Circadian clock
From Purdue Genomics Database Facility
baseltc4
Contents |
Circadian clock
Yoshikatsu Sato, Tadayoshi Hirai, and Tomoaki Nishiyama yoshi@nibb.ac.jp, tomoakin@kenroku.kanazawa-u.ac.jp
The circadian clock can be regarded as an internal processor of light signal that manage developmental activities at the right point in time (McClung, 2006). Most putative orthologues of the clock genes were present in all land plant lineages, suggesting a conserved molecular mechanism in land plants. As the components of the central oscillator, a pseudo response regulator, TOC1, and transcription factors with a single MYB-like domain, CCA1/LHY were generally characterized. A feedback loop by the reciprocal regulation between TOC1 and CCA1/LHY is accepted to be the basic framework for the clock mechanism in A.thaliana. Our analysis reveals that that does not hold true of all land plants, because potential orthologs of TOC1 were missing in P. patens, although CCA1/LHY were found in all land plant lineages. Furthermore, as a crucial event for the control of circadian period, it has been demonstrated that ZTL mediates the targeted degradation of TOC1 in light dependent manner. Excitingly, ZTL family genes (FKF1, LKP2 and ZTL) are also notable by absence in P. patens, C. reinhardtii., and C. merolae., while conserved in vascular plant lineage. These genes encode proteins that contain six kelch repeats, a LOV and an F-box domain. The unique combination of the three domains in the ZTL familly genes may be originated via an exon shuffling event in the common ancestor of vascular plant. Since TOC1 is required for the rapid increase in elongation coupled with âshade-avoidanceâ response that is an early sign of potential shading, the establishment of TOC1 and ZTL family genes in angiosperm may have adaptive significance in âshade-avoidanceâ response.
Todd Michael's Circadian Section
Todd P. Michael, Waksman Institute, Rutgers University, tmichael@waksman.rutgers.edu
Photosynthetic organisms have evolved circadian clocks to optimize their internal biology with that of the external daily light/dark cycles (Michael et al. 2003). As a result, in higher plants over 90% of the transcriptome is controlled by highly conserved time-of-day specific transcriptional networks (Michael et al. 2008). The evolution and origin of circadian timing is of particular interest.
GIGANTEA and TIME FOR COFFEE
To understand the Selaginella circadian clock, genetically defined circadian clock genes were identified using a best-blast strategy with a matrix of fully sequenced plant and algal genomes: Ostreococcus lumimarinas, Chlamydomonas reinhardtii, Physcomatrella patens, Carica papaya, Vitis vinifera, Populus trichocarpa, Oryza sativa and Arabidopsis thaliana. While most of the circadian genes were present across all lineages, two genes provided interesting information about the Selaginella circadian clock. First, like the higher plants Selaginella has one copy of GIGANTEA (GI), while Chlamydomonas, Physcomatrella and Ostreococcus do not. GI is a large, highly conserved protein that plays a central role in protein stability providing robust circadian cycling and day-length measurement required for flowering (Kim et al. 2007; Sawa et al. 2007). Second, the Selaginella genome lacks the recently defined TIME FOR COFFEE (TIK) gene that is important for both circadian stability and amplitude (Hall et al. 2003; Ding et al. 2007). The appearance of GI in the Selaginella lineage, and the subsequent appearance of TIK in higher plants, suggests the evolution of mechanisms to stabilize daily timing to make cycling robust.
Figure 1. Phylogenic relationship between GIGANTEA (GI) proteins from Populus trichocarpa (Pt), Arabidopsis thaliana (At), Oryza sativa (Os) and Selaginella moellendorffii (Sm). Pt contains two copies of GI (denoted by a capital A and B), consistent with its genome duplication. However, most plant species sequenced to date have one copy of GI. Two haplotypes were sequenced for Sm (denoted by lower case a and b).
PSEUDO RESPONSE REGULATORS
TIMING OF CAB 1 (TOC1), also known as PSEUDO RESPONSE REGULATOR 1 (PRR1), serves as the negative limb of the genetically defined feedback loop that drives daily timing of the A. thaliana circadian clock (McClung 2006). TOC1 is the founding member of a five gene family: PRR3, PRR5, PRR7 and PRR9. Mutations in TOC1 cause server circadian and flowering time defects in A. thaliana, whereas mutations in any of the other individual PRRs results in only modest defects (Michael et al., 2003). In addition, across species TOC1 is distinct from the other PRRs. PRR proteins can be traced back to marine algae O. lumimarinas and tauri, and are found in all subsequent lineages. In contrast, TOC1 is missing in P. patens, but present in Selaginella and C. reinhardtii, and only one copy is identified in P. trichocarpa.
Figure 2. Phylogenic relationship between TIMING OF CAB 1 (TOC1), also known as PSEUDO RESPONSE REGULATOR 1 (PRR1), proteins from Populus trichocarpa (Pt), Arabidopsis thaliana (At), Oryza sativa (Os), Chlamydomonas reinhardtii (Cr) and Selaginella moellendorffii (Sm). Two haplotypes were sequenced for Sm (denoted by lower case a and b).
The remaining PRRs can be placed in two additional groups that include PRR7/PRR3, and PRR5/PRR9 (Figure 3). Whereas both groups are represented in the higher plants such as Arabidopsis, poplar and rice, both moss and Selaginella contain only orthologs to the PRR7/PRR3 group. Genetic evidence support overlapping and distinct roles for AtPRR7 and AtPRR9 in a morning specific oscillator and light signaling, suggesting that the two groups represent a gene duplication leading to speciality. Therefore, either moss and Selaginella didn’t duplicate this gene family or they have lost one group. The presence of a PRR9 ortholog in Chlamydomonas and Volvox and the PRR5 in Ostreococcus argues against the later hypothesis (Figure 4), and is consistent with the loss of one group in moss and Selaginella or separate green lineages.
Figure 3. Phylogenic relationship PSEUDO RESPONSE REGULATOR proteins from Populus trichocarpa (Pt), Arabidopsis thaliana (At), Oryza sativa (Os), and Selaginella moellendorffii (Sm).
Both Selaginella PRRs are orthologous to PRR7. Since in Arabidopsis PRR7 and PRR3 transcripts are expressed at different times of day, early in the day and evening respectively, we asked if SmPRR7A could be distinguished from SmPRR7B based on characterized cis-acting elements in their respective promoters (500 bp upstream of start). In Arabidopsis, multiple circadian response elements that confer time-of-day transcription have been characterized: the evening element (EE) confers evening-specific expression and the morning element (ME) confers morning-specific expression (Michael et al., 2008). Consistent with SmPRR7A functioning like AtPRR3, there are 2 ME and 3 EE, while SmPRR7B is consistent with AtPRR7 with 5 ME and 1 EE. These results suggest that while SmPRR7 has not significantly diverged at the protein level, the regulatory sequence has evolved to the new functionality seen in higher plants.
Figure 4. Evolution of the PSEUDO RESPONSE REGULATOR (PRR) Proteins.
CONCLUSIONS
The Selaginella circadian clock provides new opportunities to understand the early events in the evolution of the daily timing. In the Selaginella lineage, there is the emergence of GI, while some genes such as TIK are missing. In addition, we were able to observe the early stages of diversification of the regulatory mechanisms of the PRR gene family in Selaginella. Together, these results suggest that Selaginella represents a key evolutionary step in refining the process of daily timing to that found in higher plants, and provides clues as to the origin of gene families like the PRRs.
References
Ding Z, Millar AJ, Davis AM, Davis SJ (2007) TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell 19(5): 1522-1536.
Farré EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr Biol. 2005 15(1): 47-54.
Hall A, Bastow RM, Davis SJ, Hanano S, McWatters HG et al. (2003) The TIME FOR COFFEE gene maintains the amplitude and timing of Arabidopsis circadian clocks. Plant Cell 15(11): 2719-2729.
Kim W-Y, Fujiwara S, Suh S-S, Kim J, Kim Y et al. (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449(7160): 356.
McClung, C.R. (2006). Plant circadian rhythms. Plant Cell 18, 792-803.
Michael T, Mockler T, Breton G, McEntee C, Byer A et al. (2008) Network discovery pipeline elucidates conserved time of day specific cis-regulatory modules. PLoS Genetics 4(2): e14.
Michael TP, Salome PA, Yu HJ, Spencer TR, Sharp EL et al. (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302(5647): 1049-1053.
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science: 1146994.
Table of gene numbers
| Gene functions | Gene | Gene used as a query | The number of putative orthologs | |||
|---|---|---|---|---|---|---|
| Arabidopsis thaliana | Oryza sativa | Selaginalla moellendorffii (a) | Physcomitrella patens | |||
| Circadian clock | LOV KELCH PROTEIN 2 (LKP2), FLAVIN-BINDING KELCH DOMAIN FBOX PROTEIN (FKF1), ZEITLUPE (ZTL) | LKP2 | 3 | 2 | 1 (2) | 0 |
| Circadian clock | PSEUDO-RESPONSE REGULATOR 3,5,7 AND 9 2) | PRR7 | 5 | 2 | 3 (6) | 4 |
| Circadian clock | TIMING OF CAB 1 | TOC1 | 1 | 1 | 1 (2) | 0 |
| Circadian clock | CIRCADIAN CLOCK ASSOCIATED 1/LATE ELONAGTED HYPOCOTYL | LHY | 9 | 4 | 2 (3) | 2 |
| Circadian clock | CONSTANS LIKE 3 | CO | 18 | 17 | 3 (5) | 6 |
| Circadian clock | GIGANTEA | GI | 1 | 1 | 1 (2) | 0 |
| Circadian clock | EARLY FLOWERING 3 3) | ELF3 | 2 | 2 | 2 (4) | 4 |
| Circadian clock | EARLY FLOWERING 4 | ELF4 | 5 | 4 | 2 (3) | 1 |
| Circadian clock | SENSITIVITY TO RED LIGHT REDUCED 1 | SRR1 | 1 | 2 | 1 (2) | 2 |
| Circadian clock | LUX ARRYTHMO/PHYTOCLOCK 1 | PCL1 | 5 | 1 | 1 (2) | 3 |
| Circadian clock | CASEIN KINASE BETA 3 | CKB3 | 4 | 3 | 1 (2) | 4 |
| Circadian clock | TIME FOR COFFEE | TIK | 2 | NA | 0 | 0 |
| Circadian clock | TEJ | TEJ | 1 | NA | 1 | NA |
| Circadian clock | LIGHT INSENSITIVE PERIOD 1 | LIP1 | 1 | NA | NA | NA |
footnote: The number of putative orthologs here refers to number of genes that is included in a clade that corresponds to all genes derived from a single gene in the last common ancestor of P. patens, S. moellendrffii, A. thaliana, and O. sativa based on phylogenetic analyses. The alignments and trees are available through http://moss.nibb.ac.jp/treedb/ (a) number of putative loci at first and number of putative alleles detected in parentheses. That is, 1 (2), indicates we found two sequences that likely represent two alleles of one locus.
