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First published online June 13, 2008; 10.1104/pp.108.123380 Plant Physiology 147:2084-2095 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Interactions between the S-Domain Receptor Kinases and AtPUB-ARM E3 Ubiquitin Ligases Suggest a Conserved Signaling Pathway in Arabidopsis1,[W],[OA]Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada M5S 3B2
The Arabidopsis (Arabidopsis thaliana) genome encompasses multiple receptor kinase families with highly variable extracellular domains. Despite their large numbers, the various ligands and the downstream interacting partners for these kinases have been deciphered only for a few members. One such member, the S-receptor kinase, is known to mediate the self-incompatibility (SI) response in Brassica. S-receptor kinase has been shown to interact and phosphorylate a U-box/ARM-repeat-containing E3 ligase, ARC1, which, in turn, acts as a positive regulator of the SI response. In an effort to identify conserved signaling pathways in Arabidopsis, we performed yeast two-hybrid analyses of various S-domain receptor kinase family members with representative Arabidopsis plant U-box/ARM-repeat (AtPUB-ARM) E3 ligases. The kinase domains from S-domain receptor kinases were found to interact with ARM-repeat domains from AtPUB-ARM proteins. These kinase domains, along with M-locus protein kinase, a positive regulator of SI response, were also able to phosphorylate the ARM-repeat domains in in vitro phosphorylation assays. Subcellular localization patterns were investigated using transient expression assays in tobacco (Nicotiana tabacum) BY-2 cells and changes were detected in the presence of interacting kinases. Finally, potential links to the involvement of these interacting modules to the hormone abscisic acid (ABA) were investigated. Interestingly, AtPUB9 displayed redistribution to the plasma membrane of BY-2 cells when either treated with ABA or coexpressed with the active kinase domain of ARK1. As well, T-DNA insertion mutants for ARK1 and AtPUB9 lines were altered in their ABA sensitivity during germination and acted at or upstream of ABI3, indicating potential involvement of these proteins in ABA responses.
The process of ubiquitin-mediated protein degradation is activated in many biological processes during the plant life cycle and is an equally important step in the regulation of protein activities (Moon et al., 2004  ; Smalle and Vierstra, 2004). Disruptions to the process can lead to prolonged activity of a target protein and clearly have effects on the plant growth and development. Three enzymes are involved in the ubiquitination of a target protein, the E1 ubiquitin-activating enzyme, the E2 ubiquitin-conjugating enzyme, and the E3 ubiquitin ligase. By far, the E3 ubiquitin ligase is the largest group of these enzymes that is related to its role in defining the substrate specificity in this pathway (Devoto et al., 2002; Dill et al., 2004). For example, there are two E1 enzymes and 41 E2 enzymes annotated in the Arabidopsis (Arabidopsis thaliana) genome (Kraft et al., 2005). The E3 ligase group is a far more diverse group and, based on known E3 ligase motifs, there are at least 1,300 predicted E3 ligase genes in the Arabidopsis genome (Smalle and Vierstra, 2004). The larger known Arabidopsis families include the RING family with approximately 469 predicted proteins and the F-box family with approximately 700 predicted proteins (Gagne et al., 2004; Stone et al., 2005). The Arabidopsis U-box family is a smaller predicted family with 62 members (Azevedo et al., 2001; Andersen et al., 2004).
The U-box is an E3 ligase motif conserved in all eukaryotes (Aravind and Koonin, 2000
The Brassica and tobacco studies suggest a role for the PUB-ARM proteins as potential signaling proteins for receptor kinases. In Arabidopsis, there are a large number of receptor kinases with a range of extracellular domains (Morris and Walker, 2003 The observed interaction between Brassica SRK-ARC1 and tobacco CHRK1-NtPUB4 and the conservation of signaling components across Brassica and Arabidopsis suggested to us that the Arabidopsis S-domain receptor kinase family could potentially utilize the numerous AtPUB-ARM family members as their downstream signaling components. To investigate this, we have performed a selected interaction screen between the SD1 receptor kinases and AtPUB-ARM family proteins and identified either common or specific interactors. Further analyses of these interactions were carried out using in vitro phosphorylation assays and transient expression assays. In addition, potential links to the plant hormone abscisic acid (ABA) were further investigated by functional analyses with selected SD1 receptor kinase and AtPUB-ARM proteins.
AtPUB-ARM Proteins Interact with Arabidopsis and Brassica S-Domain Receptor Kinases
A directed yeast two-hybrid interaction screen was conducted with ARM-repeat domains from multiple AtPUB-ARM proteins (Fig. 1A
) against kinase domains from selected receptor kinases. AtPUB-ARM proteins were chosen to represent the different modular combinations found in the AtPUB-ARM family (Fig. 1A; Mudgil et al., 2004
The various kinases included the Arabidopsis S-domain receptor kinases representing various subgroups: SD1-7 (ARK1), SD1-6 (ARK2), SD1-8 (ARK3), SD1-29, SD1-13 (RKS2), SD1-1, SD2-5, SD2-2 (RLK4), SD3-1, DUF26-21 (RKC1), and DUF26-4 (RLK3), along with two Arabidopsis Leu-rich repeat (LRR) receptor kinases, LRR XI-16 (HAESA) and LRR XI-23. In addition, related Brassica SD1 receptor kinases, SFR1, SFR2, and SRK910, which were previously shown to interact with Brassica ARC1, were included in the screen (Mazzurco et al., 2001 ). Selected kinase domains were tested for kinase activity by using an in vitro autophosphorylation assay with purified glutathione S-transferase (GST):kinase fusion proteins. The kinase domains were found to have strong autophosphorylation activity as shown in Figure. 1B or as previously shown (Mazzurco et al., 2001). Protein expression of all the constructs in the transformed yeast (Saccharomyces cerevisiae) was confirmed using immunoblot analysis with either the VP16 or LexA antibodies. From the yeast two-hybrid analyses, it was found that the kinase domains from selected SD1 receptor kinases generally interacted well with the AtPUB-ARM proteins while very low-level or no interactions were observed with non-SD1 receptor kinase family members (Fig. 1C). For example, AtPUB13, 14, and 9 interacted with all the Arabidopsis and Brassica SD1 receptor kinases as well as SD2-5, but no interactions were observed with the remaining receptor kinases. AtPUB38 also interacted with a number of the Arabidopsis and Brassica SD1 receptor kinases as well as DUF26-21. SD1-29 was the only kinase domain that interacted with all the AtPUBs tested (Fig. 1C). Thus, AtPUB-ARM proteins tended to show interaction patterns that were largely confined to the SD1 subfamily of receptor kinases. However, within the SD1 receptor kinase subgroup, there appeared to be less specificity with several AtPUB-ARM proteins interacting with all the kinase domains from selected SD1 receptor kinases.
To further characterize some of the interacting partners from the yeast two-hybrid screen, we evaluated the ability of SD1 receptor kinases to phosphorylate PUB-ARM proteins in vitro. As well, a second kinase implicated in Brassica SI, the Brassica M-locus protein kinase (MLPK), was tested. MLPK belongs to the receptor-like cytoplasmic kinase (RLCK) subfamily and is another positive regulator of the SI response, although MLPK's cellular mechanism in this response remains unknown (Murase et al., 2004
As previously shown, Brassica SRK910 shows some phosphorylation activity for ARC1 as a substrate in vitro (Gu et al., 1998 ; Fig. 2A). Interestingly, MLPK showed a much stronger phosphorylation of ARC1, relative to SRK910 (Fig. 2A). Control lanes without any kinase added exhibited no observable signal, indicating the lack of cross-reacting proteins or background phosphorylation (Fig. 2A). For AtPUB9 and AtPUB13, four Arabidopsis receptor kinases were tested: the SD1 receptor kinases, ARK1, ARK2, and SD1-29; and the LRR receptor kinase, HAESA. ARK1, ARK2, and SD1-29 interacted with AtPUB9 and AtPUB13, whereas HAESA did not (Fig. 1C). When AtPUB13 was used as the substrate, MLPK, ARK1, and ARK2 were able to efficiently phosphorylate the ARM domain of AtPUB13 (Fig. 2B). SD1-29, which was an interactor, did not have any readily detectable activity toward AtPUB13. HAESA served as a negative control and did not phosphorylate AtPUB13 as expected (Fig. 2B). Similar profiles were also seen when the ARM domain of AtPUB9 was subjected to the same treatment where MLPK, ARK1, and ARK2 displayed the best phosphorylation activity toward AtPUB9 (Fig. 2C).
We have previously shown that transient coexpression of Brassica SRK910 with Brassica ARC1 in tobacco BY-2 cells resulted in relocalization of Brassica ARC1 from the cytosol/nucleus to endoplasmic reticulum (ER)-associated proteasomes (Stone et al., 2003
Cotransformations of the PUB-ARM constructs with the different kinases produced a number of different subcellular localization changes. When the SRK910 and ARC1 constructs were coexpressed, SRK910 remained cytosolic (Fig. 3T), whereas ARC1 showed a punctuate localization pattern reminiscent of the ER-localized proteasomes as previously observed with ARC1 (Fig. 3S; Stone et al., 2003 ). Interestingly, the coexpression of both MLPK and ARC1 resulted in both proteins targeted to the perinuclear region (Fig. 3, Y and Z). Thus, the ability of MLPK to both phosphorylate and alter localization of ARC1 suggests that, along with SRK, MLPK could be utilizing ARC1 as a downstream intracellular target. For AtPUB13, the coexpression of MLPK:MYC with AtPUB13 resulted in both proteins being targeted to the perinuclear region (Fig. 3, O and P). This suggests that MLPK has a similar effect on the two UND-containing proteins, ARC1 and AtPUB13. In contrast, the coexpression of either ARK1 or ARK2 with GFP:PUB13 resulted in no alterations to either AtPUB13 (Fig. 3, U and AA) or the kinases (Fig. 3, V and BB). When the GFP:AtPUB9 localization patterns were analyzed, AtPUB9's predominant nuclear localization (Fig. 3K) changed to a cytosolic distribution, with exclusion from the nucleus in the presence of either MLPK or ARK2 (Fig. 3, Q and CC). In approximately 40% of these cells, AtPUB9 was also found in punctuate structures in the cytosol. Interestingly, when ARK1 was coexpressed with GFP:PUB9, localization of RFP:ARK1 to the nucleus (Fig. 3X) resulted in complete loss of nuclear-localized AtPUB9, and instead AtPUB9 was relocalized to the plasma membrane (Fig. 3W).
To determine whether either AtPUB9's E3 ligase activity or ARK1's kinase activity were required for the redistribution of AtPUB9 to the plasma membrane, mutations were introduced to knock out the respective activities. An AtPUB9 E3 ligase activity-deficient (ld) mutant was created by mutating a conserved Val previously shown to be required for E3 ligase activity (V91R; Zeng et al., 2004
To create a kinase-deficient (kd) version of ARK1, the conserved Lys-547 residue was changed to Ala (K547A) because this had been previously shown to abolish kinase activity of ARK1 (Tobias and Nasrallah, 1996 ). When the kinase activity of the purified recombinant GST:ARK1kd protein was analyzed, it did not have any autophosphorylation activity and it failed to use AtPUB9 as a substrate (Fig. 4C). When the kinase deficient RFP:ARK1kd construct was co-expressed with GFP:PUB9, both proteins were found in the nucleus (Fig. 4, D and E). Therefore, the redistribution of AtPUB9 to the plasma membrane is a phosphorylation-dependent process. Interestingly, we have previously shown that SRK910 induces a phosphorylation-dependent relocalization of ARC1 to ER-associated proteasomes (Stone et al., 2003).
Given the subcellular localization patterns observed for the PUB-ARM proteins in the presence of different kinases, we also investigated whether there were any treatments that could also cause changes in their subcellular localization patterns. To select some candidate treatments, microarray databases were examined for conditions that led to increased transcript levels for the AtPUB-ARM genes and ABA was found to increase AtPUB9 transcript levels rapidly within 1 h (Toufighi et al., 2005
The ability of the active ARK1 kinase domain and ABA treatment to cause membrane localization of AtPUB9 in BY-2 cells prompted us investigate the in vivo functional role of ARK1 and PUB9 in mediating ABA responses. Homozygous SALK T-DNA insertion lines were identified for PUB9 (pub9) and ARK1 (ark1.1, ark1.2), and the loss of mRNA transcripts in these lines was confirmed through reverse transcription (RT)-PCR (Fig. 5, A and B ). When seeds from pub9–/– and ark1.1–/– lines were analyzed for their ability to germinate under various concentrations of ABA, we observed that both lines exhibited hypersensitivity to 1 µM ABA when compared to wild-type Columbia (Col-0) seeds (Fig. 5C). Similar results were also observed for ark1.2–/– mutants. To test whether the loss of both AtPUB9 and ARK1 would cause an additive effect, ark1.1–/–, pub9–/– double-homozygous mutants were generated and tested for ABA sensitivity during seed germination. The ark1.1–/–, pub9–/– double mutants displayed a level of ABA sensitivity that was similar to the single mutants (Fig. 5C). The lack of any additive effect resulting from the loss of both loci suggests that ARK1 and AtPUB9 most likely functioned in a linear fashion.
The ABA sensitivity phenotype exhibited by the ark1–/– and pub9–/– single and double mutants was specific to the seed germination phase of development since no changes were observed in root growth in the presence of ABA (Fig. 5D). A similar lack of effect was also observed with ACC, even though this compound was able to (although to a lesser extent) cause plasma membrane relocalization of AtPUB9 in BY-2 cells. No phenotypic difference was observed between Col-0 and the pub9–/– and ark1.1–/– seedlings when grown on plates containing 30 µM ACC under dark or light conditions (Supplemental Fig. S2).
With both the ark1–/– and pub9–/– mutants displaying ABA hypersensitivity during seed germination, it was of interest to map where these genes functioned relative to a well-characterized ABA response gene, ABI3 (Nambara et al., 1994
The superfamily of predicted Arabidopsis receptor kinases consists of 610 members with 417 members possessing an extracellular domain, a single-pass transmembrane domain, and an intracellular kinase domain (Shiu and Bleecker, 2001a , 2001b). Some of these receptor kinases have been identified to play a role in plant cell differentiation, hormonal response pathways, plant growth and development, and pathogen perception (Li and Chory, 1997; Gomez-Gomez and Boller, 2000; Clouse, 2002; Morris and Walker, 2003; Osakabe et al., 2005). However, functions of most of the kinases are still unknown. Many of these receptors may participate in the plant surveillance system to sense changes in the environment and transmit the appropriate signal intracellularly through their kinase domains.
One of the primary challenges in studying plant receptor kinases is the identification of their downstream components or interacting partners. Both genetic and yeast interaction screens have been used by several groups for this purpose (for review, see Johnson and Ingram, 2005
In this article, we also investigated potential connections with the MLPK, which had previously been identified in the Brassica SI response (Murase et al., 2004
Previous studies have shown that Brassica ARC1 has targeting signals to allow shuttling between the cytosol and the nucleus and the presence of the activated kinase domain from SRK910 causes ARC1 to relocalize to ER-associated proteasomes (Stone et al., 2003
With the conservation of interactions between Arabidopsis SD1 receptor kinases and PUB-ARM proteins, the question remains as to what biological processes these signaling networks could be regulating. As a first step toward answering this question, we found that the subcellular location of AtPUB9 in BY-2 cells could be redirected to the plasma membrane by treatment with 10 µM ABA, replicating the ARK1 effect. Given that the plasma membrane is the predicted location of full-length SD1 receptor kinases, it is conceivable that AtPUB9 is interacting with related SD1 receptor kinases in the BY-2 cells. This observation is quite interesting because the plasma membrane is one of the major sites of action for ABA, where ABA controls various membrane-bound transporters and ion channels regulating the closure of stomata (Finkelstein et al., 2002
A biological role for both AtPUB9 and ARK1 in ABA responses is supported by the ABA germination assays, where the pub9, ark1.1, and ark1.2 mutant seeds displayed a hypersensitive response to ABA. This would suggest a negative regulatory role for ARK1 and AtPUB9 in ABA responses during germination. Interestingly, the ABA-insensitivity genes, ABI1 and ABI2, which encode protein phosphatase 2C, have been proposed to be negative regulators of ABA signaling (Leung et al., 1994
Whether ARK1 plays a primary role in the perception of ABA or a secondary role following the activation of ABA receptors is not known. Our epistatic analysis places the role of AtPUB9 during ABA responses upstream or at the same level of the transcription factor, ABI3, whereas our crosses of ARK1-deficient lines with abi3-6 failed to isolate any double homozygotes, indicating a genetic interaction between these two loci. ABI3 has been previously shown to play a role in ABA responses at or downstream of the ERA1 farnesyl transferase, whereas the ABI1 and ABI2 protein phosphatases act at or upstream of ERA1 (Brady et al., 2003
Yeast Two-Hybrid Interactions
Plasmid Constructs
Yeast Transformation
For purification of the His-tagged fusion proteins, 50 to 200 mL of 2x YT containing 100 µg mL–1 ampicillin was inoculated with 1/100th volume of an overnight culture and grown to an OD600 of 0.8 at 37°C. Isopropyl β-D-thiogalactoside was added to a final concentration of 0.5 mM induced at 37°C for 5 to 6 h, pelleted, resuspended in 10 mL of binding buffer (50 mM Tris, pH 7.5, 500 mM NaCl, 5 mM imidazole, 5% glycerol, 500 µM phenylmethylsulfonyl fluoride [PMSF], and 1 mM benzanidine), and followed with sonication. Triton X-100 was added to a final concentration of 0.01%, and the samples were spun at 17,000 rpm for 10 min at 4°C. To the supernatant, 1 mL of 50% (v/v) nickel nitrilotriacetic acid agarose washed and pre-equilibrated with binding buffer was added and mixed for 30 min at room temperature. The beads were washed four times each with 10 mL of wash buffer (50 mM Tris, pH 7.5, 500 mM NaCl, 30 mM imidazole, 5% glycerol, 500 µM PMSF, and 1 mM benzanidine). The His-tagged fusion proteins were eluted with elution buffer (50 mM Tris, pH 7.5, 500 mM NaCl, 500 mM imidazole, 5% glycerol, 500 µM PMSF, and 1 mM benzanidine), and the samples were stored at 4°C. For purification of the GST-tagged fusion proteins, the cells were induced at 16°C overnight, pelleted, resuspended in 10 to 20 mL of G-lysis buffer (50 mM HEPES, pH 7.4, 150 mM NaCl, 10 mM EDTA, 1 mM dithiothreitol, 200 µM PMSF), and frozen overnight at –20°C. The samples were thawed, PMSF was added again to a final concentration of 200 µM, and the samples were sonicated in 15-s bursts by using a probe sonicator. Triton X-100 was added to a final concentration of 1% and the samples were spun at 17,000 rpm for 10 min at 4°C. To the supernatant, 2 mL of 10% (v/v) glutathione-agarose was added and mixed for 30 min at 4°C. The beads were washed three times each with 2 mL of lysis buffer, resuspended in 6 mL of lysis buffer, and poured into a column. The GST fusions were eluted with elution buffer (50 mM HEPES, pH 8.0, 15 mM glutathione), glycerol was added to a final concentration of 20%, and the samples were stored at –20°C.
A subset of kinase domains, used for the yeast two-hybrid interactions, was subcloned from the pBTM116 vector into pGEX 4T.1 or pGEX 5X-2 vector, except for MLPK where a full-length protein was used. Kinase domains for which restriction sites were not available were amplified by PCR, cloned into pGEMT vector, sequenced, and error-free fragments were cloned into pGEX 4T or pGEX 5X-2. Site-directed mutagenesis was used to construct the kinase-deficient (K547A) catalytic domain of GST:ARK1 construct (Quickchange; Stratagene). These constructs were overexpressed in BL-21 DE3 p-Lys strain of Escherichia coli and purified as described above. For the autophosphorylation assays, approximately 0.5 µg of the purified GST:kinases were used in the autophosphorylation assays as previously described (Mazzurco et al., 2001
For the ARM domain constructs, His-tagged fusions of AtPUB9 and 13 ARM domains were constructed in PET15b, whereas the ARC1 ARM domain was cloned as a GST-tagged fusion protein. Proteins were overexpressed and purified as described above. For the kinase assay, approximately 0.1 µg of the active GST:kinase fusion proteins were mixed with 0.5 µg of the ARM domain fusion proteins in a 20-µL reaction with 20 mM HEPES, pH 7.0, 10 mM MgCl2, 2 mM MnCl2, 10 µg/mL aprotinin, and either 100 µM ATP or 5 µCi of [
Biolistic bombardments of cultured tobacco (Nicotiana tabacum) BY-2 cells were performed essentially as described previously (Stone et al., 2003
The kinase domain from the ARK1 receptor kinase was cloned into pRTL2 as an RFP-fused construct and ARK2 as a GST-fused construct, whereas a MYC tag was added to the C terminus of MLPK through PCR and cloned into pRTL2 vector. These constructs were bombarded into BY-2 cells either alone or in various combinations. Cells were fixed with 4% paraformaldehyde and visualized either directly through fluorescent microscopy for detecting GFP or incubated with either rabbit anti-GST or mouse anti-MYC antibodies, followed by fluorescence microscopy as described previously (Stone et al., 2003 For hormone treatments of cells 20 h after transformation, the transformed cells were treated with various hormones such as ABA, 2,4D, ACC, methyl jasmonate, and GA at 10 µM concentration for 2 h, fixed, and visualized as described above. Control cells were treated either with water or 0.0001 N NaOH.
All genotypes reported were grown under standard growth conditions at constant 22°C light. The ark1.1 pub9 double mutants were generated by crossing pub9 plants with ark1.1 pollen and genotyping T2 for double-mutant plants. For epistatic analysis, pollen from abi3-6, a severe ABA-insensitive allele of ABI3 (At3g24650) that contains an internal deletion, was used to cross both ark1.1 and pub9 plants. Both desiccated seeds and seeds with green embryos (a nondesiccating phenotype of abi3-6) were genotyped for both the insertion and presence of ABI3-6 allele to identify double mutants.
Seeds (approximately 75–100) from the various T-DNA insertion lines, SALK_024564 (ark1.1), SALK_002112 (ark1.2), and SALK_020751 (pub9), ark1.1/pub9 double homozygotes, abi3-6 and abi3-6/pub9 double homozygotes were plated on 0.5x Murashige and Skoog (MS) plates containing varying concentrations of ABA, stratified in the dark for 3 d, followed by germination under light. Germination was measured on days 4 and 5, poststratification, and plotted as the germination ratio relative to wild-type Col-0. The values represent the mean ± SE (n = 4). For examining the inhibitory effect of ABA on root elongation, Col-0, ark1.1, pub9, and ark1.1/pub9 double-homozygous seeds were germinated and grown vertically on 0.5x MS plates for 5 d, followed by transfer to ABA plates and grown for 5 d. The root lengths were measured prior to transfer to ABA plates and post-ABA treatment and the extent of inhibition was expressed as a ratio of root growth (in mM) on ABA/root growth (in mM) on 0.5x MS plates prior to transfer to ABA plates. The values represent the mean ± SE (n > 10). For ethylene treatments, seeds from the various lines were plated on 0.5x MS plates with 30 µM ACC, stratified for 4 d, and left at 22°C either in the dark or under light for 5 d before observation for ethylene responses.
The following materials are available in the online version of this article.
We are very grateful to Dr. Robert Mullen, University of Guelph, for providing the pRTL2 vector and tobacco BY-2 cells, as well as helpful discussions on this article. We are also very grateful to Dr. Seiji Takayama, Nara Institute of Science and Technology, for providing the MLPK cDNA, and to Dr. Peter McCourt, University of Toronto, for providing the abi3-6 seeds. Received May 22, 2008; accepted June 8, 2008; published June 13, 2008.
1 This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada and a Canada Research Chair to D.R.G. 
2 These authors contributed equally to the article.
3 Present address: Department of Biology, The University of North Carolina, Coker Hall, Chapel Hill, NC 27599. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Daphne R. Goring (d.goring{at}utoronto.ca).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.123380 * Corresponding author; e-mail d.goring{at}utoronto.ca.
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32P]-labeled autophosphorylation assay followed by autoradiography. C, Yeast two-hybrid interactions between selected kinase domains and ARM domains. For all AtPUB-ARMs, the entire ARM region following the U-box was used. The exception is AtPUB44a and AtPUB44b, where the longer ARM repeat region was split in half, with each half being tested. The Arabidopsis receptor kinase nomenclature used is according to Shiu and Bleecker (2003)
