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.

Cytokinins - recent news and views of evolutionally old molecules

“…The algal biosynthetic pathway has not been confirmed yet, no CK-metabolic genes have been identified so far in algal genomes (Gu et al 2010), and only Type B response regulators (RRs) -but not the cytokinin receptor -have been found in the green unicellular microalgae Chlamydomonas reinhardtii (Pils and Heyl 2009). Two scenarios were suggested for the evolution of CK signalling in algae by Pils and Heyl (2009): (1) algae that were not confronted with the new stress conditions faced by the land conquesting plants and did not need more elaborate developmental programmes requiring a new or more complex regulation of CKs could have lost the CHASE domain His kinase fixed in the last common ancestor of amoebae and algae over time, or (2) CHASE domain His kinase exists in the charaphytes that are ancestral to land plants but the fact that their genome sequences have not been mapped yet has prevented the identification of CK receptors in these algae lineages.…”

“…However, neither appears to be a cytokinin receptor and CKs that are essential inducers of Dictyostelium sporulation act through another pathway that is as yet unknown (Anjard and Loomis 2008). No other gene with significant homology to the CK-sensing CHASE domain has been found anywhere apart from land plants, including in algal or cyanobacterial genomes, except for the genome of the virus Ectocarpus siliculosus virus 1 (Pils and Heyl 2009;Frébort et al 2011). This virus encoding a CHASE domain-containing histidine (His) kinase integrates itself into the genome of the brown algae Ectocarpus siliculosus (which produces CKs) and thus may have acted as a possible vector (Pils and Heyl 2009).…”

“…No other gene with significant homology to the CK-sensing CHASE domain has been found anywhere apart from land plants, including in algal or cyanobacterial genomes, except for the genome of the virus Ectocarpus siliculosus virus 1 (Pils and Heyl 2009;Frébort et al 2011). This virus encoding a CHASE domain-containing histidine (His) kinase integrates itself into the genome of the brown algae Ectocarpus siliculosus (which produces CKs) and thus may have acted as a possible vector (Pils and Heyl 2009). In mammals, two enzymes have been found to share sequence homology with the TCS His kinases (Tan et al 2002).…”

“…2a; Anantharaman et al 2007), (2) during evolution, the pathway was not acquired multiple times but was rather lost in animals (Pils and Heyl 2009). …”

“…TCS is shared among bacteria, plants and origin and paths of evolution of CK biosynthesis, degradation and signalling in the context of general evolutionary events (indicated by red arrows; the relative order is unknown). Phylogenetic trees were modified from Simpson (2006) and the CK evolution compiled from Pils and Heyl (2009) and Frébort et al (2011). Stars indicate secondary endosymbiosis.…”