Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain

Heyl, Alexander; Wulfetange, Klaas; Pils, Birgit; Nielsen, Nicola; Romanov, Georgy A.; Schmülling, Thomas

doi:10.1186/1471-2148-7-62

Cited by 66 publications

(58 citation statements)

References 42 publications

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“…In contrast, the proteins of the third branch only had the CHASE domain in common but otherwise, displayed a rather diverse array of different domains, such as Guanylate Cylclase or Phosphodiesterase. When we looked at the conservation of those residues of the CHASE domain that were shown to be important for its structure and cytokinin binding (Heyl et al, 2007;Hothorn et al, 2011), a high level of conservation was found among the classical cytokinin receptors, whereas members of the newly identified subfamily had only a very low level of conservation compared with the CHASE domain of Arabidopsis histidine kinase4 (AHK4; Fig. 1B).…”

Section: A Subfamily Of Cytokinin Receptors Emergedmentioning

confidence: 99%

“…Cytokinin receptors are hybrid His kinases, because they contain both an His kinase and an RR domain. The cytokinin ligand is bound through the cyclase/His kinase-associated sensory extracellular (CHASE) domain (Anantharaman and Aravind, 2001;Mougel and Zhulin, 2001;Heyl et al, 2007), and this binding is thought to trigger a conformational change, leading to the autophosphorylation of the receptor (Miwa et al, 2007;Hothorn et al, 2011). After an intramolecular transfer from the His kinase to the RR domain of the receptor, the phosphate is transferred to His phosphotransfer (HPTs) proteins.…”

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A Subfamily of Putative Cytokinin Receptors Is Revealed by an Analysis of the Evolution of the Two-Component Signaling System of Plants

et al. 2014

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The two-component signaling system-the major signaling pathway of bacteria-is found among higher eukaryotes only in plants, where it regulates diverse processes, such as the signaling of the phytohormone cytokinin. Cytokinin is perceived by a hybrid histidine (His) kinase receptor, and the signal is transduced by a multistep phosphorelay system of His phosphotransfer proteins and different classes of response regulators (RRs). To shed light on the origin and evolution of the two-component signaling system members in plants, we conducted a comprehensive domain-based phylogenetic study across the relevant kingdoms, including Charophyceae algae, the group of green algae giving rise to land plants. Surprisingly, we identified a subfamily of cytokinin receptors with members only from the early diverging land plants Marchantia polymorpha and Physcomitrella patens and then experimentally characterized two members of this subfamily. His phosphotransfer proteins of Charophyceae seemed to be more closely related to land plants than to other groups of green algae. Farther down the signaling pathway, the type-B RRs were found across all plant clades, but many members lack either the canonical Asp residue or the DNA binding domain. In contrast, the type-A RRs seemed to be limited to land plants. Finally, the analysis provided hints that one additional group of RRs, the type-C RRs, might be degenerated receptors and thus, of a different evolutionary origin than bona fide RRs.

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Section: A Subfamily Of Cytokinin Receptors Emergedmentioning

confidence: 99%

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confidence: 99%

A Subfamily of Putative Cytokinin Receptors Is Revealed by an Analysis of the Evolution of the Two-Component Signaling System of Plants

et al. 2014

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“…Initial evidence that this family functions in cytokinin perception came from the study of AHK4 transgenically expressed in bacteria and yeast, where it was shown that AHK4 could bind cytokinins and that ligand-binding stimulated the receptor's ability to signal through a phosphorelay (Inoue et al, 2001;Ueguchi et al, 2001;Yamada et al, 2001). All three receptors contain transmembrane domains, are thought to be localized to the plasma membrane, and contain a CHASE (cyclases/histidine kinases associated sensing extracellular) domain in their predicted extracellular portion that functions in cytokinin binding (Anantharaman and Aravind, 2001;Heyl et al, 2007). The isolation and characterization of T-DNA insertion mutations has demonstrated roles for the cytokinin receptors in diverse cytokinin-regulated processes including cell division, Histidine kinase domains are indicated by rectangles, receiver domains by ovals, HPt proteins by rounded rectangles, and transmembrane domains by black bars.…”

Section: Cytokinin Receptor Familymentioning

confidence: 99%

Two-Component Signaling Elements and Histidyl-Aspartyl Phosphorelays^†

Schäller

Kieber

Shiu

2008

The Arabidopsis Book

156

154

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Two-component systems are an evolutionarily ancient means for signal transduction. These systems are comprised of a number of distinct elements, namely histidine kinases, response regulators, and in the case of multi-step phosphorelays, histidine-containing phosphotransfer proteins (HPts). Arabidopsis makes use of a two-component signaling system to mediate the response to the plant hormone cytokinin. Two-component signaling elements have also been implicated in plant responses to ethylene, abiotic stresses, and red light, and in regulating various aspects of plant growth and development. Here we present an overview of the two-component signaling elements found in Arabidopsis, including functional and phylogenetic information on both bona-fide and divergent elements. (Makino et al., 2000;Schaller, 2000). Plants, like animals, contain pyruvate dehydrogenase kinase; this enzyme is related to histidine kinases but has an altered specificity such that it now phosphorylates serine residues (Popov et al., 1993). Thus, there is evidence from eukaryotes that two-component signaling elements have evolved to fill new functions that no longer rely upon phosphorylation of histidine and aspartic acid residues. HISTIDINE KINASESAnalysis of the Arabidopsis genome supports the existence of eight histidine kinases that contain all the conserved residues required for enzymatic activity (Table 1, Figures 2 and 3), as well as additional diverged histidine-kinase like proteins that lack residues essential to histidine kinase activity. Some of the functional histidine-kinases have been identified as receptors for the plant hormones cytokinin (AHK2, AHK3, and AHK4) and ethylene (ETR1 and ERS1), but the ligands for the other three bona-fide histidine kinases (AHK1, CKI1, and CKI2) have yet to be determined. Cytokinin Receptor FamilyThe cytokinin receptor family is composed of three histidine kinases: AHK2, AHK3, and AHK4 (also called WOL1 or CRE1). Initial evidence that this family functions in cytokinin perception came from the study of AHK4 transgenically expressed in bacteria and yeast, where it was shown that AHK4 could bind cytokinins and that ligand-binding stimulated the receptor's ability to signal through a phosphorelay (Inoue et al., 2001;Ueguchi et al., 2001;Yamada et al., 2001). All three receptors contain transmembrane domains, are thought to be localized to the plasma membrane, and contain a CHASE (cyclases/histidine kinases associated sensing extracellular) domain in their predicted extracellular portion that functions in cytokinin binding (Anantharaman and Aravind, 2001;Heyl et al., 2007). The isolation and characterization of T-DNA insertion mutations has demonstrated roles for the cytokinin receptors in diverse cytokinin-regulated processes including cell division, Histidine kinase domains are indicated by rectangles, receiver domains by ovals, HPt proteins by rounded rectangles, and transmembrane domains by black bars. Sites of phosphorylation upon histidine (H) and aspartic acid (D) residues are indicated. Terminol...

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“…There are three different receptor histidine kinases in the mustard Arabidopsis thaliana: AHK2, AHK3 and AHK4/CRE1 (Inoue et al, 2001;Nishumura et al, 2004;Suzuki et al, 2001;Yamada et al, 2001). Cytokinins bind to a conserved extracellular loop of about 200 amino acids found in each of these receptors, referred to as the CHASE domain (Anantharaman and Aravind, 2001;Heyl et al, 2007). Discadenine is a derivative of the cytokinin isopentenyl adenine, which is synthesized by condensation of isopentenylpyrophosphate and 5ЈAMP followed by removal of the ribose phosphate group (Abe et al, 1976;Taya et al, 1978).…”

Section: Introductionmentioning

confidence: 99%

Cytokinins induce sporulation inDictyostelium

Anjard

Loomis

2008

Development

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The social amoeba Dictyostelium discoideum diverged from the line leading to animals shortly after the separation of plants and animals but it retained characteristics of both kingdoms. A GABA B -like receptor and a peptide, SDF-2, with homologs found only in animals, control sporulation, while cytokinins, which act as hormones in plants, keep spores dormant. When SDF-2 binds its receptor DhkA, it reduces the activity of the cAMP phosphodiesterase RegA such that cAMP levels can increase. It has been proposed that the cytokinin discadenine also produces in an increase in cAMP but acts through a different histidine kinase, DhkB. We have found that discadenine and its precursor, isopentenyl adenine, not only maintain spore dormancy but also initiate rapid encapsulation independently of the SDF-2 signal transduction pathway. DhkB and the adenylyl cyclase of late development, AcrA, are members of two component signal transduction families and both are required to transduce the cytokinin signal. As expected, strains lacking the isopentenyl-transferase enzyme chiefly responsible for cytokinin synthesis are defective in sporulation. It appears that SDF-2 and cytokinins are secreted during late development to trigger signal transduction pathways that lead to an increase in the activity of the camp-dependent protein kinase, PKA, which triggers rapid encapsulation as well as ensuring spore dormancy.

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Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain

Cited by 66 publications

References 42 publications

A Subfamily of Putative Cytokinin Receptors Is Revealed by an Analysis of the Evolution of the Two-Component Signaling System of Plants

A Subfamily of Putative Cytokinin Receptors Is Revealed by an Analysis of the Evolution of the Two-Component Signaling System of Plants

Two-Component Signaling Elements and Histidyl-Aspartyl Phosphorelays^†

Cytokinins induce sporulation inDictyostelium

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Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain

Cited by 66 publications

References 42 publications

A Subfamily of Putative Cytokinin Receptors Is Revealed by an Analysis of the Evolution of the Two-Component Signaling System of Plants

A Subfamily of Putative Cytokinin Receptors Is Revealed by an Analysis of the Evolution of the Two-Component Signaling System of Plants

Two-Component Signaling Elements and Histidyl-Aspartyl Phosphorelays†

Cytokinins induce sporulation inDictyostelium

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Two-Component Signaling Elements and Histidyl-Aspartyl Phosphorelays^†