Download Characteristic Features of the Nucleotide Sequences of Yeast

DNA RESEARCH 1, 263-269 (1994)
Characteristic Features of the Nucleotide Sequences of Yeast
Mitochondrial Ribosomal Protein Genes as Analyzed by
Computer Program GeneMark
Katsumi ISONO,1'* James D. MCININCH, 2 and Mark BORODOVSKY2
Department of Biology, Faculty of Science, Kobe University, Rokkodai, Kobe 657, Japan1
and Georgia Institute of Technology, School of Biology, Atlanta, Georgia 30332, U.S.A.2
(Received 25 December 1994)
Abstract
The nucleotide sequence data for yeast mitochondrial ribosomal protein (MRP) genes were analyzed by
the computer program GeneMark which predicts the presence of likely genes in sequence data by calculating
statistical biases in the appearance of consecutive nucleotides. The program uses a set of standard sequence
data for this calculation. We used this program for the analysis of yeast nucleotide sequence data containing
MRP genes, hoping to obtain information as to whether they share features in common that are different
from other yeast genes. Sequence data sets for ordinary yeast genes and for 27 known MRP genes were
used. The MRP genes were nicely predicted as likely genes regardless of the data sets used, whereas other
yeast genes were predicted to be likely genes only when the data set for ordinary yeast genes was used. The
assembled sequence data for chromosomes II, III, VIII and XI as well as the segmented data for chromosome
V were analyzed in a similar manner. In addition to the known MRP genes, eleven ORF's were predicted
to be likely MRP genes. Thus, the method seems very powerful in analyzing genes of heterologous origins.
Key words: yeast; mitochondrial ribosomal proteins; genomic sequence data; computer prediction
1.
Introduction
The rapid accumulation of nucleotide sequence data
of various organisms has raised a challenging theme not
only to molecular biologists but also to those who are
interested in the analysis of biological information contained in such data. Various lines of experimental evidence have suggested how a gene is recognized by transcription factors, RNA polymerases, repressor molecules,
as well as co-factors associated with them. Also, how
a pre-messenger RNA is spliced, modified with capping
and poly(A)-adding enzymes, etc. has been extensively
analyzed and there are many well documented cases of
them in several organisms. Nonetheless, it is often not
so easy to predict just at which nucleotide within a sequence a gene, or a protein-coding sequence, starts. Experimentally, presence of a promoter for a given gene can
be proven by the combination of several biochemical and
molecular biological methods. However, prediction of a
promoter in a given nucleotide sequence of even such a
well studied organism as Escherichia coli by using a computer program alone is not always successful.
During the course of our systematic sequence analCommunicated by Mituru Takanami
*
To whom correspondence should be addressed. Tel. +8178-803-0553, Fax. +81-78-803-0489, E-mail: isono
scitec.kobe-u.ac.jp
ysis of the E. coli genome, we found that the computer program GeneMark developed by Borodovsky and
McIninch1 was very useful in predicting likely genes
in the nucleotide sequence data.2"4 The algorithm of
this program is based on the statistical models (nonhomogeneous Markov chain models) for the appearance
of short stretches of nucleotide that differ in proteincoding regions and non-coding regions. One of the obvious reasons for this is the presence of codons consisting
of three nucleotides and their statistically biased appearance. An additional reason is due to the specific usage of
synonymous codons depending on the nature of genes and
their products as discussed by Ikemura.5 Furthermore,
structural constraints within various regions of proteins
encoded by respective genes are also conceivable factors
affecting the statistical biases mentioned above.
Based on these considerations, we investigated whether
or not the mitochondrial ribosomal protein (MRP) genes
of the budding yeast Saccharomyces cerevisiae could be
identified as genes in which characteristic appearance of
stretches of nucleotide would be different from other yeast
genes. It has been postulated that mitochondria are descended from bacteria-like organisms that began to be
associated with eukaryotic cells as endosymbionts and
have since become specialized organella in the course of
evolution. A number of experimental data suggest that
[Vol. 1,
Prediction of Yeast Mito-Ribosomal Protein Genes
264
Table 1. Sequences used for MRP-matrix file construction*)
LOCUS name
SCMRP
SCMRP17
SCMRPL20
SCMRPL8
SCMRPL9G
SCMRPS28
YSCMRP20A
YSCMRP49A
YSCMRP4A
S77888
SC82KBXIA
SCMTRPL6
SCMRPL31
SCYMR26
SCYMR31
SCYMR44
YSCMRP1
YSCMRP13
YSCMRP2A
YSCMRP7
YSCYML33
Accesion number '
X73673
X58362
X53840
X53841
X65014
X55977
M81696
M81697
M82841
S77888
Z25464
X69480
X15099
X56106
X17540
X17552
M15160
M22109
M15161
M22116
D90217
MRP gene
MRP-L13
MRP17
MRP-L20
MRP-L8
MRP-L9
MRP-S28
MRP20
MRP49
MRP4
MRP-L27
MRP8
MRP-L6
MRP-L31
YMR26
YMR31
YMR44
MRP1
MRP13
MRP2
MRP7
MRP-L33
SCYBL038W
SCYBR122C
SCYBR146W
SCYBR251W
SCYBR268W
SCYKL170W
Z35799
Z35991
Z36015
Z36120
Z36137
Z28169
MRP-L16
MRP-L36
MRP-S9
MRP-S5
MRP-L37
MRP-L38
Length Chromosome
828 bp XI
396
588
717
810
861
791
414
XI
XI
X
VII or XV
Homologyc)
-
L17, S13
1,116
XVI
7
300
XIII
L3
S15
S2
L6
S14
L27
L30
699
591
837
924
318
414
II
II
II
II
II
XI
L16
S9
S5
L14
1,185
441
660
618
393
474
372
297
966
975
348
?
?
XI
VIII
X
XI
VIII
XI
VII or XV
VI
XIII or XVI
IV
?
Reference
8, 32
8, 17
8, 18
19
31
20
26
8, 34
10, 27
30
8, 17
10, 21
8, 19
22
23
33
24
25
35
28
29
9
9
9
9
9
8
a)
Two alternative initiation codons are assigned in YSCMRP20A for the protein coding region of MRP20, which result in
ORF's of 791 and 762 bp, respectively. The former was adopted in our calculation. Also, the intron sequence (149 bp)
included in the gene YMR44 has been omitted. The six bottom sequences were included later (see text).
b
^ Only the primary accession number of each sequence is listed.
c
' Homology to E. coli ribosomal protein genes is shown. - : No similarity was found with any known ribosomal protein genes.
many of the MRP's of S. cerevisiae are very similar to
the ribosomal proteins of E. coli. Their genes are, however, not present in the mitochondrial genome. Instead,
almost all of them reside in the nucleus, suggesting the
transfer of MRP genes from the original mitochondrial
genome to the nuclear genome during the course of evolution (for review see ref. 6). The only MRP gene that
is located in the mitochondrial genome of S. cerevisiae is
a gene termed VAR1.7 This is to indicate that the yeast
genome, and perhaps other eukaryotic genomes, are likely
to contain genes and their surrounding sequences derived
from two or more origins. Therefore, it might be that
such imported segments are different in their characteristic appearance of consecutive nucleotides from the original chromosomal nucleotide sequence. Below, we will
show that at least such is the case for the MRP genes of
yeast.
2.
Materials and Methods
The computer program GeneMark (previously, the
program was named GENMARK; see ref. 1) has been
modified, and used in a SUN SparcStation 2 with SUN
4.1 operating system, or more recently, in a SUN SparcStation 20 with Solaris 2.3 operating system. As the
standard matrix sequences for training the program, nucleotide sequence data containing 21 known MRP genes
were collected from the GenBank nucleotide sequence
database (release 85.0) as well as from the complete sequence for chromosome XI that was obtained from the
EMBL ftp site (ftp.embl-heidelberg.de). An order four
GeneMark matrix (MRP-mat.4) was constructed from a
collection of protein-coding sequences by using the program AM AT (Borodovsky and Mclninch, unpublished).
An order five matrix was also prepared using the same
data set and termed MRP-mat.5. Both matrices were
used in subsequent analysis. The GenBank LOCUS
No. 6]
K. Isono, J. D. Mclninch, and M. Borodovsky
names and accession numbers of the nucleotide sequence
data for MRP genes and the lengths of protein-coding
regions including the translational terminators that were
incorporated into these matrices are listed in Table 1.
The yeast nuclear gene matrix, sc_cul.5 prepared by
Borodovsky and Mclninch (unpublished) was used for
the prediction of other nuclear genes. Results obtained
by running GeneMark were visualized and analyzed by
the SUN Openwindow-bundled tool Page View.
Recently, the sequence data for the entire chromosome XI have become available,8 along with the assembled nucleotide sequence data for chromosome II.9 The
data were obtained from the ftp site at the Sanger Centre (ftp.sanger.ac.uk). Similarly, the assembled data for
chromosome VIII10 were obtained from the ftp site at the
Stanford University (genome-ftp.stanford.edu). The data
for chromosome III11 as well as the segmental data for
chromosome V were taken from the GenBank database.
265
statistic characteristics in these MRP genes are not very
much conflicting with each other. However, since the
five MRP genes on chromosome II were not predicted as
highly likely genes when the old matrices, MRP-mat.4
and MRP-mat.5, were used, it is likely either that the
MRP genes of yeast are not very homogeneous as far
as the statistic characteristics detected by GeneMark are
concerned, or that the number of genes whose nucleotide
sequence data were incorporated into the matrix files was
too small for statistically meaningful calculation.
We then performed similar analysis of the nucleotide
sequence data for chromosomes III, VIII, and XI that
were assembled into one contiguous sequence and became
recently available. In addition, the nucleotide sequence
data for several large segments of chromosome V were
also analyzed. For these analyses, we used the MRP- and
yeast genomic-matrices mentioned above. All genes that
had been assigned as MRP genes were nicely predicted as
highly likely genes. A typical example of the analysis is
presented in Fig. 1. In this example, a region of chromo3. Results and Discussion
some XI containing one of the MRP genes termed MRPThe gene has been assigned to ORF
3.1. Analysis with GeneMark of the nucleotide sequence 8 was analyzed.
9
It
is
preceded
by two nuclear genes, an RNA
YKL142w.
data for chromosomes II, III, V, VIII and XI
polymerase
II
PRB1
homolog
(ORF YKL144c) and the
The MRP-mat.4 (order 4) and MRP-mat.5 (order 5)
LTV1
gene
(encoding
a
low
temperature
viability promatrices were constructed as described in Materials and
tein;
ORF
YKL143w),
and
followed
by
the
SDH3 gene
Methods and used to analyze the nucleotide sequence
(encoding
a
succinate
dehydrogenase;
ORF
YKL141w)
as
data of the three yeast chromosomal sequence data that
have recently become available. In addition, the data for indicated. All four genes were predicted to be likely genes
chromosomes III and V were extracted from the Gen- when the sc_cul.5 (order 5) matrix was used (Fig. la). In
Bank database and analyzed. In the annotation lines contrast, when the MRP-matrices were used, only MRP8
to the chromosome II sequence data, five mitochondrial was nicely predicted as likely genes, but ORF's YKL144c
protein genes, MRP-S5, MRP-S9, MRP-L27, MRP-L36 and YKL141w were not predicted to be likely genes at
and MRP-L37, are assigned to ORF's, termed YBR251w, all (Fig. lb). Interestingly, the likelihood prediction usYBR146w, YBR282w, YBR122c and YBR268w, respec- ing the MRP-27 mat. 4 matrix for ORF YKL143w (the
tively. In addition, ORF YBL038w has been assigned, LTV1 gene) was quite high except for the middle portion,
though less strongly, to the gene MRP-L16. Among these although the protein encoded by this gene did not show
ORF's, however, only the one for MRP-L27was detected a significant degree of similarity to any MRP genes nor
as a highly likely MRP-gene by running program Gene- to any other mitochondrial protein genes.
Mark against the chromosome II sequence data in conIn addition to the known MRP genes, there were eleven
junction with MRP-mat.4 and MRP-mat.5. All other ORF's that were predicted as likely MRP genes by GenMRP-ORF's were detected, but much less significantly. eMark in the nucleotide sequence data for chromosomes
Since the sequence data for MRP-L21 was previously II, III, V, VIII and XI. In most cases, the likelihood probavailable under the LOCUS name of S77888 as listed ability was very high. However, none of the ORF's dein Table 1, we suspected that the number of genes and tected in this way showed a significant degree of similarhence the cumulative length of sequences we used for ity to known ribosomal protein genes of prokaryotic as
the construction of MRP-matrix files were not sufficient. well as eukaryotic origins. It is not surprising, because
Therefore, we included the data for the genes on chro- many yeast MRP genes showed no significant similarmosome II and constructed new matrices. A total of ity to any known ribosomal protein genes. Among the
27 MRP genes were thus incorporated into the new ma- mitochondrial ribosomal protein genes of S. cerevisiae,
trices as shown in Table 1. Accordingly, the new ma- there are as many as 13 out of 20 genes (65%) that do
trices were named MRP-27-mat.4 (order 4) and MRP- not posses apparent similarity to any known ribosomal
27-mat.5 (order 5). By using the two new matrices, we protein genes of other organisms.6 The ORF's that were
were able to detect all the MRP genes on chromosome predicted to be likely MRP genes by GeneMark could
II as highly likely genes. This is to indicate that the thus be additional examples of this category, although
with these data alone, it is difficult to decide whether
[Vol. 1,
Prediction of Yeast Mito-Ribosomal Protein Genes
266
VMMCKXI: CHRlW
1778*0
Wi-98
Nucleotide Position
Y«t*Ch>.XJ: MRP nun-onMr 4 uwd
VKL142W: UftPS
YKL143W: LTV)
YKL141W: SDH3
1
Si
177B40
176192
178544
Nuclootioo Position
Figure 1. GeneMark prediction of likely genes in a region of chromosome XI. A stretch of chromosome XI nucleotide sequence
data (nucleotides 176,080 through 180,304) was analyzed with GeneMark in conjunction with the nuclear matrix sc-cul.5 (a) and
MRP-27mat,4 (b). Four ORF's (YKL144c, YKL143w, YKL142w and YKL141w) were identified in this region as indicated. ORF
YKL142w (stippled) corresponds to the MRP8 gene.17 Ordinate indicates the likelihood probability and abscissa the nucleotide
positions within the assembled sequence data. 8 Horizontal bars drawn at probability value of 0.5 indicate the positions and extent
of ORF's.
No. 6]
K. Isono, J. D. Mclninch, and M. Borodovsky
267
R»fl1 -2 corrected. Order *. Window 96. SIBP 12 **
R»Ol-2 ongmat. O d « ' « Window 96 S»C '2 4
l\
99318
99«SS
100020
Nucieotide Position
M316
99*r9
100020
Nucieotide Position
Figure 2. GeneMark prediction of likely genes in a region of chromosome VIII. A stretch of chromosome VIII nucieotide sequence
data (nucleotides 98,612 through 100,724) was analyzed with GeneMark in conjunction with the MRP-27mat.4 matrix. The original
assembled sequence showed the existence of two highly likely MRP genes in this region (ORF-A and -B) that almost overlap each
other (a). The corrected sequence, however, shows only one ORF as a highly likely MRP gene (b).
they are indeed MRP genes that are not known till now.
Further analysis is needed to establish if they are indeed
unidentified MRP genes or not.
We have attempted similar analysis of the MRP genes
of other organisms. There is only one case of MRP gene
that is included in the current releases of GenBank (Release 85), EMBL (Release 40) and DDBJ (Release 19)
databases, i.e. the nucieotide sequence of an MRP gene,
termed CYT-21, of Neurospora crassa stored under the
LOCUS name of NCCYT21 (accession no. X06360). The
protein encoded by this gene shows similarity, though
not of high degree, to E. coli ribosomal protein S16.12
The gene was not detected as a likely gene by GeneMark
with MRP-27-mat.4, however. It is conceivable that the
higher G+C content of N. crassa genomic DNA (53.4%),
including the CYT-21 gene, than that of S. cerevisiae
(38.3%), might be one of the major reasons for these results. However, since no other MRP-gene sequences of
N. crassa are currently available, it is not possible to
perform further comparison at the moment.
During the course of analysis of the nucieotide sequence
data of chromosome VIII, we found that there is a region of the assembled nucieotide sequence data for this
chromosome that contained the MRP4 gene. The gene
was assigned to ORF YHL004w (nucieotide positions at
99,213 through 100,397) of the assembled sequence data.
Upon analysis of the region containing this ORF with
GeneMark and MRP-27mat.5, two likely genes (ORFA and -B) were recognized to exist in different reading
frames as likely MRP genes that almost overlap each
other as shown in Fig. 2a. No assignment was given to
the second ORF in frame 1 (ORF-B). Therefore, we examined the nucieotide sequence data for the MRP4 gene
reported by Davis et al.13 and compared it with the assembled chromosome VIII sequence data. It then became
clear that the assembled sequence data of chromosome
VIII (LOCUS SCCHRVIII; no accession number is available yet) contained an extra stretch of 40 bp at position
99,965 through 100,004 that is highly repetitive to the
stretch immediately following it. This 40 bp stretch does
not exist in the sequence data, SC82KBXIA (accession
number Z25464), reported by Davis et al.13 After eliminating this stretch from the assembled data, which resulted in the cumulative length of the assembled sequence
to be 562,598 bp instead of 562,638 bp, we found that the
GeneMark prediction pattern suggested the presence of
only one ORF as a highly likely MRP gene (Fig. 2b).
Thus, the program is proven to be powerful to find sequence errors of this category as discussed by Kasai et
al.3
268
Prediction of Yeast Mito-Ribosomal Protein Genes
In the current databases, there are four entries that
contain complete nucleotide sequences of mitochondria
from plant and fungal species. They include the data
for the mitochondrial genome of the liverwort Marcantia
polymorpha (MPOMTCG, accession no. M68929), that
is the only complete mitochondrial genome sequence of
a plant species and is the longest of all mitochondrial
genome sequences reported to date.14 The overall G+C
content of this sequence is 42.4% and is slightly higher
than that of the S. cerevisiae genome (38.3%). There
are sixteen ribosomal protein genes identified within the
sequence data based on sequence similarity to those of
the ribosomal protein genes of E. coli.15 In contrast, the
mitochondrial genomes of fungal as well as mammalian
species, including that of S. cerevisiae, contain no typical ribosomal protein gene. In fact, the mitochondrial
genomes of 5. cerevisiae and a few other fungal species
are known to contain only a single ribosomal protein
gene, termed VAR1,7 that has no known counterpart in
E. coli and other bacteria. We have performed GeneMark
analysis of the liverwort mitochondrial genome with yeast
MRP-matrices as well as with E. coli matrices. However,
none of the fifteen ribosomal protein genes described were
predicted to be likely genes. Thus, although the genes encoded in the mitochondrial genome still retain sequence
features with which their identification with those of E.
coli can be made, they do not retain sequence characteristics with which their likelihood can be predicted by GeneMark in conjunction with either E. coli- or with yeast
MRP-matrices. Further analyses are now in progress in
which stretches of the yeast MRP gene sequences that
are crucial for them to be identified as likely genes will
be investigated.
Acknowledgements: This work was supported in
part by Grant-in-aid for scientific research from the Ministry of Education Nos. 06261226 and 06558103 (to KI)
and grant GM00783 from NIH (to MB and JDM). We are
grateful to Showa-Hokokai (Osaka) and Kambara-Tosao
Fund (Kobe University) for financial support.
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