Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae

Abstract

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 Ca(2+)/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.

Figure 1.

Distribution pattern of Arabidopsis and yeast kinase reveals lack of RLK and Raf-like MAP3K in yeast. The tree displays the phylogenetic relationship between the 12 conventional protein kinase clusters shown in Table II. Each branch represents a cluster described in Table II. A branch length unit corresponds to a 10-fold difference in BLAST E value. Arabidopsis-specific clusters are denoted by a white triangle. Each branch is labeled with the cluster number followed by the number of Arabidopsis (A.t.) and yeast (S.c.) kinases in the cluster. Each non-RLK cluster is briefly annotated, and the corresponding figure number is identified when a cluster is displayed later.

Figure 2.

Arabidopsis lacks homologs for yeast provirus insertion in mouse (PIM)-like, Ca²⁺/calmodulin-dependent protein kinase (CaMK), NPR/HAL5, polyamine transport kinase (PTK), and RAN kinase families. The tree displays cluster 7 and is extensively compressed at family level due to the large number of proteins included. The black triangle branch denotes subcluster of multiple kinases. Yeast- and Arabidopsis-specific subcluster are denoted by one asterisk and two asterisks, respectively. Some of the compressed subclusters are shown later (see Figs. 7, 8, 9, 10, 11), and corresponding figure numbers are identified. A black diamond denotes branch representing a yeast kinase. Corresponding yeast kinase families and groups are labeled at the right end of the tree.

Figure 6.

Arabidopsis preserves the phospho-relay signaling mechanism. The tree of His kinases is displayed. Branch representing a yeast kinase is denoted by a black diamond and text following an Arabidopsis gene identification, when present, represents name previously assigned to the kinase. Subclusters, when corresponding to a functional group, are labeled at the right end of the tree in blue text.

Figure 7.

Trees of MAP3K (a) and STE20-like/MAP4K kinases (b). These are subclusters from the tree shown in Figure 2. Branch representing a yeast kinase is denoted by a black diamond and name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification.

Figure 11.

The trees of GSK3/Shaggy-like kinase family (a) and Casein kinase II family (b). It represents a subcluster from the tree shown in Figure 2. A black diamond denotes branch representing a yeast kinase. Name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification. The shaded box identified protein kinases with significant mutual E values (clustered together to the right of the vertical line indicating a BLAST E value of 10^-80, see Fig. 2).

Figure 3.

Arabidopsis lacks obvious orthologs to PKA and PKC but preserves and sometimes expands other kinase family of the yeast kinase group AGC. The tree displays cluster 8. Branch representing a yeast kinase is labeled with a black diamond, and the corresponding yeast kinase families are labeled at the right end of the tree. The shaded box identified protein kinases with significant mutual E values (clustered together to the right or near left of the vertical line indicating a BLAST E value of 10^-80).

Figure 4.

Expansion of the yeast casein kinase I family member HRR25 and CLK kinase family in Arabidopsis. The tree displays cluster 9. A black diamond denotes a branch representing a yeast kinase, and the corresponding yeast kinase families are labeled at the right end of the tree. Name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification. The shaded box identified protein kinases with significant mutual E values (clustered together to the right of the vertical line indicating a BLAST E value of 10^-80).

Figure 5.

Relative distribution of yeast and Arabidopsis kinases in clusters 11 and 12. The trees for the two clusters are shown in a and b, respectively, with the yeast gene denoted with a black diamond. Name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification. The shaded box identified protein kinases with significant mutual E values (10^-92).

Figure 8.

Trees of MAP2Ks (a) and MAPKs (b). These are subclusters from the tree shown in Figure 2. Branch representing a yeast kinase is denoted by a filled diamond and name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification.

Figure 9.

Expansion of the yeast kinase SNF1 in Arabidopsis. The tree of SnRKs is displayed. It represents a subcluster from the tree shown in Figure 2. Branch representing a yeast kinase is denoted by a black diamond, and name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification. The shaded box identified protein kinases with significant mutual E values (clustered together to the right of the vertical line indicating a BLAST E value of 10^-80).

Figure 10.

The tree of cyclin-dependent protein kinases (CDKs). It represents a subcluster from the tree shown in Figure 2. Branch representing a yeast kinase is denoted by a black diamond, and name(s) previously assigned to an Arabidopsis kinase through experimental characterization, when present, follow an Arabidopsis gene identification. The shaded box identified protein kinases with significant mutual E values (clustered together to the right or near left of the vertical line indicating a BLAST E value of 10^-80).