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Dahlem Research School

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Home Page » Research groups » Heyl » Evolution of the two-component system

Research group Heyl

Evolution of the cytokinin regulatory system — or how to turn a class of ubiquitous adenine derivatives into a specific hormone

Evolutionary novelties can arise either through co-opting an existing component to a new task or through the de novo generation of a new gene/genes. In my lab we investigate how members of a group of adenine derivatives present in all organisms evolved into a plant hormone, cytokinin, with specific functions. The cytokinin signal transduction system is similar to the His-to-Asp multi-step phosphor-relay system found in bacteria. In order to understand the origin and the evolutionary trends of this signaling pathway, we surveyed the genomes/EST data of over 40 species ranging from bacteria to modern land plants for genes involved in cytokinin signal transduction. Phylogenetic analysis revealed a novel subfamily of cytokinin receptors found only in the moss Physcomitrella patens and in Marchantia polymorpha (Figure 3). Subsequent wet-lab experiments confirmed their functionality (Gruhn et al., 2014).

Phylogenetic tree of CHASE domain containing histidine kinases
Figure 3. Phylogenetic tree of CHASE domain containing histidine kinases reveals a new subfamily of plant cytokinin receptors. (A) The Cyclase/ Histidine kinase Associated Sensory Extracellular (CHASE) domain sequences from all organisms under investigation were aligned and a phylogenetic tree using a Maximum Likelihood and Bayesian methods were inferred (for details see material and methods section). Since tree topology was identical with both methods, bootstrap values and posterior probabilities are depicted on the Maximum Likelihood tree. The newly identified subfamily of plant cytokinin receptors is indicated with red lines and the clade with classical cytokinin receptors is marked by blue lines. EST evidence is symbolized by a filled circle and the lack of EST evidence by an open circle. (B) Left: Maximum likelihood tree of the CHASE domain, Middle: Conservation of amino acids important for structure and function of the CHASE domain (Hothorn et al., 2011). The highlighted positions (A-Y) are in respect to the CHASE domain of AHK4 (For details see Gruhn et al., 2014). Dark blue shows identity to AHK4, light blue marks conservative substitution, white boxes symbolizes no conservation related to the respective position in the CHASE sequence of AHK4. Right: Domain architecture of the whole protein. For details see the materials and methods section.

The analysis revealed furthermore the first evidence for cytokinin receptors in Charophyte algae. Further down the signaling pathway, the type-B RRs were found across all plant clades - including the chlorophyte algae, but surprisingly many members lack either the canonical Asp residue or the DNA-binding domain. In contrast, the type-A RRs appear to be strictly 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 evolutionarily of a different origin than bona fide response regulators (Gruhn et al, 2014). These and other data led to a model for the evolution of the cytokinin signaling, in which almost all of the domains necessary are present in cyanobacteria and were transferred during the endosymbiosis to the plant lineage. During the evolution of the Streptophytes, the domains were arranged in such as fashion as to allow the formation of the cytokinin signaling pahtway as we know it from modern land plants (Figure 4).

In addition the Heyl group has been leading the collaborative effort of finding a common nomenclature for cytokinin signaling (Heyl et al, 2013) and participated in the annotation of genomes, such as Physcomitrella patens (Rensing et al, 2008) and Sellaginella moellendorfii (Banks et al, 2011).

Phylogenetic tree of CHASE domain containing histidine kinases
Figure 4: Model for the evolution of the cytokinin regulatory system. (a) Current model of the cytokinin signaling pathway and key enzymes of its metabolism in angiosperms; (b) model for the origin and evolution of the cytokinin regulatory system. The genes necessary for this system were introduced into plantsvia the primary endosymbiosis. Subsequent sub-functionalization and neo-functionalization of duplicated genes led to the cytokinin circuitry found inmodern plants. The model is based on data from Gruhn et al., 2014. The different domains shown are labeled according to the Pfamdatabase ( RR = response regulator receiver domain (PF00072); Myb-related DNA-binding domain (PF00249);HK = histidine kinase, composed of the histidine kinase A domain (PF00512) and the Histidine kinase-ATPase domain (PF02518); HPT = histidinephosphotransfer protein, contains the Hpt domain (PF01627); CHASE = cyclase histidine kinase associated sensory extracellular (PF03924);IPT = isopentenyl transferase; cytokinin oxidase (PF09265). Circles and question marks indicate uncertainty about the presence of the respectiveprotein, which is due to the lack of sequenced genomes from Charophytes. white boxes symbolizes no conservation related to the respective position in the CHASE sequence of AHK4. Right: Domain architecture of the whole protein. For details see the materials and methods section.


New publication

An article about the analysis of a cytokinin-responsive gene of Arabidopsis thaliana encoding a novel F-box protein regulating sterol biosynthesis has been published in Journal of Experimental Botany.
May 2017

New publication

A report about constitutively active mutants of the cytokinin receptors AHK2 und AHK3 and their impact on organ size, flowering time, and plant longevity has been published in Plant Physiology.
March 2017

New publication

An article about the role of the transcription factor ERF105 in freezing tolerance and cold acclimation has been published in Plant Cell and Environment.
January 2017

Krolow Award 2016

The Krolow Award 2016 was given to Dr. Anne Cortleven for her work about the role of Cytokinin in the plant response to high light stress.
November 2016
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Updated: 2017-04-23