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

Abstract

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...

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

“…This tree showed that the RR domains of the RRCs are more closely related to RR domains of His kinases from plants than the RRAs or RRBs. This finding is in accordance with previous analyses (Kiba et al, 2004;Schaller et al, 2008). Another hint that this class of RRs might be, in fact, degenerated receptors rather than bona fide RRs comes from the presence of an HATPase domain in two members of this clade (Fig.…”

Analysis of Cytokinin Mutants and Regulation of Cytokinin Metabolic Genes Reveals Important Regulatory Roles of Cytokinins in Drought, Salt and Abscisic Acid Responses, and Abscisic Acid Biosynthesis

“…Phosphorylation, which is catalyzed by protein kinases, is one of the key mechanisms for intracellular signal transduction in both eukaryotic and prokaryotic cells. Typically, His kinases sense extracellular stimuli by autophosphorylation and transfer a phosphoryl group to the response regulator, resulting in the activation of downstream proteins that elicit a specific response (Mizuno, 2005;Schaller et al, 2008).…”

Role of the Putative Osmosensor Arabidopsis Histidine Kinase1 in Dehydration Avoidance and Low-Water-Potential Response

“…Five of these encode ethylene receptors, while the remaining six (AHK1, AHK2, AHK3, CRE1/AHK4, CKI1, and CKI2/AHK5) encode nonethylene receptor kinases. AHK2, AHK3, and CRE1 are cytokinin receptors and mediate cytokinin signaling via interaction with downstream Arabidopsis His phosphotransfer proteins and Arabidopsis response regulators (Schaller et al, 2008;To and Kieber, 2008;Perilli et al, 2010). AHK1 is not a cytokinin receptor, and the signal or ligand that activates AHK1 is not known.…”