Abstract
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.
Highlights
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
In the first step of our analysis, we focused on the evolution of the cyclase/His kinase-associated sensory extracellular (CHASE) domains
The observed domain architecture was different between the three clades, with the two land plant branches showing the conserved domain pattern of cytokinin receptors (CHASE, Histidine Kinase A domain [HisK]; Histidine kinase, DNA gyrase B, and HSP90-like ATPase domain [HATPase], and RR domains; Fig. 1B)
Summary
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. The analysis provided hints that one additional group of RRs, the type-C RRs, might be degenerated receptors and of a different evolutionary origin than bona fide RRs. Starting out as unicellular algae, plants have undergone many dramatic changes, enabling them to make major modifications in lifestyle, such as the transition from a single cell to multicellularity or from an aquatic to a terrestrial habitat (Rensing et al, 2008; Prochnik et al, 2010; Cock and Coelho, 2011). The ability of plants to use cytokinin as a phytohormone represents an evolutionary novelty (Gruhn and Heyl, 2013), which raises the questions of how a group of ubiquitous adenine derivatives became regulated signaling molecules and how the required regulatory system, known from modern land plants, evolved We addressed these questions by analyzing the evolution of the key players constituting the cytokinin signaling pathway using the genomes and/or EST collections of key species of bacteria, unicellular eukaryotes, algae, and land plants. These and other findings indicate a much greater level of complexity for the evolution of cytokinin signaling than previously anticipated (Pils and Heyl, 2009)
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