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First published online July 24, 2003; 10.1104/pp.103.021485 Plant Physiology 132:2152-2165 (2003) © 2003 American Society of Plant Biologists Systematic Trans-Genomic Comparison of Protein Kinases between Arabidopsis and Saccharomyces cerevisiae1San Diego Supercomputer Center and Department of Biology, University of California, San Diego, 9500 Gilman Drive, La Jolla, California 92093–0537 (D.W., M.G.); and Department of Cell Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037 (J.F.H.)
The genome of the budding yeast (Saccharomyces cerevisiae) provides an important paradigm for transgenomic comparisons with other eukaryotic species. Here, we report a systematic comparison of the protein kinases of yeast (119 kinases) and a reference plant Arabidopsis (1,019 kinases). Using a whole-protein-based, hierarchical clustering approach, the complete set of protein kinases from both species were clustered. We validated our clustering by three observations: (a) clustering pattern of functional orthologs proven in genetic complementation experiments, (b) consistency with reported classifications of yeast kinases, and (c) consistency with the biochemical properties of those Arabidopsis kinases already experimentally characterized. The clustering pattern identified no overlap between yeast kinases and the receptor-like kinases (RLKs) of Arabidopsis. Ten more kinase families were found to be specific for one of the two species. Among them, the calcium-dependent protein kinase and phosphoenolpyruvate carboxylase kinase families are specific for plants, whereas the Ca2+/calmodulin-dependent protein kinase and provirus insertion in mouse-like kinase families were found only in yeast and animals. Three yeast kinase families, nitrogen permease reactivator/halotolerance-5), polyamine transport kinase, and negative regulator of sexual conjugation and meiosis, are absent in both plants and animals. The majority of yeast kinase families (21 of 26) display Arabidopsis counterparts, and all are mapped into Arabidopsis families of intracellular kinases that are not related to RLKs. Representatives from 11 of the common families (54 kinases from Arabidopsis and 17 from yeast) share an extremely high degree of similarity (blast E value < 10-80), suggesting the likelihood of orthologous functions. Selective expansion of yeast kinase families was observed in Arabidopsis. This is most evident for yeast genes CBK1, HRR25, and SNF1 and the kinase family S6K. Reduction of kinase families was also observed, as in the case of the NEK-like family. The distinguishing features between the two sets of kinases are the selective expansion of yeast families and the generation of a limited number of new kinase families for new functionality in Arabidopsis, most notably, the Arabidopsis RLKs that constitute important components of plant intercellular communication apparatus.
Comparative genomics allow one to make functional projections from well-studied model organisms to species about which we know much less at the molecular and cellular level. At the same time, these studies can identify groups of genes that are unique to a species. Protein kinases are good targets for such study because they constitute a well-conserved group of proteins. Protein kinases are important components of cellular regulatory systems. They are organized into signaling cascades, which form the backbone of the signaling network. Specific signals are restricted to specific pathways by the substrate specificity of the involved kinases. Systematic comparison of protein kinases between species can shed light on how the signaling network has been conserved and has differentiated during evolution. In this case, a comparison of yeast (Saccharomyces cerevisiae) and Arabidopsis allows us to identify groups of protein kinases that have been specifically elaborated in plants and, in some cases, to infer probable function of Arabidopsis protein kinases.
The budding yeast and Arabidopsis provide ideal candidate species for
systematic trans-genomic study. Such a study requires a comprehensive list of
protein kinases for each species being studied. The completeness and accuracy
of the sequence information directly determines the likelihood of success of
such integrative approaches. The budding yeast has long been a prototype for
eukaryotic biological research. It is a much simpler system than Arabidopsis
but shares cellular architecture and regulatory mechanisms with higher
eukaryotic organisms. Sequencing of its genome was completed in 1996
(Goffeau et al., 1996
Analysis of the relationships between lineages of proteins is commonly done
using programs such as ClustalW (Thompson
et al., 1994
Clustering of families of diverse multifunctional proteins such as protein
kinases suffers from a second technical problem, transitivity. Commonly used
methods such as unweighted pair-group method using arithmetic average
(Sokal and Michener, 1958
Protein kinases of S. cerevisiae (119) and protein kinases of Arabidopsis (1,019) were clustered based on their amino acid sequences. Determination of inter-protein distances expressed as BLAST E values, selection of clustering thresholds, and the clustering procedure were performed as described in "Materials and Methods." It is important to note that this clustering is based on comparison of the entire sequence. BLAST detects all conserved regions shared by two sequences (Altschul et al., 1997  ) so that
domains outside the kinase catalytic region critically affect the result.
Because the non-catalytic domains are key indicators of function, this is an
important positive feature of this approach. Because the terms family, group,
and class have often been used to identify various sets of kinases, throughout
this manuscript, we use the neutral term "cluster" to refer to
groups of kinases operationally defined by specific distance thresholds
expressed as BLAST E values.
The degree to which functional inferences can be made depends on the
evolutionary distance separating the sequences. In maximum linkage clustering,
the members of a cluster are all guaranteed to be within a certain threshold
distance of each other, that is, they constitute a clique. Our experience in
this project, and in the clustering of a set of plant protein kinases that
includes all Arabidopsis kinases and 117 kinases from other plant species
(Gribskov, 2002
Table I shows a synopsis of
the 15 clusters produced at the threshold E value of 1. The 12 clusters of
conventional protein kinases (not His kinase like and not PI kinase like, see
"Materials and Methods") are, at a threshold E value of 11.0,
merged into one tree (Fig. 1).
Each cluster was examined to investigate the distribution of yeast and
Arabidopsis kinases at the family and subfamily level
(Table I). Two types of
clusters of conventional protein kinases were observed. One type of cluster
(clusters 1–4) contains all of the RLKs and related cytoplasmic kinases.
The other type of cluster (clusters 5–12) corresponds to intracellular
protein kinases. For these families, we also list the corresponding PlantsP
classification number (Table
I), which is a number assigned to each protein kinase family based
on a complete classification of plant protein kinases
(Gribskov, 2002
Six clusters (clusters 1–6) comprise only Arabidopsis protein kinases. No overlap was observed between yeast protein kinases and Arabidopsis RLK and related protein kinases (clusters 1–4). Clusters 5 and 6 also comprise only Arabidopsis kinases. These include putative Raf-related mitogen-activated protein kinase kinase kinases (MAP3Ks) such as AtCTR1, a component of the ethylene response pathway (Kieber et al., 1993 ). Also
included is a subcluster containing protein kinases ATN1
(Tregear et al., 1996), AtMRK1
(Ichimura et al., 1997), and
the Arabidopsis homolog of soybean (Glycine max) GmPK6
(Feng et al., 1993). These
kinases share similarities with the catalytic domains of both Raf-like and
mammalian mixed-lineage kinase (MLK) MAP3K families
(Ichimura et al., 1997;
Jouannic et al., 1999). S.
cerevisiae lacks both raf-like and MLK MAP3K
(Hunter and Plowman,
1997).
Other clusters comprise both Arabidopsis and yeast protein kinases. The
trees for these clusters are shown in Figures
2 to
6. Each of Figures
7 to
11 shows the tree of a
subcluster (or a kinase family) compressed in
Figure 2. Within each tree, a
branch representing a yeast kinase is denoted by a diamond followed by the
kinase's standard name and systematic name defined in the SGD database
(Weng et al., 2003
Within cluster 7 (Fig. 2),
which contains 78 (of 119) yeast protein kinases, we identified five
yeast-specific families (PIM like, CaMK, NPR/HAL5, PTK, and RAN) and two
Arabidopsis-specific families (CPK and PPCK). Other families, such as CDK and
components of the MAP kinase cascades, are common to both species. This
cluster contains four yeast kinase groups, CaMK, CMGC, STE11/STE20, and
STE7/MEK (Hunter and Plowman,
1997
Cluster 8 (Fig. 3)
corresponds closely to the AGC kinase group, which includes the PKA (cAMP
dependent), PKC (DAB activated, PL dependent), AGC, S6K (ribosomal protein S6
kinase), and DBF2 kinase families in yeast
(Hunter and Plowman, 1997
Clusters 9 and 10 are merged into one tree in Figure 4. They comprise the CK1 (casein kinase I) and the CDK-like kinase (CLK) family, respectively. Within the CK1 family, we observed the expansion of a single yeast gene, HRR25, into a subfamily of 13 closely related Arabidopsis homologs. This was the greatest gene expansion observed in our analysis.
Clusters 11 and 12 comprise only five and one Arabidopsis kinases, respectively. Cluster 11 (Fig. 5A) includes the yeast NEK-like kinase family, which has three yeast members but just one Arabidopsis kinase. The yeast IRE1 kinase and three Arabidopsis homologs are also included in this cluster (Fig. 5A). Cluster 12 comprises only three genes, the yeast-specific kinase ISR1, the yeast kinase VPS15, and its Arabidopsis homolog At4g29380 (E = 2 x 10-97; Fig. 5B).
Finally, due to a lack of homology with conventional protein kinases, His kinases (clusters 13 and 14) and phosphatidylinositol kinase-like protein kinases (cluster 15) form distinct clusters (Table I). The tree for cluster 13 is shown in Figure 6. A number of protein kinase families correspond to subclusters of cluster 7 (Table I) and are compressed in the tree shown in Figure 2. These include kinases of the MAP kinase signaling cascade, the plant CPKs, the SnRKs, the CDKs, etc. To display a map of potential cross-species orthologs, the trees for the kinases of the MAP signaling cascade (Figs. 7 and 8), the SnRKs (Fig. 9), the CDKs (Fig. 10), the shaggy/GSK-3-like kinases, and casein kinase II (CK2) kinases (Fig. 11) are shown.
The experimentally generated knowledge in biological literature represents
the best possible reference for evaluating a computational analysis.
Fortunately, a substantial amount of knowledge is available in this case
because yeast is an alternative genetic host for experimental studies of plant
protein kinases, and the set of protein kinases of this organism is one of the
best studied. We used three criteria to assess the performance of our
clustering procedure. First, a search of PubMed found 11 Arabidopsis kinases,
which rescued genetic deletion phenotype of the corresponding yeast kinase. In
this work, seven of the 11 kinase pairs were coclustered. The other four pairs
were put in close neighborhood (Table
II). This is expected because some kinases will first merge with
their paralogs rather than orthologs. The genetic complementation assay
selects ortholog(s) only for the deleted gene. It is not informative regarding
whether the selected Arabidopsis gene(s) would also complement the yeast
gene's paralog(s). Further, if based on cDNA expression library screening,
this assay can only select those candidates that are abundant in the cDNA
expression library. However, not all isoforms of a kinase family will be
abundant in a particular cDNA library if they display complementary tissue
distribution patterns. For example, AtMEKK1 was selected to complement the
STE11 deletion (Covic and Lew,
1996
Table III lists yeast kinases for which potential Arabidopsis orthologs were identified by this hierarchical clustering approach. Overall, plant counterparts were identified for 21 of 26 yeast protein kinase families. Within these families, potential orthologs were identified and highlighted in the corresponding trees. In summary, 54 Arabidopsis protein kinases were identified as orthologous to 17 yeast protein kinases.
Plants are relatively less studied than other model organisms. As a consequence, the set of Arabidopsis protein kinases is not well studied at the molecular and cellular level yet. This makes it important to perform systematic comparative genomic comparison with well-studied eukaryotic species. The budding yeast is the best studied eukaryotic model organism and serves as an important paradigm for transgenomic comparisons with other eukaryotic species (Chervitz et al., 1998 ; Rubin et al.,
2000). This is the first systematic comparative genomic study of
the protein kinases of yeast and a plant multicellular species to identify the
genes specifically elaborated in multicellular plant species and to provide a
basis for functional inference. The budding yeast has been used as an
alternative genetic host for experimental characterization of Arabidopsis
kinases. The protein kinase set of this model species has been classified
previously into biochemically proven families. This makes it possible to
validate our results. We believe our results will be helpful for the current
endeavor to learn more about these kinases and to better understand the
signaling network of Arabidopsis. Our study further validates yeast as a good
model system for the study of the plant intracellular kinase network. The
distinguishing features of the two kinase sets are not the number of core
kinase families. Instead, they are selective expansion of some families and
the generation of a limited number of new kinase families in Arabidopsis, most
notably the Arabidopsis RLK family. This study uses a hybrid maximum linkage/average linkage clustering of full-length protein sequences. The use of stringent thresholds in initial steps, combined with the maximum linkage methodology, ensures that the clustering procedure discriminates between two unrelated multidomain proteins when each of them shares a domain with a third multidomain protein. Proteins that are closely related in yeast and Arabidopsis will share extensive sequence similarity both within and outside the kinase catalytic domain. Therefore, we expect that molecules whose function is truly conserved will be merged in the maximum linkage clustering procedure because the initial proliferation of the protein kinase family preceded the divergence of the plant and fungal lineages. This is supported by the clustering patterns of Arabidopsis and yeast proteins in reported cases, where the Arabidopsis protein can complement the corresponding yeast mutant and, thus, is a functional homolog (Table II). In this work, additional potential Arabidopsis orthologs were identified. They might have been missed by the genetic complementation assays due to their low abundance in the screened cDNA libraries or due to the assay's tendency to favor constitutive (or more active) isoforms. Our result is further validated by its consistency with the biochemical activities of a number of Arabidopsis kinases and its consistency with reported systematic classification of yeast kinases, most of which have been experimentally proven. This clustering effort identifies potential orthologs whose biochemical function can be directly tested in future genetic complementation assays.
This is the first conclusive observation, to our knowledge, that yeast lacks homologs to plant RLK (Fig. 1). In animals, there are numerous receptor Tyr kinases and relatively few receptor Ser/Thr kinases. Multicellular species, such as Arabidopsis, require elaborate intercellular signaling mechanism to regulate growth, development, and response to the environment. Transmembrane receptor protein kinases play key roles in making the proximal response to intercellular signals. The absence of transmembrane receptor-like protein kinases in yeast reflects a reduced need to respond to extracellular signals due to unicellular habit.
The MAP Kinase Cascade
Nevertheless, there are Arabidopsis MAP3Ks that have no yeast counterpart.
Arabidopsis MAP3Ks can be divided into three subfamilies, namely the Raf like,
the STE11/MEKK like, and the CDC15-like MAP3K. The Arabidopsis-specific
Raf-related family (Table II)
includes AtMAP3K
In addition, Arabidopsis possesses two clusters of short MAP3K-related
proteins, with the sizes of most of them ranging from 300 to 450 amino acid
residues. These putative kinases seem to display a plant-specific feature in
that they contain MAP3K-like catalytic domains but lack the usually long
stretch of regulatory domains flanking the catalytic region. The first
cluster, the GmPK6/AtMRK1/ATN-1 like, shares similarity with both Raf-like
MAP3K and mammalian MLK in the catalytic domain but lacks obvious regulatory
domains, except that a subset of them contains ankyrin repeats in the
N-terminal one-half (Table II,
cluster 5). For example, the Arabidopsis homolog of GmPK6 shares 39% identity
(56% positive) with the catalytic region of human MLK-2 but lacks the Leu
zipper and the large C-terminal domains typical of MLKs
(Dorow et al., 1995
The SNF1-Like Kinase (SnRK) Family
The CDK Family
This signaling machinery is utilized by prokaryotic species to sense and
respond to environmental stimuli
(Schaller, 2000
Due to a lack of homology with conventional protein kinases, these kinases
form their own cluster (Fig.
6). The five Arabidopsis phytochromes are also included in this
cluster due to their possession of a His kinase-like domain. However,
phytochrome His kinase domains are very divergent from those of prokaryotes,
and, in the case of PhyA, have been shown to exhibit Ser/Thr as opposed to His
kinase activity (Fankhauser,
2001
Besides the Arabidopsis RLK, five species-specific protein kinase families
were found for each species. The Arabidopsis-specific families include CPK,
PPCK, Raf-like kinase, and the two clusters of short MAP3K-like kinases
discussed earlier. Further, the CPK and PPCK kinase families are not found in
animals either. The plant CPKs appear to have originated from the fusion of a
CaMK-like ancestor with its calmodulin-like regulatory subunit
(Harmon et al., 2000
The majority of yeast protein kinase families (21 of 26) exhibit obvious
counterparts and sometimes are extensively expanded in Arabidopsis. This is
most evident in cases where one yeast kinase shares high similarity with
multiple Arabidopsis kinases. Examples include the yeast kinase CBK1
(Fig. 3), HRR25
(Fig. 4), and SNF1
(Fig. 9). The two yeast CK2
isoforms, CKA1 and CKA2, coclustered with four Arabidopsis homologs at an E
value of 10-92 (Fig.
11B). The yeast GSK3/shaggy-like kinase MRK1 and RIM1, as another
example, coclustered with 10 Arabidopsis homologs at an E value of
10-92 (Fig. 11A).
Our observation is consistent with previous reports that the distinguishing
feature of the protein sets of yeast and animals is not the size of their
"core proteome" but the selective expansion of some families and
the generation of a limited number of new protein families in multicellular
organisms (Chervitz et al.,
1998 However, these observations show that gene expansion is not always evenly distributed across yeast kinases. The expansion of kinase CBK1, HRR25, and SNF1 all represent events where one member of a protein kinase family is selectively expanded. As discussed above, only two of the four yeast GSK3/shaggy-like kinases were merged with Arabidopsis homologs at an E value of 10-92. The other two, MCK1 and YOL128c, were not until an E value of 10-48 was reached (Fig. 11). The Arabidopsis SnRKs (Fig. 9) and MAPKs (Fig. 8B) coclustered with only a subset of the corresponding yeast protein kinases. The yeast NEK-like family, for example, is actually reduced in Arabidopsis (Fig. 5A). It remains to be seen whether other plant species share this selective kinase preservation and expansion pattern with Arabidopsis and whether non-plant multicellular species display complementary gene preservation and duplication patterns during evolution. Along with RLK kinases and the preservation of the His kinase signaling mechanism, these gene preservation and expansion patterns may prove to be important characteristics distinguishing the plant and animal signaling network.
Sequence Set of Protein Kinases
Yeast (Saccharomyces cerevisiae) and Arabidopsis protein kinase
sequences were retrieved from the functional genomic databases YPD
(Costanzo et al., 2001
BLAST version 2.09 (Altschul et al.,
1997
The clustering was performed in multiple steps. Each step used a
sequentially less stringent clustering threshold than the previous step. This
procedure is similar to that used by Yona et al.
(1999
The threshold E values were determined based on inspection of the
distribution of the E values in the {S} x {S} BLAST comparison. Clusters
were observed. Selected thresholds correspond to minima in this distribution.
Such thresholds have been used successfully by Rost
(2002 A maximum linkage clustering program written in C performed clustering at each step. This program, cluster.c, is available from the authors upon request. Inputs to this program are a clustering threshold and a distance matrix, initially the most stringent threshold and the distance matrix {S} x {S} mentioned above. This program loops over the following three steps: (a) sort the distances and identify the shortest one (smallest E value), (b) merge the corresponding pair of clusters/sequences, and (c) update the distances from each sequence (or previously existing cluster) to the new cluster as the maximum of the distances from it to the two clusters/sequences being merged (hence the term maximum linkage). The loop stops when the shortest distance identified in step one exceeds the threshold and results in a cluster set {C}. Distances between generated clusters are then recalculated as the geometric mean of the distances between the members of the clusters. This resulted in a new distance matrix {C} x {C}, which is used as input for the next round of maximum linkage clustering. Received February 3, 2003; returned for revision March 26, 2003; accepted May 7, 2003.
1 This work was supported by the National Science Foundation (grant no. DBI–9975808) and was assisted by the facilities of the National Biomedical Computation Resource (through grant no. P41–RR08605 from the National Institutes of Health National Center for Research Resources).  * Corresponding author; e-mail dwang{at}sdsc.edu; fax 858–822–0873.
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TOP
ABSTRACT
RESULTS
1, AtEDR1, and AtCTR1 in a single subcluster of 12
kinases. There are two additional subclusters of seven and three Raflike
kinases, respectively (data not shown). These kinases currently have not been
characterized, and functional annotation awaits genetic and/or biochemical
data. The STE11/MEKK-like family includes a number of previously described
proteins, AtANP 1 to 3; AtMAP3K-
, -
, and -
; and AtMEKK1.
The CDC15-like family contains the yeast CDC15 gene and two Arabidopsis
kinases, the AtMAP3K
1 (Jouannic et
al., 2001
