editing in Plants 337

a number of editing sites. There is no common

denominator distinguishing a C to be edited The rst such trans-factor was identied in

338 Takenaka et al.

containing the three

www.annualreviews.org RNA Editing in Plants 339

340 Takenaka et al.

www.annualreviews.org RNA Editing in Plants 341

342 Takenaka et al.

E domain DYW domain

www.annualreviews.org RNA Editing in Plants 343

344 Takenaka et al.

RNA Editing clade of liverworts. But even between closely

www.annualreviews.org RNA Editing in Plants 345

MEF10 in Arabidopsis, it has accumulated so Selection and Maintenance of

encoded by the edited codon is much better

conserved with the respective proteins from

346 Takenaka et al.

www.annualreviews.org RNA Editing in Plants 347

CONCLUSION ated through, for example, a regulatory func-

1. Individual RNA-editing sites are recognized by specic PPR proteins.

348 Takenaka et al.

specicity of TAL-type III effectors. Science 326:150912

www.annualreviews.org RNA Editing in Plants 349

an initiation codon. Nature 353:17880

350 Takenaka et al.

www.annualreviews.org RNA Editing in Plants 351

for pentatricopeptide repeat RNA editing factors. PLoS ONE 8(6):e65343

352 Takenaka et al.

Contents Annual Review of

Volume 47, 2013

Dissecting Social Cell Biology and Tumors Using Drosophila Genetics

Jose Carlos Pastor-Pareja and Tian Xu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p51

New Gene Evolution: Little Did We Know

Nina Costantino, David S. Waugh, and Xinhua Ji p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 405

New From Annual Reviews:

Editor: Stephen E. Fienberg, Carnegie Mellon University

Annual Reviews | Connect With Our Experts

You might also like

Editor: Stephen E. Fienberg, Carnegie Mellon University