Vol 13, Issue 5, 794-799, May 2003
LETTER
Parallel Evolution by Gene Duplication in the Genomes of Two Unicellular Fungi
Austin L. Hughes1,3 and
Robert Friedman2
1Department of Biological Sciences, University of South
Carolina, Columbia, South Carolina 29208, USA; 2Department of
Biology, Arizona State University, Tempe, Arizona 85287, USA
 |
ABSTRACT
|
|---|
Phylogenetic analysis of conserved gene families in fission yeast
Schizosaccharomyces pombe and brewer's yeast
Saccharomyces cerevisiae showed that gene duplications have
occurred independently in the same families in each of these two
lineages to a far greater extent than expected by chance. These species
represent distinct lineages of the phylum Ascomycota that independently
evolved a "yeast" life cycle with a unicellular thallus that
reproduces by budding, and many of the genes that have duplicated
independently in the two lineages are known to be involved in crucial
aspects of this life cycle. Parallel gene duplication thus appears to
have played a role in the independent origin of similar adaptations in
the two species. The results indicate that using phylogenetic analysis
to test for parallel gene duplication in different species may help in
identifying genes responsible for similar but independently evolved
adaptations.
By giving rise to new genes encoding proteins of
potentially novel function, gene duplication has long been thought to
play a role in the adaptation of organisms to their environment (Ohno
1970 ; Hughes 1994; Lynch and Conery 2000). However, the patterns by
which gene duplications have given rise to functionally new genes over
the course of evolution remain poorly understood (Hughes 1999; Lynch
and Conery 2000; Friedman and Hughes 2001a; Wolfe 2001; Gu et al. 2002;
McLysaght et al. 2002). It has been proposed that duplication of
different sets of genes in different lineages can promote speciation
and adaptive radiation (Lynch and Force 2000). Thus, differential gene
duplication is hypothesized to play a role in the origin of phenotypic
diversity. On the other hand, it might be hypothesized that parallel
duplication of the same set of genes can play a role in the adaptation
of distantly related species to similar ecological niches. Thus, gene
duplication may contribute to both divergent and convergent evolution
at the phenotypic level.
We examined these processes by comparing the complete sets of
protein-coding genes in two species of fungi in the phylum Ascomycota,
the fission yeast Schizosaccharomyces pombe and brewer's
yeast Saccharomyces cerevisiae. In contrast to many
Ascomycota, both of these species have a life cycle characterized by a
unicellular thallus that reproduces by budding (a "yeast" life
cycle). S. pombe and S. cerevisiae belong to distinct
classes (Archaeacomycetes and Hemiacsomycetes, respectively) that have
been separated for as long as 420 million years (Sipiczki 2000), and
the yeast life cycle is a derived character in Ascomycota that has
evolved independently in the two lineages (Berbee and Taylor 1993).
Using phylogenetic analysis, we timed gene duplications in these two
species relative to their last common ancestor to examine the extent to
which gene duplication has occurred in a parallel manner in these two
lineages that have adapted independently to a similar mode of life.
|
RESULTS
|
|---|
Phylogenetic Analyses
Assembling conserved protein families by homology search and
constructing phylogenetic trees of each family by the quartet maximum
likelihood method (Strimmer and von Haeseler 1996), we identified a
total of 645 such families in which the phylogeny supported an
orthologous relationship between a gene or genes of S. pombe
and a gene or genes of S. cerevisiae. For each gene
duplication in these families, branch order in the phylogenetic tree
was used to test the hypothesis that gene duplication occurred prior to
the last common ancestor of the two species (Fig.
1). A slightly higher proportion of
duplications in S. pombe than in S. cerevisiae were
dated prior to their last common ancestor, but the difference between
the two species was not statistically significant (Fig. 1).
In 56 families, one or more gene duplications were found to have
occurred independently in each species after their last common ancestor
(Fig. 2). On the basis of the observed
rates of gene duplication after the common ancestor in the 645 families
examined, independent gene duplication in each species was observed far
more frequently than expected by chance (Fig. 2). These 56 families
included 22 families of ribosomal proteins. To test whether the
observed pattern was specific to ribosomal proteins, we conducted the
same analysis after excluding the ribosomal proteins from the data set.
In this case also, independent gene duplications in the two species
were observed in the same families to a far greater extent than
expected by chance (Fig. 2).
Duplication Time Estimates
On the assumption of a constant rate of protein evolution
("molecular clock"), we dated 132 gene duplications occurring after
the divergence of the two species relative to the age of their common
ancestor, assumed to have occurred 420 million years ago (Sipiczki
2000). The genome of S. cerevisiae shows evidence of numerous
duplicated genomic blocks, which are possibly the result of an ancient
polyploidization event (Wolfe and Shields 1997; Seoighe and Wolfe 1999;
Friedman and Hughes 2001a). In contrast, the genome of S.
pombe shows no evidence of a duplicated structure (Wood et al.
2002). We dated gene duplications in S. cerevisiae involving
elements of putative duplicated blocks (Seoighe and Wolfe 1999)
separately from other duplications.
Elements of duplicated blocks showed a significantly lower variance in
estimated duplication times than other pairs of duplicated genes in
S. cerevisiae or S. pombe (Fig.
3). This result is consistent with the
hypothesis that many of the former genes were duplicated within a
narrow time frame as would occur in the event of polyploidization (Fig.
3). However, the range of duplication times even of genes within the
blocks was so large as to cast doubt on the hypothesis that all of them
were duplicated simultaneously. The estimated mean duplication times
for S. cerevisiae genes in duplicated blocks (197 ± 12
million years) and not in duplicated blocks (205 ± 18 million years)
were similar (Fig. 3). In contrast, estimated mean duplication time for
S. pombe genes (310 ± 17 million years) was significantly
earlier (Fig. 3).
View larger version (18K):
[in this window]
[in a new window]
|
Figure 3. Box-and-whiskers plots of estimated duplication times for gene pairs
duplicated after the last common ancestor of Schizosaccharomyces
pombe and Saccharomyces cerevisiae, grouped as follows:
(1) 48 duplications in S. cerevisiae of genes that are not
elements of duplicated genomic blocks; (2) 39 duplications in S.
cerevisiae of genes that are elements of duplicated genomic blocks;
and (3) 46 duplications in S. pombe. The hypothesis of an
equal variance in all three groups was rejected (Levene's test;
P = 0.004). However, the hypothesis of equal variance in
S. cerevisiae duplications not in blocks and S. pombe
duplications could not be rejected (Levene's test). One-way analysis
of variance showed a significant difference in mean duplication time
between the three groups (P < 0.001), and the
Kruskal-Wallis test showed a significant difference in median
duplication times among the three groups (P < 0.001). In
each plot, the box covers the range between the first
(Q1) and third (Q3) quartiles in
the data. A horizontal line indicates the median, and a dot the mean.
The vertical lines ("whiskers") cover the range from
Q1 – 1.5
(Q3–Q1) to
Q3 + 1.5
(Q3–Q1). Outliers are indicated
by asterisks.
|
|
|
DISCUSSION
|
|---|
The 56 gene families duplicated independently in S. pombe
and S. cerevisiae include several proteins involved in cell
growth and fission. In addition to ribosomal proteins (Venema and
Tollervey 1999) already mentioned, these include numerous proteins
known to be involved in bud site selection, cell wall biosynthesis, and
other key aspects of the cell cycle (Table
1). Given the high frequency of genes with
crucial cell cycle functions in the 56 independently duplicated
families, it seems likely that gene duplication in these families was
involved in adaptation of the two lineages to the unicellular yeast
life cycle. The difference in mean duplication times between the two
species indicates that adaptation to this life cycle occurred
considerably earlier in the lineage of S. pombe than in that
of S. cerevisiae. This is consistent with phylogenetic
evidence supporting early branching of S. pombe within the
Ascomycota and more recent radiation of the order Saccharomycetales
(including S. cerevisiae; Berbee and Taylor 1993).
View this table:
[in this window]
[in a new window]
|
Table 1. Gene Families Independently Duplicated in S. cerevisiae and
S. pombe Encoding Proteins With Known Roles in Processes
Important to the Cell Cycle (Excluding
Ribosomal Proteins)
|
|
The fact that many of the gene duplications in duplicated blocks of the
S. cerevisiae genome were estimated to have occurred  200
million years ago (Mya) is consistent with the occurrence of a
polyploidization event around this time, as has been proposed
previously (Friedman and Hughes 2001a). Such a polyploidization event
may have been a source of duplicate genes that this fungus was able to
use in adapting to a unicellular lifestyle. It is of interest, however,
that S. pombe has adapted to a similar lifestyle through gene
duplication without polyploidization. Furthermore, numerous gene
duplications occurred in S. cerevisiae outside of the
duplicated blocks and thus independently of the polyploidization event.
Likewise, not all of the duplications within the blocks appear to have
occurred at the same time (Fig. 3), indicating that duplication of
genomic blocks has been an ongoing feature of the evolution of S.
cerevisiae (Friedman and Hughes 2001a). Consequently, our results
indicate that, although polyploidization can provide raw material for
adaptive evolution, it is by no means essential to the origin of
multiple new genes with novel functions. Thus, a peak of gene
duplications over the course of evolutionary history need not imply a
polyploidization event, contrary to the implication of some recent
papers (e.g., Gu et al. 2002; McLysaght et al. 2002).
There is evidence that gene duplication occurs continually over the
course of genome evolution (Lynch and Conery 2000). The mechanisms
involved include "tandem" duplication of individual genes,
duplication of larger genomic segments (Samonte and Eichler 2002), and
(more rarely) whole genome duplication by polyploidization. Most
duplicate genes are eventually lost, but duplicates that become
specialized for adaptively important new functions have a much greater
chance of being retained (Hughes 1994; Lynch et al. 2001). In each of
the two yeast species, after their last common ancestor, substantial
numbers of new duplicate genes have been retained in the genome. Our
results indicate that such a peak of retained gene duplications is the
signature of adaptive evolution at the genomic level.
Furthermore, our results indicate a novel approach for identifying
genes potentially underlying phenotypic adaptations of interest. If two
distantly related organisms have evolved similar phenotypic adaptations
independently, phylogenetic analyses can be used as in the present
study to identify gene families that have duplicated independently in
the two lineages. Such gene families will, in turn, provide a set of
candidate genes for understanding the molecular basis of adaptations
shared by the two lineages.
|
METHODS
|
|---|
Sequences and Homology Searches
The set of complete protein translations (proteome) for S.
cerevisiae was obtained at
http://genome-www.stanford.edu/Saccharomyces; that for S.
pombe at http://www.sanger.ac.uk/Projects/S_pombe; that for
Arabidopsis thaliana at http://www.tigr.org; that for
Caenorhabditis elegans at http://www.sanger.ac.uk/C_elegans;
and that for Drosophila melanogaster at
ftp://ftp.ebi.ac.uk/pub/databases/edgp/sequence_sets. Proteome data
sets from 38 complete genomes of bacteria and all available sequences
from a set of other representative organisms (the slime mold
Dictyostelium discoidium, the zebrafish Danio rerio,
the pufferfish Takifugu rubripes, the frog Xenopus
laevis, the human Homo sapiens, and the mouse Mus
musculus) were obtained from the National Center for Biotechnology
Information (NCBI, http://www.ncbi.nlm.nih.gov/).
The text file of the nonredundant proteins was formatted as a database
file using the BLAST tools obtained from the National Center for
Biotechnology Information (NCBI) ftp site (ftp://ftp.ncbi.nlm.nih.gov;
Altschul et al. 1997). After the nonredundant proteome was determined
for each genome, each protein was used to search for homology among the
rest of the proteome. This "all against all" BLAST method was
performed using the blastall executable, which is packaged with the
BLAST tools. Similarly, each protein in the nonredundant human proteome
was searched against all proteins from other genomes. In searching
human proteins against the remainder of the human proteome and in
searching human proteins against nonhuman proteins, we used an expect
value of E = 10–50. A strict search criterion
identifies as homologous only proteins showing evidence of homology
throughout the length of the protein, rather than those with homology
in only one domain or a few domains (Friedman and Hughes 2001a,b). In
all cases, we used the defaults of a BLOSUM62 substitution matrix and
the SEG filter (Wootton and Federhen 1993). The resultant records were
filtered using MSPcrunch, a program to filter and convert the BLAST
output to a tabular format (Sonnhammer and Durbin 1994).
Given all pairs of homologous proteins, a "single link" method was
used to find the protein families. This step groups genes that share
homology. For example, if gene A and B are in a family, and B and C are
in another family, then A, B, and C are in a family. Furthermore, in
this example, if A and D also share homology, then A, B, C, and D are
in a family. Within families, amino acid sequences were aligned using
CLUSTAL W 1.81 (Thompson et al. 1994).
Phylogenetic Analyses
Phylogenetic trees were constructed by the quartet
maximum-likelihood (ML) method (Strimmer and van Haeseler 1996) as
implemented in TREEPUZZLE 5.0, using the JTT (Jones et al. 1992) model
of amino acid evolution and assuming that rate variation among sites
followed a gamma distribution. On the basis of tree topology, we
determined the time of each gene duplication event in S.
cerevisiae or S. pombe relative to divergence of S.
cerevisiae and S. pombe. This method of timing duplication
events does not assume a constant rate of molecular evolution
(molecular clock) and is independent of the rooting of the tree. We
considered a branch to be significantly supported if it was supported
in 95% or more of 10,000 puzzling steps; this represents a highly
conservative test for significance of an internal branch (Strimmer and
van Haeseler 1996). Strimmer and van Haeseler (1996) recommend the use
of a 70% criterion; we therefore report these results as well (Fig.
1). We concluded that a gene duplicated prior to the cladogenetic event
if the internal branch supporting that duplication was significantly
supported.
Molecular Clock Analyses
To have an estimate of the time of duplication of genes in S.
cerevisiae and S. pombe that duplicated after the last
common ancestor of the two species, we applied the linearized tree
method to these fungal sequences (Takezaki et al. 1995). The trees were
calibrated using 420 million years as the divergence time of the two
species (Sipiczki 2000). Note that the relative values of the estimated
duplication times for genes duplicated within the S. pombe and
S. cerevisiae lineages (Fig. 3) are not dependent on the
accuracy of the estimate of the age of their common ancestor.
The Poisson model of amino acid evolution was used in constructing the
linearized trees. This simple model was used because it has a lower
variance than more complex models (Nei and Kumar 2000) and because, in
these analyses involving relatively closely related sequences, it
yielded essentially identical results to more complex models (data not
shown). Ribosomal proteins were not used in the linearized tree
analyses because amino acid sequences of these proteins were identical
or nearly so within species, making a divergence time estimate
impossible. Also excluded were other families in which the amino acid
sequences within one species were identical. Furthermore, we excluded
any case in which the assumption of linearity was not met in the tree
involving sequences from S. pombe and S. cerevisiae.
In separate preliminary analyses for each of the two species, we used
t-tests to test the hypothesis of the equality of mean
divergence time in the following two groups of genes: (1) genes
duplicated in each species; (2) genes duplicated in only one of the
species. In each species, there was no significant difference between
the means for these two groups. For S. pombe, the mean
estimated divergence time for genes duplicated independently in both
species was 316 ± 18 (standard error) Mya, whereas that for genes
duplicated only in S. pombe was 300 ± 33 Mya. For S.
cerevisiae, the mean estimated divergence time for genes duplicated
independently in both species was 192 ± 18 Mya, whereas that for
genes duplicated in S. cerevisiae it was 206 ± 15 Mya.
Because there was no significant difference between these two groups in
each species, the two groups were pooled within species for subsequent
analyses.
Estimated divergence times were compared by one-way analysis of
variance among the following three groups: (1) S. pombe genes;
(2) S. cerevisiae genes that are elements of putative
duplicated blocks (as defined by Seoighe and Wolfe 1999);
and (3) S. cerevisiae genes that are not elements of putative
duplicated blocks. Levene's test of homogeneity of variance rejected
the hypothesis of homogeneity of variance between these groups;
however, the hypothesis of homogeneity of variance between groups 1 and
3 was not rejected. One-way analysis of variance was used in analyzing
the data because it is known to be resistant to lack of homogeneity of
variance (Lindman 1974).
|
WEB SITE REFERENCES
|
|---|
ftp://ftp.ebi.ac.uk/pub/databases/edgp/sequence_sets;
Drosophila melanogaster proteome.
http://www.ncbi.nlm.nih.gov/; National Center for Biotechnology
Information (NCBI).
http://genome-www.stanford.edu/Saccharomyces; Saccharomyces
cerevisiae proteome.
http://www.sanger.ac.uk/C_elegans; Caenorhabditis elegans
proteome.
http://www.sanger.ac.uk/Projects/S_pombe; Schizosaccharomyces
pombe proteome.
http://www.tigr.org; Arabidopsis thaliana proteome.
|
Acknowledgements
|
|---|
This research was supported by NIH grants R33 GM066710 and R01
GM43940 to A.L.H. We are grateful for comments by Federica Verra and
Aoife McLysaght.
The publication costs of this article were defrayed in part by payment
of page charges. This article must therefore be hereby marked
"advertisement" in accordance with 18 USC section 1734 solely to
indicate this fact.
|
Footnotes
|
|---|
3 Corresponding author. 
E-MAIL austin{at}biol.sc.edu; FAX (604) 877-6085.
Article and publication are at
http://www.genome.org/cgi/doi/10.1101/gr.714603.
|
REFERENCES
|
|---|
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.[Abstract/Free Full Text]
Baudry, K., Swain, E., Rahier, A., Germann, M., Batta, A., Rondet, S., Mandala, S., Henry, K., Tint, G.S., Edlind, T., et al. 2001. The effect of erg26-1 mutation on the regulation of lipid metabolism in Saccharomyces cerevisiae. J. Biol. Chem. 276: 12702-12711.[Abstract/Free Full Text]
Berbee, M.L. and Taylor, J.W. 1993. Dating the evolutionary radiations of true fungi. Can. J. Bot. 71: 1114-1127.
Black, M.W. and Pelham, H.R.B. 2000. A selective transport route from Golgi to late endosomes that requires the yeast GGA proteins. J. Cell Biol. 151: 587-600.[Abstract/Free Full Text]
Friedman, R. and Hughes, A.L. 2001a. Pattern and timing of gene duplication in animal genomes. Genome Res. 11: 1842-1847.[Abstract/Free Full Text]
___, 2001b. Gene duplication and the structure of eukaryotic genomes. Genome Res. 11: 373-381.[Abstract/Free Full Text]
Fyrst, H., Oskouian, B., Kuypers, F.A., and Saba, J.D. 1999. The PLB2 gene of Saccharomyces cerevisiae confers resistance to lysophosphatidylcholine and encodes a phospholipase B/lysophospholipase. Biochemistry 38: 5864-5871.[CrossRef][Medline]
Gu, X., Wang, Y., and Gu, J. 2002. Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat. Genet. 31: 205-209.[CrossRef][Medline]
Helliwell, S.B., Howald, I., Barbet, N., and Hall, M.N. 1998. TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics 148: 99-112.[Abstract/Free Full Text]
Hughes, A.L. 1994. The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B 256: 119-124.[Medline]
___,, 1999. Adaptive evolution of genes and genomes. Oxford University Press, New York, NY.
Jones, D.T., Taylor, W.R., and Thornton, J.M. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8: 275-282.[Abstract/Free Full Text]
Li, X., Rivas, M.P., Fang, M., Marchena, J., Mehrota, B., Chaudhary, A., Feng, L., Prestwich, G.D., and Bankaitis, V.A. 2002. Analysis of oxysterol binding protein homologue Kse1p function in regulation of Sec14p-dependent protein transport from the yeast Golgi complex. J. Cell Biol. 157: 63-77.[Abstract/Free Full Text]
Lindman, H.R., 1974. Analysis of variance in complex experimental designs. W.H. Freeman, San Francisco, CA.
Lussier, M., Sdicu, A.M., and Bussey, H. 1999. The KTR and MNN1 mannosyltransferase families of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1426: 323-334.[Medline]
Lynch, M. and Conery, J.S. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.[Abstract/Free Full Text]
Lynch, M. and Force, A. 2000. The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156: 590-605.[CrossRef]
Lynch, M., O'Hely, M., Walsh, B., and Force, A. 2001. The probability of preservation of a newly arisen gene duplicate. Genetics 159: 1789-1884.[Abstract/Free Full Text]
Marsolier, M.-C., Roussel, P., Leroy, C., and Mann, C. 2000. Involvement of the PP2C-like phosphatase Ptc2p in the DNA checkpoint pathways of Saccharomyces cerevisiae. Genetics 154: 1523-1532.[Abstract/Free Full Text]
McLysaght, A., Hokamp, K., and Wolfe, K.H. 2002. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31: 200-204.[CrossRef][Medline]
Mehta, K.D., Leung, D., Lefebvre, L., and Smith, M. 1990. The ANB1 locus of Saccharomyces cerevisiae encodes the protein synthesis initiation factor eIF-4D. J. Biol. Chem. 265: 8802-8807.[Abstract/Free Full Text]
Montijn, R.C., Vink, E., Müller, W.H., Verkleij, A.J., Van den Ende, H., Henrissat, B., and Klis, F.M. 1999. Localization of synthesis of  1,6-glucan in Saccharomyces cerevisiae. J. Bacteriol. 181: 7414-7420.[Abstract/Free Full Text]
Mouassite, M., Camougrand, N., Schwob, E., Demaison, G., Laclau, M., and Guérin, M. 2000. The "SUN" family: Yeast SUN4/SCW3 is involved in cell separation. Yeast 16: 905-919.[CrossRef][Medline]
Nei, M. and Kumar, S., 2000. Molecular evolution and phylogenetics. Oxford University Press, New York, NY.
Ni, L. and Snyder, M. 2001. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12: 2147-2170.[Abstract/Free Full Text]
Niederberger, C., Gräub, R., Schweingruber, A.-M., Fankhauser, H., Rusu, M., Poitelea, M., Edenharter, L., and Schweingruber, M.E. 1998. Exogenous inositol and genes responsible for inositol transport are required for mating and sporulation in Schizosaccharomyces pombe. Curr. Genet. 33: 255-261.[CrossRef][Medline]
Ohno, S., 1970. Evolution by gene duplication. Springer Verlag, New York, NY.
Ozaki, K., Tanaka, K., Imamura, H., Hhara, T., Kameyama, T., Nonaka, H., Hirano, H., Matsuura, Y., and Takai, Y. 1996. Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15: 2196-2207.[Medline]
Powers, T. and Walter, P. 1999. Regulation of ribosome biogenesis by the Rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 10: 987-1000.[Abstract/Free Full Text]
Ramne, A., Bilsland-Marchesan, E., Erickson, S., and Sunnerhagen, P. 2000. The protein kinases Rck1 and Rck2 inhibit meiosis in budding yeast. Mol. Gen. Genet. 263: 253-261.[CrossRef][Medline]
Samonte, R.V. and Eichler, E.E. 2002. Segmental duplications and the evolution of the primate genome. Nat. Rev. Genet. 3: 65-72.[Medline]
Schmelze, T., Helliwell, S.B., and Hall, M.N. 2002. Yeast protein kinases and the RHO1 exchange factor TUS1 are novel components of the cell integrity pathway in yeast. Mol. Cell. Biol. 22: 1329-1339.[Abstract/Free Full Text]
Schorling, S., Vallée, B., Barz, W.P., Riezman, H., and Oesterhelt, D. 2001. Lag1p and Lac1p are essential for the acyl-coA-dependent ceramide synthase reaction in Saccharomyces cerevisiae. Mol. Biol. Cell 12: 3417-3427.[Abstract/Free Full Text]
Seoighe, C. and Wolfe, K.H. 1999. Updated map of duplicated regions in the yeast genome. Gene 238: 253-261.[CrossRef][Medline]
Sipiczki, M. 2000. Where does fission yeast sit on the tree of life? Genome Biol. 1: reviews1011.1-1011.4.[CrossRef]
Sonnhammer, E.L.L. and Durbin, R. 1994. A workbench for large scale sequence homology analysis. Comput. App. Biol. Sci. 10: 301-307.
Strimmer, K. and von Haeseler, A. 1996. Quartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13: 964-969.
Takezaki, N., Rzhetsky, A., and Nei, M. 1995. Phylogenetic test of the molecular clock and linearized tree. Mol. Biol. Evol. 12: 823-833.[Abstract]
Thompson, J.D., Higgins, D.G., and Gibson, T. 1994. CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.[Abstract/Free Full Text]
Venema, J. and Tollervey, D. 1999. Ribsome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33: 261-311.[CrossRef][Medline]
Watson, H.A., Cope, M.J.T.V., Grien, A.C., Drubin, D.G., and Wendland, B. 2001. In vivo role for actin-regulating kinases in endocytosis and yeast epsin phosphorylation. Mol. Biol. Cell 12: 3668-3679.[Abstract/Free Full Text]
Wolfe, K.H. 2001. Yesterday's polyploids and the mystery of diploidization. Nat. Rev. Genet. 2: 334-341.
Wolfe, K.H. and Shields, D.C. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713.[CrossRef][Medline]
Wood, V., Gwilliam, R., Rajandream, M.A., Lyne, M., Lyne, R., Stewart, A., Sgouros, J., Peat, N., Hayles, J., Baker, S., et al. 2002. The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880.[CrossRef][Medline]
Wootton, J.C. and Federhen, S. 1993. Statistics of local complexity in amino acid sequences and sequence databases. Comp. Chem. 17: 149-163.
Yenush, L., Mulet, J.M., Arino, J., and Serrano, R. 2002. The Ppz protein phosphatases are key regulators of K+ and pH homeostasis: Implications for salt tolerance, cell wall integrity and cell cycle progression. EMBO J. 21: 920-929.[CrossRef][Medline]
Received August 15, 2002;
accepted in revised format March 4, 2003.
13:794-799 © by 2003 Cold Spring Harbor Laboratory Press ISSN 1088-9051/03 $5.00
 CiteULike  Connotea  Del.icio.us  Digg  Reddit  Technorati What's this?
This article has been cited by other articles:
|
|
|
|
 
D. R. Scannell, A. C. Frank, G. C. Conant, K. P. Byrne, M. Woolfit, and K. H. Wolfe
Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication
PNAS,
May 15, 2007;
104(20):
8397 - 8402.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. A. Chapman, J. E. Bowers, F. A. Feltus, and A. H. Paterson
Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication
PNAS,
February 21, 2006;
103(8):
2730 - 2735.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S.-H. Shiu, M.-C. Shih, and W.-H. Li
Transcription Factor Families Have Much Higher Expansion Rates in Plants than in Animals
Plant Physiology,
September 1, 2005;
139(1):
18 - 26.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Robinson-Rechavi, B. Boussau, and V. Laudet
Phylogenetic Dating and Characterization of Gene Duplications in Vertebrates: The Cartilaginous Fish Reference
Mol. Biol. Evol.,
March 1, 2004;
21(3):
580 - 586.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
Top
ABSTRACT
RESULTS
95% of 10,000
quartet-puzzling steps. In parentheses are numbers of duplications for
which the internal branch was supported by 
2 = 117.2 and 82.3, respectively;
P < 0.00001 in both cases).