Unraveling the evolution of cytokinin signaling

Abstract

The conquest of the land by plants required dramatic morphological and metabolic adaptations. Complex developmental programs under tight regulation evolved during this process. Key regulators of plant development are phytohormones, such as cytokinins. Cytokinins are adenine derivatives that affect various processes in plants. The cytokinin signal transduction system, which is mediated via a multistep variant of the bacterial two-component signaling system, is well characterized in the model plant Arabidopsis (Arabidopsis thaliana). To understand the origin and evolutionary pattern of this signaling pathway, we surveyed the genomes of several sequenced key plant species ranging from unicellular algae, moss, and lycophytes, to higher land plants, including Arabidopsis and rice (Oryza sativa), for proteins involved in cytokinin signal transduction. Phylogenetic analysis revealed that the hormone-binding receptor and a class of negative regulators first appeared in land plants. Other components of the signaling pathway were present in all species investigated. Furthermore, we found that the receptors evolved under different evolutionary constraints from the other components of the pathway: The number of receptors remained fairly constant, while the other protein families expanded.

Figure 1.

Phylogenetic tree of CHASE domains in plants. Proteins containing a CHASE domain were identified by a HMM search. A phylogenetic tree of CHASE domains of those proteins was generated using the PHYML program. [See online article for color version of this figure.]

Figure 2.

Phylogenetic tree of HPt domains in plants. Proteins containing a HPt domain were identified by a HMM search. Proteins containing additional domains were eliminated from the analysis. A phylogenetic tree of HPt domains was generated using the PHYML program. [See online article for color version of this figure.]

Figure 3.

Phylogenetic tree of all RR domains. Proteins containing a RR domain were identified by a HMM search. Proteins containing additional domains other than a Myb domain were eliminated from the analysis. A phylogenetic tree of RR domains was generated using the MrBayes program. The clade of the type-A RRs is highlighted in green and the clade of the type-B RRs is highlighted in yellow.

Figure 4.

Phylogenetic tree of type-B RRs. Using the type-B RRs identified (Fig. 3), a tree was generated using the PHYML program. It was based on a full-length sequence alignment of type-B RRs, optimized with the Gblocks program. The type-C RR ARR22 from Arabidopsis was used as outgroup. [See online article for color version of this figure.]

Figure 5.

Phylogenetic tree of type-A RRs. Using the type-A RRs identified (Fig. 3), a tree was generated using the PHYML program. The tree was based on the RR domain sequences only. The type-C RR ARR22 from Arabidopsis was used as an outgroup. [See online article for color version of this figure.]

Figure 6.

Phylogenetic tree of type-C RRs. Using the type-C RRs identified (Fig. 3), a tree was generated using the PHYML program. The tree was based on the RR domain sequences only. [See online article for color version of this figure.]

Figure 7.

Model of the evolution of the cytokinin signaling pathway.