- Research article
- Open Access
Characterization of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa and Prunus persica
© Immanen et al.; licensee BioMed Central Ltd. 2013
- Received: 24 July 2013
- Accepted: 27 November 2013
- Published: 16 December 2013
Through the diversity of cytokinin regulated processes, this phytohormone has a profound impact on plant growth and development. Cytokinin signaling is involved in the control of apical and lateral meristem activity, branching pattern of the shoot, and leaf senescence. These processes influence several traits, including the stem diameter, shoot architecture, and perennial life cycle, which define the development of woody plants. To facilitate research about the role of cytokinin in regulation of woody plant development, we have identified genes associated with cytokinin signaling and homeostasis pathways from two hardwood tree species.
Taking advantage of the sequenced black cottonwood (Populus trichocarpa) and peach (Prunus persica) genomes, we have compiled a comprehensive list of genes involved in these pathways. We identified genes belonging to the six families of cytokinin oxidases (CKXs), isopentenyl transferases (IPTs), LONELY GUY genes (LOGs), two-component receptors, histidine containing phosphotransmitters (HPts), and response regulators (RRs). All together 85 Populus and 45 Prunus genes were identified, and compared to their Arabidopsis orthologs through phylogenetic analyses.
In general, when compared to Arabidopsis, differences in gene family structure were often seen in only one of the two tree species. However, one class of genes associated with cytokinin signal transduction, the CKI1-like family of two-component histidine kinases, was larger in both Populus and Prunus than in Arabidopsis.
- Cytokinin signaling
- Cytokinin homeostasis
- Populus trichocarpa
- Black cottonwood
- Prunus persica
Cytokinin signaling contributes to the regulation of multiple fundamental processes active in plant development. These include cell division, meristem maintenance, shoot initiation and growth, vascular patterning, flower and seed development, nutrient uptake, chloroplast differentiation and light perception [1–3]. Additionally, this hormone plays a role in regulating several developmental programs defining the life of perennial woody plants, including the activity of vascular cambium, branching pattern of the shoot, and the onset of leaf senescence. The long life span and extensive radial growth contribute to the large size and massive amount of wood present in a tree, creating a stark contrast to the much smaller herbaceous annuals. However, only few studies have thus far been published about the role of cytokinin in the regulation of woody plant development. To facilitate this research, we are now presenting a comprehensive description of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa and Prunus persica. Gene identification in tree genomes was based on homology with Arabidopsis genes, as cytokinin homeostasis and signal transduction pathways have been extensively studied and well-characterized in this species [1–3].
Structurally, cytokinins are adenine derivatives; based on side chain identity they can be classified into four groups representing isopentenyladenine (iP), trans-zeatin (tZ), cis-zeatin, and aromatic cytokinins. iP and tZ are the bioactive forms of this hormone, to which plants respond through a multistep two-component histidine-aspartate (His-Asp-His-Asp) phosphorelay system [4–6]. The phosphorelay is initiated when a cytokinin ligand binds to a histidine kinase receptor, which triggers autophosphorylation of a His residue. After an intramolecular transfer of the phosphoryl to an Asp residue, it will be transferred to a His in a cytosolic histidine phosphotransfer (HPt) protein. The HPts provide a mobile connection between the cytosol and nucleus; they continuously cycle between these two compartments. In the nucleus, the HPt transfers the phosphoryl onto an Asp in a phospho-accepting response regulator (RRs). RRs can be classified into several different types according to their structure and function. Type-B RRs, which belong to the Myb-transcription factors, activate the transcription of cytokinin primary response genes. Among them are the type-A RRs, which are involved in a negative feedback mechanism that helps to fine-tune the function of cytokinin signaling pathway. Type-A RRs repress activity of type-B RRs [4, 7] and are stabilized by HPt mediated phosphorylation (To et al. ). Adding further flexibility to the signaling pathway, many of its components are capable of forming both homo- and heterodimers [9–13]. Different combinations of the two-component elements presumably add diversity into the process and outcome of the phosphorelay.
Cytokinin signaling represents an ancient hormonal pathway. All of its components are already present in the genome of moss Physcomitrella patens[14, 15], indicating that the cytokinin phosphorelay was already functional prior to the development of a well-defined plant vasculature. As compared to the moss, the cytokinin signaling pathway has, however, become more diverse during the evolution of land plants. The number of members in most cytokinin signaling gene families is much higher in the genomes of vascular plants than in Physcomitrella[14, 15]. In general, the dynamic nature of plant genomes has influenced the evolution of all gene families in vascular plants. All angiosperm lineages have undergone reoccurring genome duplications, indicating that polyploidization confers a fitness advantage for plant species. Each advent of a whole genome duplication is subsequently followed by a gradual gene loss; this rediploidization ultimately promotes a new duplication, allowing the process to repeat in a cyclical manner .
To study the structure of cytokinin signaling and homeostasis genes families in woody plants, we sought to characterize and compare them between two hardwood tree species. For the first species in our phylogenetic study, we chose the most common model tree for molecular biology: Populus trichocarpa, black cottonwood. Populus is a fast growing a dioecious tree, which can reach reproductive maturity in four to six years. Populus trees provide a wood source for the pulp and paper industry and have the potential to be developed into a biofuel feedstock . P. trichocarpa has a relatively small diploid (2n = 38) genome with the haploid size of 485 Mbp. The first version of genome assembly was published in 2006 by Tuskan et al. . Due to the challenges of genome assembly in a highly heterozygous tree species, only the current, third genome assembly of P. trichocarpa, has been able to resolve a large number of reads that were previously published as unassembled scaffolds. Specific loci identities have only recently been assigned to all predicted genes. Thanks to these improvements, we have now for the first time been able to reliably recover a complete set of cytokinin signaling and homeostasis genes from a tree species. Accordingly, we will discuss how our analysis differs from previously published reports of P. trichocarpa cytokinin signaling genes [14, 19, 20].
The second hardwood tree species used in this study is the economically important fruit tree peach, Prunus persica. In terms of cultivated surface area, P. persica is the third most important temperate fruit crop. Additionally, it is a member of the economically important Rosaceae family, which includes important crops such as peaches, apples, pears, cherries, plums, apricots, strawberries, almonds, and roses. An international effort has led to the genome sequencing and development of Prunus persica as a genomic model for the Rosaceae family [21–23]. This hardwood tree is a self-pollinating diploid (2n = 16), with a short juvenile period (2–3 years) and a genome size of 265 Mbp [22, 23].
Currently only a little is known about the role of cytokinin signaling in the regulation of tree or fruit development in Rosaceae. The available data indicates that cytokinins are important for fruit development: high hormone levels have been measured in growing peach fruits . It has also been demonstrated that exogenous application of cytokinin on sweet cherry fruits significantly increases fruit size and weight . Additionally, cytokinin treated fruits showed increased fruit firmness, increased fruit soluble solid concentrations and a delay in exocarp coloration . Similar results have also been seen in apples and pears that have been treated exogenously with cytokinin [26–29]. Taking together, these observations indicate that the cytokinin signaling and homeostasis pathways can provide candidate genes for the breeding of fast growing and high quality Rosaceae fruits.
The third species chosen for our study is the most common herbaceous model plant, Arabidopsis thaliana. Arabidopsis provides an excellent reference genome, as its cytokinin homeostasis and signal transduction pathways have been characterized in detail [1–3]. In addition to the contrast between the woody perennial versus herbaceous annual life cycles, the selected three model species differ in their reproductive strategies. Both Prunus and Arabidopsis have hermaphroditic flowers, whereas Populus is a dioecious tree whose genomic sequence was derived from a female plant .
All three model species belong to the rosid clade of angiosperm plants. Populus (Malpighiales) and Prunus (Rosales) belong to the eurosids I subclade (Fabidae), whereas Arabidopsis (Brassicales) belongs to the eurosids II (Malvidae) . They display diverse genome duplication histories: since their last common ancestor, Populus lineage has undergone one whole genome duplication, Arabidopis two, and Prunus none [18, 31, 32]. Based on the genome duplication history and number of synonymous nucleotide substitutions, the molecular-clock rate has been calculated to be faster in Arabidopsis than in Populus. Due to the genome duplication history and gene evolution rate, the Populus genome has on average 1.5 orthologs for each Arabidopsis gene , and Prunus 0.85  (http://www.rosaceae.org/projects/peach_genome/v1.0/homology). The differences in the cytokinin signaling and homeostasis related gene family sizes are consistent with the general genomic trends. We identified a total of 85 genes from the Populus trichocarpa genome and 45 genes from Prunus persica, as compared to the 60 Arabidopsis genes. The gene family structures between the two tree species and Arabidopsis were compared through phylogenetic analyses.
Populus and Prunus homologues of Arabidopsis genes were identified by searching the Populus trichocarpa genome database versions 1.1 and 3.0 using various bioinformatic tools and databases available via the Populus genome portal (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html; http://www.phytozome.net/search.php), and the Prunus persica genome version 1 , using databases available via The Genome Portal of the Department of Energy Joint Genome Institute  (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html), and Phytozome portal  (http://www.phytozome.net/search.php?org=Org_Ptrichocarpa_v3.0; http://www.phytozome.net/search.php?method=Org_Ppersica). The bioinformatics tools included BLAST searches, Gene Ontology (GO), Kyoto Encyclopedia of Genes and Genomes (KEGG), EuKaryotic Orthologous Groups Database (KOG) and ortholog finder. Arabidopsis sequences were identified using The Arabidopsis Information Resource (TAIR). Amino acid sequences were aligned using ClustalW followed by manual adjustments when needed . The best bidirectional hit (BBH) method was used as the first approach to determine orthologous pairs of the cytokinin signaling and response genes in Prunus as described by . Protein sequences were aligned using Jalviewand ClustalW2  followed by manual adjustments where needed. The resulting alignment was precisely back-translated to yield a data matrix of the corresponding nucleotide sequences. Gene models, transcript IDs and physical loci of Populus genes used in construction of phylogenetic trees can be found in Additional file 1: Table S1. Gene models and EST support for Prunus genes can be found in Additional file 2: Table S2 (physical loci of the genes are not available in the current 1.0 version of the genome), and TAIR gene numbers of Arabidopsis genes in Additional file 3: Table S3.
We used a maximum likelihood search strategy on amino acid alignments to investigate orthologs and paralogs in the cytokinin signaling and homeostasis gene families. Sequences were aligned using MUSCLE with default settings . A single most optimal tree for each data set was computed using the RaxML BlackBox web server (http://embnet.vital-it.ch/raxml-bb/) running RaxML version 7.2.8 . Default settings were used with the WAG model of molecular evolution including a gamma parameter. One hundred bootstrap samples were generated to assess support for the inferred relationships. Local bootstrap values (in percentages) are indicated for branches with ≥50% support.
To characterize the genetic components of cytokinin signaling and homeostasis pathways from Populus and Prunus, we identified genes belonging to the six families of cytokinin oxidases (CKXs), isopentenyl transferases (IPTs), LONELY GUY genes (LOGs), two-component receptors, histidine containing phosphotransmitters (HPts), and type-B, type-A, and type-C response regulators (RRs). Below we will briefly summarize what is known about each gene family in Arabidopsis, after which we describe them in our two tree species.
LONELY GUY (LOG) genes
The initial perception of bioactive cytokinins takes place through CRE1-like two-component histidine kinase receptors, which belong to the superfamily of two-component regulators [5, 54]. In addition to the cytokinin receptors, this family contains a two-component histidine kinase CKI1 that is able to activate the cytokinin phosphorelay , five ethylene receptors (ETR1, ETR2, ERS1, ERS2 and EIN4), five phytochromes (PHYA-E), one putative osmosensor (AtHK1), and a histidine kinase (CKI2/AHK5) associated with ethylene and ABA signaling [56–58]. Our focus will be on the CRE1- and CKI1-like subfamilies that are known to participate in cytokinin signaling phosphorelay.
Arabidopsis has three cytokinin receptors: CRE1/WOL/AHK4, AHK2 and AHK3 [5, 54, 59]. These receptors have a cytokinin binding CHASE domain, transmembrane domains, a His kinase domain and a receiver domain which contains the phospho-accepting Asp. They share overlapping functions: single null mutants do not have notable phenotypes, whereas the triple mutant is a severely dwarfed and infertile plant .
One of the three receptors, CRE1, has both kinase and phosphatase activity: upon binding cytokinin it phosphorylates HPts, whereas in the absence of the hormone it instead dephosphorylates them . Its phosphatase activity helps to quickly inactivate the phosphorelay when the cytokinin levels decrease. In addition to the three canonical receptors, Arabidopsis has a fourth two-component histidine kinase, CKI1, which is capable of inducing cytokinin responses . This kinase can initiate the phosphorelay, but independently of cytokinin [6, 60–62]. As it is missing the cytokinin binding CHASE domain, it does not represent a true cytokinin receptor. Further in contrast to the CRE1-like receptors, which are mainly located at the endoplasmic reticulum [11, 63], CKI1 appears to be present at the plasma membrane [4, 64].
Histidine containing phosphotransmitters
Upon binding cytokinin, the CRE1-like receptors initiate phosphorylation of histidine containing phosphotransmitters (HPts), which are continuously cycling between cytosol and nucleus . This movement enables the transfer of phosphoryl groups from the membrane-localized receptors to the nuclear-localized response regulators.
The HPts are characterized by a short motif, HQxKGSSxS, which contains a conserved phospho-accepting His residue (Additional file 8: Figure S5) . In Arabidopsis, five members of the gene family (AHP1-5) contain this canonical consensus motif [69–72]. They share partially redundant functions since higher-order null mutants, that are lacking multiple genes from the same gene family, display a progressively reduced sensitivity to cytokinin .
In contrast to the five canonical members, two Arabidopsis HPt genes, AHP6 and AHP-like (At4g04402), contain an atypical motif lacking the conserved His residue . AHP6 has an inhibitory role on the cytokinin phosphorelay, and has been classified as a pseudo HPt . AHP6 negatively interferes with the phosphorelay, potentially by competing with the other AHPs for interaction with phoshorylated receptors. In Arabidopsis roots, the expression of AHP6 promotes differentiation of protoxylem, the first xylem cell type that forms in a developing vasculature . The negative function of AHP6 contributes to the generation of distinct and well-defined domains of low cytokinin signaling. The function and expression pattern of the AHP-like gene is not known.
Interestingly, both Populus and Prunus have four orthologs of a single Arabidopsis gene, AHP4. However, this is the case also in two monocot species; rice and maize, which both have three orthologs of this gene [73, 75, 76]. Compared to other species, it appears that Arabidopsis has lost its AHP4 homologs during evolution. Somewhat surprisingly, despite the loss of these potentially redundant genes, the phenotype of an Arabidopsis AHP4 null mutant is not very striking. In Arabidopsis, AHP4 is primarily expressed in young flowers, and the null mutant shows slightly more secondary cell wall thickening at some anther tissues; yet its fertility is not impaired . Presumably the AHP4 function is still redundant with the other Arabidopsis HPt proteins. One Populus AHP4 ortholog (PtHP4b) is missing the conserved phospho-accepting His residue. This reflects the situation in monocots, where all three rice AHP4 orthologs , and two from the three maize orthologs, also lack the conserved histidine . These genes appear to have evolved into pseudo-response regulators with a potentially inhibitory role on the cytokinin signaling phosphorelay.
Response regulators (RRs) represent the final components of the cytokinin signaling phosphorelay. The common feature of all RRs is a receiver domain, which contains the phospho-accepting Asp residue as part of the core sequence DD-D-K (Asp Asp-Asp-Lys) [56, 57]. The RRs can be classified into four subfamilies: A-type RRs with the receiver domain; B-type RRs with the receiver domain fused to a DNA-binding (GARP) sequence; C-type RRs, which despite an atypical amino acid sequence of their receiver domain, still contain the phospho-accepting Asp residue; and pseudo RRs lacking the conserved Asp in their receiver domain. Members of the type-A, -B and -C RR subfamilies participate in the cytokinin signaling phoshorelay [56, 57, 78]. The pseudo RRs are, instead of cytokinin signaling, known to function in the regulation of light responses, including circadian rhythms [79–81]. We will not discuss them in this article.
Type-B RRs are DNA-binding transcriptional regulators that positively mediate cytokinin responses [4, 82–84]. They activate transcription of cytokinin primary response genes; among them the type-A RRs. The expression of type-B RRs themselves is not induced through cytokinin signaling; their activity is regulated through phosphorylation of a conserved Asp residue in the receiver domain. At least one Arabidopsis B-type RR, ARR2, is rapidly degraded upon its cytokinin induced phophorylation . This mechanism presumably provides proteolysis mediated feedback regulation for its activity. In Arabidopsis, the type-B RRs share partially redundant functions; higher order null mutants show a progressively decreased sensitivity to cytokinin [84, 86, 87].
The promoters of type-A RR genes contain a high number of B-type RR binding sites [82, 83, 89, 90]. Accordingly, phosphorylated type-B RRs activate the expression of type-A RR genes, which function as negative feedback regulators of cytokinin signaling [8, 91–93]. Type-A RRs may repress the type-B RR activity either by competing with them for phosphotransfer from upstream HPts or by forming inactive heterodimers with them . Similar to the B-type, in general, individual A-type RRs are also redundant in Arabidopsis; sensitivity to cytokinin increases progressively in higher order mutants [86, 87, 91]). Nevertheless, there are also phenotypic differences between Arabidopsis mutants lacking multiple type-A RRs in different combinations. At least two RRs often share highly redundant functions, but these functions differ somewhat from those shared between the other gene pairs [8, 91–93]. It seems likely that some functional specificity has evolved between the different RR genes and contributes to their retention in plant genomes.
The Populus genome contains eleven types-A RRs (PtRR1-11), whereas Prunus has only four, compared to the ten genes present in the Arabidopsis (Figure 6, Additional file 9: Figure S6). Both Ramírez-Carvajal et al.  and Pils and Heyl  identified these same type-A Populus RRs (Figure 6). It appears that Prunus has lost members of this subfamily during its evolution. However, based on the relatively high redundancy between Arabidopsis RRs, this gene family appears to be well buffered against loss of individual genes.
Type-C, or extra, RRs represent a response regulator subfamily characterized by an atypical receiver domain amino acid sequence . Arabidopsis has two of them, ARR22 and ARR24. They display very restricted expression patterns: ARR22 is expressed exclusively in developing seeds , and ARR24 only in developing and mature pollen grains . ARR22 can interact and dephosphorylate HPt proteins in vitro; it thus appears to represent a negative regulator of the cytokinin signaling phosphorelay [78, 95]. In contrast to the type-A RRs, the expression of type-C RRs is not cytokinin inducible [78, 96]. Ectopic over-expression of ARR22 gives rise to a distinct phenotype; the plants are dwarf and sterile . Yet surprisingly, neither a vegetative nor a reproductive phenotype was detected in either single or double null mutants of these two genes [95, 96]. The function of type-C RRs remains elusive.
Compared to the two Arabidopsis genes, Populus has eight type-C RRs (PtARR26-33), whereas interestingly, none was found in the Prunus genome (Figure 6, Additional file 9: Figure S6). Pils and Heyl  identified 10 unnamed type-C Populus RRs, four of which have been removed from the new assembly; whereas PtRR28 and PtRR33 represent newly identified genes on our list. The expansion of type-C subfamily appears to be specific for the evolution of Populus lineage, as we know that several other species have less of them: rice has only two, and both maize and soybean have three . All eight Populus type-C RRs appear to share a common ancestor with the two Arabidopsis extra RRs. Two of them, PtRR27 and PtRR29, have an atypical conserved motif (HD-D-K and DD-E-K, respectively), and may represent pseudo response regulators.
We report here the first comprehensive description of cytokinin signaling and homeostasis gene families in two hardwood tree species; Populus trichocarpa and Prunus persica. Genomes of both species contain the same cytokinin signal transduction components as Arabidopsis, reflecting the ancient origin of this hormone signaling system. In general, the identified gene families were larger in Populus and smaller in Prunus when compared to Arabidopsis.
In contrast to the consensus ratios, some cytokinin signaling and homeostasis gene families have distinctively expanded in one or two of the tree species as compared to Arabidopsis. One of the expanded clades is the CKI1-like subfamily of two-component histidine kinases. This family has three members in both Populus and Prunus, as compared to a single gene in Arabidopsis. This shared expansion indicates that the gene number has probably been multiplied in a common ancestor of the two tree species. Interestingly, in Arabidopsis CKI1 has been shown to participate in the regulation of both reproductive and secondary vascular development. Future research will show if the extra CKI1 orthologs have any role in the control of cambial activity and wood production in tree species.
Another difference is seen in the HPt gene family, where both tree species have four homologs of the single Arabidopsis AHP4 gene. Yet, in this case, several other species also have multiple AHP4 homologs present in their genomes. Some of these homologs appear to represent pseudo HPts, which potentially act to inhibit the cytokinin phosphorelay. It seems that that there has been no tree lineage specific expansion, but that Arabidopsis has instead lost all but one of its AHP4 homologs.
In contrast to the changes shared by both tree species, some gene expansions appear to have taken place only in the Populus lineage. One clade of the LOG gene family, the Populus orthologs of Arabidopsis AtLOG5, has expanded four-fold as compared to either of the two other species. Another gene subfamily, the C-type RRs, has multiplied four-fold in the Populus lineage as compared to Arabidopsis, but has instead disappeared from Prunus. Possibly other RRs have replaced function of this RR class in Prunus. As the function of C-type RRs has remained elusive in Arabidopsis, Populus could potentially turn out to be a better model for studying their activity.
We hope that the identification of cytokinin signaling and homeostasis pathway from two hardwood tree species may serve as a reference upon which functional analyses can be developed to determine the role that cytokinin plays in vegetative and reproductive tree development. Additionally, these genes may serve as potential candidate genes for marker-assisted breeding towards increased wood and fruit production.
This work was funded by a collaborative initiative between the Finnish and Chilean Governments (SusEn by Academy of Finland and CONICYT CCF-01). LM received additional funding from CONICYT, FONDECYT/Regular N°1121021.
- Sakakibara H: Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol. 2006, 57: 431-449. 10.1146/annurev.arplant.57.032905.105231.View ArticlePubMedGoogle Scholar
- Durbak A, Yao H, McSteen P: Hormone signaling in plant development. Curr Opin Plant Biol. 2012, 15: 92-96. 10.1016/j.pbi.2011.12.004.View ArticlePubMedGoogle Scholar
- Hwang I, Sheen J, Müller B: Cytokinin signaling networks. Annu Rev Plant Biol. 2012, 63: 353-380. 10.1146/annurev-arplant-042811-105503.View ArticlePubMedGoogle Scholar
- Hwang I, Sheen J: Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature. 2001, 413: 383-389. 10.1038/35096500.View ArticlePubMedGoogle Scholar
- Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T: Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 2001, 409: 1060-1063. 10.1038/35059117.View ArticlePubMedGoogle Scholar
- Mähönen AP, Higuchi M, Törmäkangas K, Miyawaki K, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T: Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol. 2006, 16: 1116-1122. 10.1016/j.cub.2006.04.030.View ArticlePubMedGoogle Scholar
- Imamura A, Hanaki N, Umeda H, Nakamura A, Suzuki T, Ueguchi C, Mizuno T: Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc Natl Acad Sci U S A. 1998, 95: 2691-2696. 10.1073/pnas.95.5.2691.PubMed CentralView ArticlePubMedGoogle Scholar
- To JP, Deruère J, Maxwell BB, Morris VF, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ: Cytokinin regulates type-a Arabidopsis response regulator activity and protein stability via two-component phosphorelay. Plant Cell. 2007, 19: 3901-3914. 10.1105/tpc.107.052662.PubMed CentralView ArticlePubMedGoogle Scholar
- Dortay H, Mehnert N, Bürkle L, Schmülling T, Heyl A: Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana. FEBS J. 2006, 273: 4631-4644. 10.1111/j.1742-4658.2006.05467.x.View ArticlePubMedGoogle Scholar
- Dortay H, Gruhn N, Pfeifer A, Schwerdtner M, Schmülling T, Heyl A: Toward an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J Proteome Res. 2008, 7: 3649-3660. 10.1021/pr0703831.View ArticlePubMedGoogle Scholar
- Caesar K, Thamm AM, Witthöft J, Elgass K, Huppenberger P, Grefen C, Horak J, Harter K: Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J Exp Bot. 2011, 62: 5571-5580. 10.1093/jxb/err238.PubMed CentralView ArticlePubMedGoogle Scholar
- Punwani JA, Hutchison CE, Schaller GE, Kieber JJ: The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J. 2010, 62: 473-482. 10.1111/j.1365-313X.2010.04165.x.View ArticlePubMedGoogle Scholar
- Veerabagu M, Elgass K, Kirchler T, Huppenberger P, Harter K, Chaban C, Mira-Rodado V: The Arabidopsis B-type response regulator 18 homomerizes and positively regulates cytokinin responses. Plant J. 2012, 72: 721-731. 10.1111/j.1365-313X.2012.05101.x.View ArticlePubMedGoogle Scholar
- Pils B, Heyl A: Unraveling the evolution of cytokinin signaling. Plant Physiol. 2009, 151: 782-791. 10.1104/pp.109.139188.PubMed CentralView ArticlePubMedGoogle Scholar
- Ishida K, Yamashino T, Nakanishi H, Mizuno T: Classification of the genes involved in the two-component system of the moss Physcomitrella patens. Biosci Biotechnol Biochem. 2010, 74: 2542-2545. 10.1271/bbb.100623.View ArticlePubMedGoogle Scholar
- Chapman BA, Bowers JE, Feltus FA, Paterson AH: Buffering crucial functions by paleologous duplicated genes may impart cyclicality to angiosperm genome duplication. Proc Natl Acad Sci USA. 2006, 103: 2730-2735. 10.1073/pnas.0507782103.PubMed CentralView ArticlePubMedGoogle Scholar
- Wullschleger SD, Weston DJ, Difazio SP, Tuskan GA: Revisiting the sequencing of the first tree genome: populus trichocarpa. Tree Physiol. 2013, 33: 357-364. 10.1093/treephys/tps081.View ArticlePubMedGoogle Scholar
- Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, et al: The genome of black cottonwood, populus trichocarpa (torr. & Gray). Science. 2006, 313: 1596-1604. 10.1126/science.1128691.View ArticlePubMedGoogle Scholar
- Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tähtiharju S, Elo A, Decourteix M, Ljung K, Bhalerao R, Keinonen K, Albert VA, Helariutta Y: Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA. 2008, 105: 20032-20037. 10.1073/pnas.0805617106.PubMed CentralView ArticlePubMedGoogle Scholar
- Ramírez-Carvajal GA, Morse AM, Davis JM: Transcript profiles of the cytokinin response regulator gene family in populus imply diverse roles in plant development. New Phytol. 2008, 177: 77-89.PubMedGoogle Scholar
- Sosinski B, Gannavarapu M, Beck LE, Rajapakse S, Ballard RE, Abbott AG: Characterization of microsatellite markers in peach [Prunus persica (L.)Batsch]. Theor Appl Genet. 2000, 101: 421-428. 10.1007/s001220051499.View ArticleGoogle Scholar
- Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott AG: The peach genome. Tree Genetics Genomes. 2012, 8: 531-547. 10.1007/s11295-012-0493-8.View ArticleGoogle Scholar
- Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F, Zuccolo A, Rossini L, Jenkins J, Vendramin E, Meisel LA, Decroocq V, Sosinski B, Prochnik S, Mitros T, Policriti A, Cipriani G, Dondini L, Ficklin S, Goodstein DM, Xuan P, Fabbro CD, Aramini V, Copetti D, Gonzalez S, Horner DS, et al: The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013, 45: 487-494. 10.1038/ng.2586.View ArticlePubMedGoogle Scholar
- Arnau J, Tadeo F, Guerri J, Primo-Millo E: Cytokinins in peach: endogenous levels during early fruit development. Plant Physiol Biochem. 1999, 37: 741-750. 10.1016/S0981-9428(00)86687-5.View ArticleGoogle Scholar
- Zhang C, Whiting M: Improving “Bing” sweet cherry fruit quality with plant growth regulators. Sci Hort. 2011, 127: 341-346. 10.1016/j.scienta.2010.11.006.View ArticleGoogle Scholar
- Ogata R, Saito T, Oshima K: Effect of N-phenyl-N-(4-pyridyl) urea on fruit size: apple, Japanese pear, grapevine and kiwifruit. Acta Hort. 1989, 239: 395-398.View ArticleGoogle Scholar
- Tartarini S, Sansavini S, Ventura M: CPPU control of fruit morphogenesis in apple. Sci Hort. 1993, 53: 273-279. 10.1016/0304-4238(93)90047-T.View ArticleGoogle Scholar
- Zhang C, Tanabe K, Wang S, Tamura F, Yoshida A, Matsumoto K: The impact of cell division and cell enlargement on the evolution of fruit size in Pyrus pyrifolia. Ann Bot. 2006, 98: 537-543. 10.1093/aob/mcl144.PubMed CentralView ArticlePubMedGoogle Scholar
- Zhang C, Lee U, Tanabe K: Hormonal regulation of fruit set, parthenogenesis induction and fruit expansion in Japanese pear. Plant Growth Regul. 2008, 55: 231-240. 10.1007/s10725-008-9279-2.View ArticleGoogle Scholar
- Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE: Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA. 2009, 106: 3853-3858. 10.1073/pnas.0813376106.PubMed CentralView ArticlePubMedGoogle Scholar
- Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH: Synteny and collinearity in plant genomes. Science. 2008, 320: 486-488. 10.1126/science.1153917.View ArticlePubMedGoogle Scholar
- Jung S, Cestaro A, Troggio M, Main D, Zheng P, Cho I, Folta KM, Sosinski B, Abbott A, Celton JM, Arús P, Shulaev V, Verde I, Morgante M, Rokhsar D, Velasco R, Sargent DJ: Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies. BMC Genomics. 2012, 4 (13): 129-doi: 10.1186/1471-2164-13-129View ArticleGoogle Scholar
- Paterson AH, Freeling M, Tang H, Wang X: Insights from the comparison of plant genome sequences. Annu Rev Plant Biol. 2010, 61: 349-372. 10.1146/annurev-arplant-042809-112235. doi: 10.1146/annurev-arplant-042809-112235View ArticlePubMedGoogle Scholar
- Jung S, Staton M, Lee T, Blenda A, Svancara R, Abbott A, Main D: GDR (Genome Database for Rosaceae): integrated web-database for Rosaceae genomics and genetics data. Nucleic Acids Res. 2008, 36 (Database issue): D1034-D1040.PubMed CentralPubMedGoogle Scholar
- Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor N, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I: The genome portal of the department of energy joint genome institute I. V. Nucleic Acids Res. 2012, 40 (database issue): D26-D32.PubMed CentralView ArticlePubMedGoogle Scholar
- Goodstein D, Shu S, Howson R, Neupane R, Hayes R, Fazo J, Mitros T, Dirks W, Hellsten W, Putnam N, Rokhsar D: Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012, 40 (D1): D1178-D1186. 10.1093/nar/gkr944.PubMed CentralView ArticlePubMedGoogle Scholar
- Lamesch P, Berardini T, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander D, Garcia-Hernandez M, Karthikeyan A, Lee C, Nelson W, Ploetz L, Singh S, Wensel A, Huala : The Arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2011, 1-9. doi: 10.1093/nar/gkr1090Google Scholar
- Hulsen T, Huynen M, de Vlieg J, Groenen M: Benchmarking ortholog identification methods using functional genomics data. Genome Biol. 2006, 7: R31-10.1186/gb-2006-7-4-r31.PubMed CentralView ArticlePubMedGoogle Scholar
- Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009, 25: 1189-1191. 10.1093/bioinformatics/btp033. doi: 10.1093/bioinformatics/btp033PubMed CentralView ArticlePubMedGoogle Scholar
- Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32: 1792-1797. 10.1093/nar/gkh340.PubMed CentralView ArticlePubMedGoogle Scholar
- Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 2008, 57: 758-771. 10.1080/10635150802429642.View ArticlePubMedGoogle Scholar
- Werner T, Motyka V, Strnad M, Schmülling T: Regulation of plant growth by cytokinin. Proc Natl Acad Sci U S A. 2001, 98: 10487-10492. 10.1073/pnas.171304098.PubMed CentralView ArticlePubMedGoogle Scholar
- Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T: Cytokinin deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 2003, 15: 2532-2550. 10.1105/tpc.014928.PubMed CentralView ArticlePubMedGoogle Scholar
- Schmülling T, Werner T, Riefler M, Krupková E, Bartrina y Manns I: Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res. 2003, 116: 241-252. 10.1007/s10265-003-0096-4.View ArticlePubMedGoogle Scholar
- Kakimoto T: Identification of plant cytokinin biosynthesis enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol. 2001, 42: 677-685. 10.1093/pcp/pce112.View ArticlePubMedGoogle Scholar
- Takei K, Sakakibara H, Taniguchi M, Sugiyama T: Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: Implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol. 2001, 42: 85-93. 10.1093/pcp/pce009.View ArticlePubMedGoogle Scholar
- Miyawaki K, Matsumoto-Kitano M, Kakimoto T: Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 2004, 37: 128-138. 10.1046/j.1365-313X.2003.01945.x.View ArticlePubMedGoogle Scholar
- Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T: Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci U S A. 2006, 103: 16598-16603. 10.1073/pnas.0603522103.PubMed CentralView ArticlePubMedGoogle Scholar
- Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K, Miyawaki K, Kakimoto T: Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci U S A. 2008, 105: 20027-20031. 10.1073/pnas.0805619105.PubMed CentralView ArticlePubMedGoogle Scholar
- Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H: Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell. 2009, 21: 3152-3169. 10.1105/tpc.109.068676.PubMed CentralView ArticlePubMedGoogle Scholar
- Tokunaga H, Kojima M, Kuroha T, Ishida T, Sugimoto K, Kiba T, Sakakibara H: Arabidopsis lonely guy (LOG) multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation. Plant J. 2012, 69: 355-365. 10.1111/j.1365-313X.2011.04795.x.View ArticlePubMedGoogle Scholar
- Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J: Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 2007, 445: 652-655. 10.1038/nature05504.View ArticlePubMedGoogle Scholar
- Chickarmane VS, Gordon SP, Tarr PT, Heisler MG, Meyerowitz EM: Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc Natl Acad Sci USA. 2012, 109: 4002-4007. 10.1073/pnas.1200636109.PubMed CentralView ArticlePubMedGoogle Scholar
- Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T: In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA. 2004, 101: 8821-8826. 10.1073/pnas.0402887101.PubMed CentralView ArticlePubMedGoogle Scholar
- Kakimoto T: CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science. 1996, 274: 982-985. 10.1126/science.274.5289.982.View ArticlePubMedGoogle Scholar
- Hwang I, Chen HC, Sheen J: Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 2002, 129: 500-515. 10.1104/pp.005504.PubMed CentralView ArticlePubMedGoogle Scholar
- Kakimoto T: Perception and signal transduction of cytokinins. Annu Rev Plant Biol. 2003, 54: 605-627. 10.1146/annurev.arplant.54.031902.134802.View ArticlePubMedGoogle Scholar
- Iwama A, Yamashino T, Tanaka Y, Sakakibara H, Kakimoto T, Sato S, Kato T, Tabata S, Nagatani A, Mizuno T: AHK5 histidine kinase regulates root elongation through an ETR1-dependent abscisic acid and ethylene signaling pathway in Arabidopsis thaliana. Plant Cell Physiol. 2007, 48: 375-380.View ArticlePubMedGoogle Scholar
- Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey N, Helariutta Y: A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 2000, 14: 2938-2943. 10.1101/gad.189200.PubMed CentralView ArticlePubMedGoogle Scholar
- Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T: The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 2001, 42: 1017-1023. 10.1093/pcp/pce127.View ArticlePubMedGoogle Scholar
- Deng Y, Dong H, Mu J, Ren B, Zheng B, Ji Z, Yang WC, Liang Y, Zuo J: Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell. 2010, 22: 1232-1248. 10.1105/tpc.108.065128.PubMed CentralView ArticlePubMedGoogle Scholar
- Pekárová B, Klumpler T, Třísková O, Horák J, Jansen S, Dopitová R, Borkovcová P, Papoušková V, Nejedlá E, Sklenář V, Marek J, Zídek L, Hejátko J, Janda L: Structure and binding specificity of the receiver domain of sensor histidine kinase CKI1 from Arabidopsis thaliana. Plant J. 2011, 67: 827-839. 10.1111/j.1365-313X.2011.04637.x.View ArticlePubMedGoogle Scholar
- Wulfetange K, Lomin SN, Romanov GA, Stolz A, Heyl A, Schmülling T: The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 2011, 156: 1808-1818. 10.1104/pp.111.180539.PubMed CentralView ArticlePubMedGoogle Scholar
- Hejátko J, Ryu H, Kim GT, Dobesová R, Choi S, Choi SM, Soucek P, Horák J, Pekárová B, Palme K, Brzobohaty B, Hwang I: The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell. 2009, 21: 2008-2021. 10.1105/tpc.109.066696.PubMed CentralView ArticlePubMedGoogle Scholar
- Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS: Genome-wide analysis of two-component systems and prediction of stress-responsive two-component system members in soybean. DNA Res. 2010, 17: 303-324. 10.1093/dnares/dsq021.PubMed CentralView ArticlePubMedGoogle Scholar
- Ito Y, Kurata N: Identification and characterization of cytokinin-signalling gene families in rice. Gene. 2006, 382: 57-65.View ArticlePubMedGoogle Scholar
- Pischke MS, Jones LG, Otsuga D, Fernandez DE, Drews GN, Sussman MR: An Arabidopsis histidine kinase is essential for megagametogenesis. Proc Natl Acad Sci USA. 2002, 99: 15800-15805. 10.1073/pnas.232580499.PubMed CentralView ArticlePubMedGoogle Scholar
- Suzuki T, Ishikawa K, Yamashino T, Mizuno T: An Arabidopsis histidine-containing phosphotransfer (HPt) factor implicated in phosphorelay signal transduction: overexpression of AHP2 in plants results in hypersensitiveness to cytokinin. Plant Cell Physiol. 2002, 43: 123-129. 10.1093/pcp/pcf007.View ArticlePubMedGoogle Scholar
- Miyata S, Urao T, Yamaguchi-Shinozaki K, Shinozaki K: Characterization of genes for two-component phosphorelay mediators with a single HPt domain in Arabidopsis thaliana. FEBS Lett. 1998, 437: 11-14. 10.1016/S0014-5793(98)01188-0.View ArticlePubMedGoogle Scholar
- Suzuki T, Imamura A, Ueguchi C, Mizuno T: Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol. 1998, 39: 1258-1268. 10.1093/oxfordjournals.pcp.a029329.View ArticlePubMedGoogle Scholar
- Suzuki T, Sakurai K, Imamura A, Nakamura A, Ueguchi C, Mizuno T: Compilation and characterization of histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci Biotechnol Biochem. 2000, 64: 2486-2489. 10.1271/bbb.64.2486.View ArticlePubMedGoogle Scholar
- Tanaka Y, Suzuki T, Yamashino T, Mizuno T: Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci Biotechol. Biochem. 2004, 68: 462-465. 10.1271/bbb.68.462.View ArticleGoogle Scholar
- Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ: The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell. 2006, 18: 3073-3087. 10.1105/tpc.106.045674.PubMed CentralView ArticlePubMedGoogle Scholar
- Mähönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Törmäkangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y: Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science. 2006, 311: 94-98. 10.1126/science.1118875.View ArticlePubMedGoogle Scholar
- Tsai YC, Weir NR, Hill K, Zhang W, Kim HJ, Shiu SH, Schaller GE, Kieber JJ: Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol. 2012, 158: 1666-1684. 10.1104/pp.111.192765.PubMed CentralView ArticlePubMedGoogle Scholar
- Chu ZX, Ma Q, Lin YX, Tang XL, Zhou YQ, Zhu SW, Fan J, Cheng BJ: Genome-wide identification, classification, and analysis of two-component signal system genes in maize. Genet Mol Res. 2011, 10: 3316-3330. 10.4238/2011.December.8.3.View ArticlePubMedGoogle Scholar
- Jung KW, Oh SI, Kim YY, Yoo KS, Cui MH, Shin JS: Arabidopsis histidine-containing phosphotransfer factor 4 (AHP4) negatively regulates secondary wall thickening of the anther endothecium during flowering. Mol Cells. 2008, 25: 294-300.PubMedGoogle Scholar
- Kiba T, Aoki K, Sakakibara H, Mizuno T: Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the wol cytokinin-receptor mutant. Plant Cell Physiol. 2004, 45: 1063-1077. 10.1093/pcp/pch128.View ArticlePubMedGoogle Scholar
- Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Ueguchi C, Sugiyama T, Mizuno T: Genes encoding pseudo-response regulators: insight into His-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol. 2000, 41: 791-803. 10.1093/pcp/41.6.791.View ArticlePubMedGoogle Scholar
- Mizuno T: Plant response regulators implicated in signal transduction and circadian rhythm. Curr Opin Plant Biol. 2004, 7: 499-505. 10.1016/j.pbi.2004.07.015.View ArticlePubMedGoogle Scholar
- Murakami M, Yamashino T, Mizuno T: Characterization of circadian-associated APRR3 pseudo-response regulator belonging to the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 2004, 45: 645-650. 10.1093/pcp/pch065.View ArticlePubMedGoogle Scholar
- Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A: ARR1, a transcription factor for genes immediately responsive to cytokinins. Science. 2001, 294: 1519-1521. 10.1126/science.1065201.View ArticlePubMedGoogle Scholar
- Imamura A, Kiba T, Tajima Y, Yamashino T, Mizuno T: In vivo and in vitro characterization of the ARR11 response regulator implicated in the His-to-Asp phosphorelay signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 2003, 44: 122-131. 10.1093/pcp/pcg014.View ArticlePubMedGoogle Scholar
- Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE: Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell. 2005, 17: 3007-3018. 10.1105/tpc.105.035451.PubMed CentralView ArticlePubMedGoogle Scholar
- Kim K, Ryu H, Cho YH, Scacchi E, Sabatini S, Hwang I: Cytokinin-facilitated proteolysis of ARABIDOPSIS RESPONSE REGULATOR 2 attenuates signaling output in two-component circuitry. Plant J. 2012, 69: 934-945. 10.1111/j.1365-313X.2011.04843.x.View ArticlePubMedGoogle Scholar
- Ishida K, Yamashino T, Yokoyama A, Mizuno T: Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol. 2008, 49: 47-57. 10.1093/pcp/pcm165.View ArticlePubMedGoogle Scholar
- Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE: Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell. 2008, 20: 2102-2116. 10.1105/tpc.108.059584.PubMed CentralView ArticlePubMedGoogle Scholar
- Tajima Y, Imamura A, Kiba T, Amano Y, Yamashino T, Mizuno T: Comparative studies on the type-B response regulators revealing their distinctive properties in the His-to-Asp phosphorelay signal transduction of Arabidopsis thaliana. Plant Cell Physiol. 2004, 45: 28-39. 10.1093/pcp/pcg154.View ArticlePubMedGoogle Scholar
- Lohrmann J, Buchholz G, Keitel C, Sweere U, Kircher S, Bäurle I, Kudla J, Schäfer E, Harter K: Differential expression and nuclear localization of response regulator-like proteins from Arabidopsis thaliana. Plant Biol. 1999, 1: 495-505. 10.1111/j.1438-8677.1999.tb00775.x.View ArticleGoogle Scholar
- Rashotte AM, Carson SD, To JP, Kieber JJ: Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 2003, 132: 1998-2011. 10.1104/pp.103.021436.PubMed CentralView ArticlePubMedGoogle Scholar
- To JPC, Haberer G, Ferreira FJ, Deruère J, Mason MG, Schaller GE, Alonso JM, Ecker JR, Kieber JJ: Type-A Arabidopsis response regulators are partially reduntant negative regulators of cytokinin signaling. Plant Cell. 2004, 16: 658-671. 10.1105/tpc.018978.PubMed CentralView ArticlePubMedGoogle Scholar
- Buechel S, Leibfried A, To JP, Zhao Z, Andersen SU, Kieber JJ, Lohmann JU: Role of A-type ARABIDOPSIS RESPONSE REGULATORS in meristem maintenance and regeneration. Eur J Cell Biol. 2010, 89: 279-284. 10.1016/j.ejcb.2009.11.016.View ArticlePubMedGoogle Scholar
- Zhang W, To JP, Cheng CY, Eric Schaller G, Kieber JJ: Type-A response regulators are required for proper root apical meristem function through post-transcriptional regulation of PIN auxin efflux carriers. Plant J. 2011, 68: 1-10. 10.1111/j.1365-313X.2011.04668.x.View ArticlePubMedGoogle Scholar
- Kim J: Phosphorylation of A-Type ARR to function as negative regulator of cytokinin signal transduction. Plant Signal Behav. 2008, 3: 348-350. 10.4161/psb.3.5.5375.PubMed CentralView ArticlePubMedGoogle Scholar
- Horák J, Grefen C, Berendzen KW, Hahn A, Stierhof YD, Stadelhofer B, Stahl M, Koncz C, Harter K: The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol. 2008, 8: 77-10.1186/1471-2229-8-77.PubMed CentralView ArticlePubMedGoogle Scholar
- Gattolin S, Alandete-Saez M, Elliott K, Gonzalez-Carranza Z, Naomab E, Powell C, Roberts JA: Spatial and temporal expression of the response regulators ARR22 and ARR24 in Arabidopsis thaliana. J Exp Bot. 2006, 57: 4225-4233. 10.1093/jxb/erl205.View ArticlePubMedGoogle Scholar
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