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.

Figure 1.

Histidyl-Aspartyl Phosphorelay. 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. Terminology is based on that of Parkinson (1993). (A) Simple two-component system that employs a histidine kinase and a response regulator. (B) Multi-step phosphorelay that employs a hybrid histidine kinase with both histidine kinase and receiver domains, a histidine-containing phosphotransfer protein (HPt), and a response regulator.

Figure 2.

Representative Domain Structures of Arabidopsis Two-Component Signaling Elements. Histidine kinase domains are indicated by rectangles, receiver domains by ovals, HPt proteins by rounded rectangles, and transmembrane domains by black bars. Additional domains are as indicated and are described in the text. (A) Bona-fide signaling elements likely to participate in phosphorelays. Sites of phosphorylation upon histidine (H) and aspartic acid (D) residues are indicated. (B) Divergent signaling elements from Arabidopsis that lack residues normally associated with participation in a two-component phosphorelay. An X in a histidine-kinase-like domain indicates that it lacks multiple residues implicated in histidine kinase activity. The divergent HPt (APHP1) contains an Asn (N) substitution for the His that normally gets phosphorylated. The divergent response regulators typically contain a Glu (E) substitution for the Asp that normally gets phosphorylated.

Figure 3.

Phylogenetic Relationship of Histidine Kinases. Sequences containing conserved histidine-kinase domains (open circles) and diverged histidine kinase domains (filled squares) were identified in Arabidopsis. An unrooted bootstrapped tree is shown based on amino-acid alignment of the histidine-kinase domain sequences. The histidine kinase domain was defined as the sequence extending from the phospho-acceptor domain through the ATPase domain.

Figure 4.

Phylogenetic Relationship of HPt Proteins. An unrooted bootstrapped tree is shown based on amino-acid alignment of HPt domain sequences.

Figure 5.

Phylogenetic Relationship of Receiver Domains from Response Regulators and Hybrid Kinases. An unrooted bootstrapped tree is shown based on amino-acid alignment of receiver and pseudoreceiver domain sequences. The different families of receiver domains are highlighted, with subfamilies 1, 2 and 3 being indicated for the type-B ARRs. Note that the tree has some low bootstrap values indicating that regions of this tree should be considered to be simply radiations.

Figure 6.

Cytokinin Signal Transduction Occurs Through a Multi-Step Phosphorelay. Cytokinin receptors, AHPs, and type-B ARRs function as a positive regulatory circuit to relay the cytokinin signal from plasma membrane to nucleus. Type-B ARRs act as transcription factors, one target being genes encoding type-A ARRs. The type-A ARRs feed back to inhibit their own transcription and may also mediate other cytokinin responses. The roles of the listed cytokinin receptors, AHPs, type-B response regulators, and type-A response regulators in cytokinin signal transduction have each been confirmed by the analysis of T-DNA insertion mutations.