©
1996 Oxford University Press
2199-2203
Footnote
Compilation and classification of higher plant mitochondrial tRNA genes
Compilation and classification of higher plant mitochondrial tRNA genes
P.
Veronico
,
R.
Gallerani
1
and
L. R.
Ceci*
Centro di Studio sui Mitocondri e Metabolismo Energetico, Sezione di Trani, Via
Corato, 17, 70059
Trani
,
Italy
and
1
Dipartimento di Biochimica e Biologia Molecolare, Università di Bari, Via Amendola 165/A, 70126
Bari
,
Italy
Received February 27, 1996;
Revised and Accepted April 30, 1996
ABSTRACT
This compilation reports the tRNA genes detected on higher plant mitochondrial
genomes subdivided into the widely accepted categories of `genuine' and
`chloroplast-like' genes. Moreover, it includes a list of pseudo or truncated genes
divided in the same way.
INTRODUCTION
The tRNA genes present in higher plant mitochondrial genomes show the unique
feature of a double origin (
1
). Indeed some of them are located on chloroplast DNA regions inserted into the
mitochondrial genomes during their evolution. These genes, usually classified
as `chloroplast-like', still retain a high sequence similarity (95-100%) with their chloroplast analogues. They represent about one
third of all the tRNA genes identified on the higher plant mitochondrial
genomes. Interestingly, only the tRNA genes, among those present on the
imported chloroplast DNA fragments, may be actively transcribed in the
mitochondria.
The other tRNA genes detected on the higher plant mitochondrial genomes show a
sequence similarity with their chloroplast counterparts of 65-80% and are usually classified as `native' or `genuine' mitochondrial
genes (
1
).
Exhaustive analysis of the tRNA genes present on the higher plant mitochondrial
genomes has also demonstrated that these genomes do not contain a complete set
of tRNA genes (
2
-
4
). Genes for tRNA-Ala, tRNA-Arg, tRNA-Leu, tRNA-Thr, tRNA-Val have never been detected or, if present, are
not active. The import into the mitochondria of cytoplasmic tRNA molecules,
corresponding to the missing tRNA genes has been observed in several plants
(see
5
for a review and
6
).
Description of the compilation
The aim of this compilation is to update the tRNA genes identified on the higher
plant mitochondrial genomes. It contains 115 sequences, 44 more than those
present in the last compilation on tRNA genes (
7
). Complete gene sequences are reported in Table
1
.
Pseudo-genes and truncated genes, which are particularly diffuse on higher plant
mitochondrial genomes owing to the numerous rearrangements occurred in the
course of their evolution, are listed separately in Table
2
.
Sequences corresponding to the `t-elements' detected in wheat (
26
and references therein) and to the pseudo-gene found downstream of the
trn
fM in potato (
27
), which do not show any similarity with known tRNA genes or molecules, have not
been reported.
The higher plant mitochondrial tRNAs show a highly conserved canonical structure
as compared with the secondary structures of their counterparts in metazoa and
nematodes. The sequences of their genes have been divided into the classical
tRNA domains according to Sprinzl
et al.
(
7
). Nucleotides have been numbered from 0 to 76. Positions corresponding to
nucleotides which are not always present (0, 17, 17a, 20a, 20b, the nucleotides
of the extra loop, 47 and 74-76) are indicated by dashes. Nucleotides conforming to invariant and semi-invariant positions of conventional tRNAs have been underlined. The
genes are indicated by bold capital letters corresponding to the one letter
code of the charged amino acid. Anticodons have been reported in small letters.
Initials of the latin name indicate the plant species:
A.t. Arabidopsis thaliana
(thale cress),
B.v. Beta vulgaris
(sugar beet),
B.n. Brassica napus
(rapeseed),
B.o. Brassica oleracea
(cauliflower),
G.m. Glycine max
(soybean),
H.a. Helianthus annuus
(sunflower),
L.l. Lupinus luteus
(lupine),
L.e. Lycopersicon esculentum
(tomato),
O.b. Oenothera berteriana
(primrose),
P.v. Phaseolus vulgaris
(bean),
R.s. Raphanus sativus
(horseradish),
S.t. Solanum tuberosum
(potato) for the dicotyledons, and
O.s. Oryza sativa
(rice)
, T.a. Triticum aestivum
(wheat),
Z.m. Zea mays
(maize) for the monocotyledons. The reference for each sequence is reported,
when possible, as its EMBL database accession number.
Table 1
.
(a) Nucleotides 14 and 15 were reported as CC in (7).
(b) Nucleotide C
28
is edited to U in the mature tRNA (8).(c) The gene is present in double copy in the
Triticum aestivum
mitochondrial genome (9).(d) Position 20b contained an A in (7). Nucleotide 57 was reported as C in (7)
and in the original paper (11), but it is a G in the sequence submitted to the
Databases.(e) Nucleotide C
4
is edited to U in the mature tRNA (8).(f) Nucleotide C
4
is edited to U in the mature tRNA (12).(g) The gene was reported as
trn
M in the original paper (14) and in (7). However it has been shown by tRNA
sequencing that the analogous potato gene codes for a tRNA-Ile (L*AU) (L*=lysidine-like hypermodified nucleotide) (15).(h) The same gene seems to have been published twice by different
authors (16,17).(i) The gene is present in double copy in the
Helianthus annuus
mitochondrial genome (4).(j) The gene was reported as
trn
L in (7).(k) A portion of the gene corresponding to positions 52-65 is repeated 17 nt downstream of the gene.(l) Position 20a was empty and nucleotide 21 was reported as C in (7).(m) The gene is present in double copy in the
Triticum aestivum
mitochondrial genome (18).(n) Evidence for the transcription of more than a single
trn
Q gene has been reported (19).(o) A
Phaseolus vulgaris
mitochondrial
trnS
(GCT) gene was reported in the last compilation of tRNA genes (7). Our controls
failed to find the reported sequence either in the literature or in the
Databases.(p) The gene was reported as a chloroplast gene in (7) where three nucleotides
of the variable region were also omitted.(q) Position 0 was empty and nucleotide C
56
was omitted in (7).(r) Nucleotide 31 was reported as C in (7).(s) The gene was reported with a TAA anticodon in (7) due to a different
subdivision of nucleotides among the domains.(t) The gene is identical in three different
Beta
species (
B.vulgaris, B.trygina
and
B.webbiana
) (20).(u) Nucleotides 46 and 47 were inverted in (7).(v) The gene is transcribed but not processed to the correct size (21).(w) The gene is deposited in the EMBL Database with the accession number X07923,
but the sequence reported under the cited accession number actually corresponds
to the chloroplast gene (23).
Table 2
.
(a) A 49 bp intron is present after nucleotide 43.(b) Two introns of 64 and 48 bp are present after nucleotides 28 and 43,
respectively.(c) A 48 bp intron is present after nucleotide 43.(d) The sequence deposited in the Databases belongs to the male-fertile genome even if it has been recorded as belonging to male-sterile genome (24). An identical portion of the
trn
Mi gene is also present in the male-sterile genome. In the male-fertile genome this portion of the
trn
Mi gene is part of a tRNA-like element of 145 bp.(e) This
trn
Y gene derives from an original trnF gene (11). An extranucleotide (A) is
present after nucleotide 9.(f) The analogous chloroplast gene presents an intron after position 37. A 541
bp 5'-portion of this intron is present in the
Helianthus annuus
mitochondrial genome.(g) The analogous chloroplast gene presents an intron after position 37. A 134
bp 3'-portion of this intron is present in the
Helianthus annuus
mitochondrial genome.(h) A 4 bp insertion is present in the T-loop after nucleotide 60, which is not present in the analogous
chloroplast genes.(i) A 5 bp insertion is present after position 60, which is not present in the
analogous chloroplast genes.
(j) See note (z) of Table 1.
Genuine and chloroplast-like genes are listed separately.
For each gene, sequences belonging to dicotyledonous plants are reported before
those obtained from monocotyledonous plants, with the first of the monocots
indicated by an asterisk. This further subdivision derives from the observation
that the distribution of tRNA genes is not identical between monocotyledons and
dicotyledons. The
trnC
and
trnF
genes, for example, have a chloroplast origin in monocotyledons, while they are
genuine mitochondrial genes in dicotyledons (
4
,
5
). A different origin has also been observed for the
trnG
gene. A genuine
trnG
gene has been identified in several dicotyledonous mitochondrial genomes, but
it has never been reported for a monocotyledonous plant. On the contrary, it
has been shown that the mitochondria of the monocotyledonous
Triticum aestivum
are able to import a tRNA-Gly from the cytoplasm (
18
). The reason for the heterogeneous origin of tRNA genes in higher plant
mitochondrial genomes is not known, but the different distribution of the
mitochondrial tRNA genes between monocotyledonous and dicotyledonous plants
suggests that evolutionary events may have played a relevant role in this
distribution.
Transcription analysis of tRNA genes in higher plant mitochondria shows that not
all the tRNA genes are transcribed. A + or - sign in Table
1
indicates, when available, the result of this analysis.
The sequences reported in Table
1
and Table
2
have been deposited in the European Bioinformatics Institute (EBI) Data
Library. Information on how to obtain the sequences can be requested by
electronic mail at the Netserv@ebi.ac.uk address, sending the command `help
plmitRNA'. The compilation is also available via anonymous FTP from
ftp.ebi.ac.uk in the directory pub/databases/plmitRNA.
REFERENCES
1 Maréchal-Drouard,L., Weil,J.-H. and Dietrich A. (1993) Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 13-32.
2 Joyce,P.B.M., Spencer,D.F., Bonen,L. and Gray M.W. (1988) Plant Mol. Biol. 10, 251-262.
3 Sangaré,A., Weil,J.-H., Grienenberger,J.M., Fauron,C. and Lonsdale D. (1990) Mol. Gen. Genet. 223, 224-232. MEDLINE Abstract
4 Ceci,L.R., Veronico,P. and Gallerani R. (1996) DNA Sequence 6, 159-166.
5 Dietrich,A., Weil,J.-H. and Maréchal-Drouard L. (1992) Annu. Rev. Cell Biol. 8, 115-131. MEDLINE Abstract
6 Ceci,L.R., Dell'Orco,M. and Gallerani R. (1992) Plant Mol. Biol. 19, 863-866. MEDLINE Abstract
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15 Weber,F., Dietrich,A., Weil,J.-H. and Maréchal-Drouard L. (1990) Nucleic Acids Res. 18, 5027-5030. MEDLINE Abstract
16 Handa,H. and Nakajima K. (1992) Biochim. Biophys. Acta 1130, 117-119.
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22 Schuster,W. and Brennicke A. (1987) EMBO J. 6, 2857-2863.
23 Schuster,W., Grienenberger,J.-M., Weil,J.-H. and Brennicke A. (1988) Nucleic Acids Res. 16, 7737. MEDLINE Abstract
24 Singh,M. and Brown G.G. (1991) Plant Cell 3, 1349-1362. MEDLINE Abstract
25 Fejes,E., Masters,B.S., McCarty,D.M. and Hauswirth W.W. (1988) Curr. Genet. 13, 509-515. MEDLINE Abstract
26 Spencer,D.F., Schnare,M.N., Coulthart,M.B. and Gray M.W. (1992) Plant Mol. Biol. 20, 347-352. MEDLINE Abstract
27 Maréchal-Drouard,L., Khamiss,O. and Dietrich A. (1993) Plant Mol. Biol. 22, 1157-1161.
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To whom correspondence should be addressed
