Evolutionary relationships among barley and Arabidopsis core circadian clock and clock-associated genes

Abstract

The circadian clock regulates a multitude of plant developmental and metabolic processes. In crop species, it contributes significantly to plant performance and productivity and to the adaptation and geographical range over which crops can be grown. To understand the clock in barley and how it relates to the components in the Arabidopsis thaliana clock, we have performed a systematic analysis of core circadian clock and clock-associated genes in barley, Arabidopsis and another eight species including tomato, potato, a range of monocotyledonous species and the moss, Physcomitrella patens. We have identified orthologues and paralogues of Arabidopsis genes which are conserved in all species, monocot/dicot differences, species-specific differences and variation in gene copy number (e.g. gene duplications among the various species). We propose that the common ancestor of barley and Arabidopsis had two-thirds of the key clock components identified in Arabidopsis prior to the separation of the monocot/dicot groups. After this separation, multiple independent gene duplication events took place in both monocot and dicot ancestors.

Fig. 1

Feedback loops of the Arabidopsis clock. Simplified schematic diagram of the 24-h Arabidopsis clock. Feedback loops of the core clock genes are represented in the centre. Full lines represent transcriptional feedback loops, whereas dashed lines represent post-translational regulation. Arrows represent activation, while arrows with blunt ends represent repression. The diagram represents a compilation of gene regulation from numerous publications referred to in the “Introduction”. For simplicity, the PRR3 component was not included in the above regulatory network. Expression peaks of clock genes are represented at different times of the day and night in the outer circle (Nakamichi 2011)

Fig. 2

Robust analysis in the identification of clock orthologues. Cross-species reciprocal BLAST diagram of a LUX, b LHY and c ELF4 genes. Arrows indicate direction of BLAST analysis, i.e. a sequence from one database was used to identify orthologous sequences in the database of another species

Fig. 3

Genomic structure of a TOC1 (PRR1) and b LHY and CCA1 in Arabidopsis (At) and barley (Hv). Exons are numbered; 5′ and 3′ UTRs are open boxes; coding sequences are dark boxes, except domain-encoding exons. There may be further 5′ UTR sequence upstream of the HvLHY exon 1 designated in the Figure (dotted line) which has not yet been fully sequenced

Fig. 4

a Phylogenetic tree of ZTL and FKF1 genes. Due to the lack of complete sequence information for the TaZTLb gene, the partial wheat ZTLb CDS from PUT43520 was used to represent wheat. Since P. patens does not contain a true orthologue of ZTL or FKF1, the root was placed on the FKF1 family branch. b Phylogenetic trees of the ELF4-like family. Due to the lack of complete CDS data for the TaELF4-like3, the partially related cDNA from PUT145474 was used to represent this wheat branch. In constructing the trees, all gaps and missing data were eliminated from sequence alignments. Genes that do not follow expected topology are shown in grey. Evolutionary distances are presented in number of base substitutions per site. Barley genes are highlighted with a box

Fig. 5

Schematic diagram of the proposed evolutionary history of circadian clock components of barley, Arabidopsis and their putative common ancestor. Independent duplication events are represented by fine diagonal lines. The diagram at the bottom right is related to the main diagram and it refers to the numbers of genes from each group