A modern circadian clock in the common angiosperm ancestor of monocots and eudicots
© McClung; licensee BioMed Central Ltd. 2010
Received: 14 April 2010
Accepted: 07 May 2010
Published: 7 May 2010
The circadian clock enhances fitness through temporal organization of plant gene expression, metabolism and physiology. Two recent studies, one in BMC Evolutionary Biology, demonstrate through phylogenetic analysis of the CCA1/LHY and TOC1/PRR gene families that the common ancestor of monocots and eudicots had components sufficient to construct a circadian clock consisting of multiple interlocked feedback loops.
See research article http://www.biomedcentral.com/1471-2148/10/126
The recent availability of several plant genome sequences has made it clear that whole genome duplication (polyploidization) has occurred frequently during angiosperm evolution. It is thought that the provision of duplicated genes permits evolution through functional specialization as well as the acquisition of innovative functions. There are several examples in which multiple members of gene families contribute to the circadian clock mechanism, raising a number of questions. Practically, functional redundancy among family members limits the identification of clock components through forward genetics . Of more general interest is the question of how these gene families have evolved among plants. In addition, there is considerable interest in determining the extent to which the clock model that has been developed for Arabidopsis will serve as a model for clock function among plants in general. A recent paper in BMC Evolutionary Biology describing the angiosperm PSEUDO-RESPONSE REGULATOR (PRR) gene family addresses each of these questions .
Circadian clocks: complex and highly conserved mechanisms for coordinating metabolism and physiology with the environment
A circadian rhythm is an endogenously generated rhythm with a period of about 24 h, approximating the period of the rotation of the earth on its axis. These rhythms provide temporal organization of biological processes from cyanobacteria to mammals . In plants, circadian rhythmicity is widespread and pervasive [4, 5]. Approximately one-third of the Arabidopsis transcriptome shows circadian oscillations in abundance in continuous conditions , but if one looks under a variety of light and temperature cycles that proportion grows to an astonishing ~90% , underlining the probable importance of circadian rhythm to overall fitness [4, 5].
The value of model organisms such as Arabidopsis stems from the generalization of knowledge acquired in the model to all flowering plants, and especially to those of agricultural significance. The increasing availability of genomic sequences from multiple plants is now permitting our first insights into this issue.
Phylogenetic analysis of the PRR and CCA1/LHYgene families shows that circadian clocks composed of multiple interlocked feedback loops evolved prior to the divergence of monocots and eudicots
Molecular phylogenetic analysis of the PRR genes indicates that the common ancestor of the monocots and eudicots had three PRR gene clades . Since the divergence of the monocots and eudicots, the clades corresponding to PRR3/PRR7 and PRR5/PRR9 have expanded independently in both lineages as a result of genome duplications . Within the eudicots, or 'true dicots', a subset of the former broad classification of dicots that includes more than half of extant plant species, two further genome duplications occurred in Arabidopsis following its divergence from papaya (Carica papaya) but, after each duplication, one of the paralogs was lost. In contrast, poplar has retained the duplicate copies of PRR5, PRR7 and PRR9, which originated in a genome duplication, termed the Salicoid duplication, that occurred in the poplar lineage after its separation from the papaya-Arabidopsis lineage. PRR3 has been completely lost from the poplar genome, although it is unclear whether this loss predated or followed the Salicoid duplication. The Brassica rapa genome has triploidized since its divergence form Arabidopsis approximately 14.5 million years ago, yet for no members of the B. rapa TOC1/PRR gene family have all three copies persisted, making it clear that differential PRR gene loss has occurred .
Takata et al.  have conducted a parallel analysis of angiosperm CCA1/LHY genes, and their observations are consistent with those obtained in their analysis of the PRR genes; the common ancestor of monocots and eudicots had one CCA1/LHY gene and there has been independent duplication of the LHY/CCA1 genes in the monocots and eudicots. Within the eudicots, there has been independent duplication in poplar and Arabidopsis.
The key conclusion from these studies is that the common ancestor of the monocots and eudicots had the basic components necessary for the construction of a circadian clock with multiple interlocked feedback loops prior to the separation of these groups 200 million years ago . This makes it very likely that the Arabidopsis clock will prove a useful model for most agricultural species. It will be interesting to determine whether the more basal angiosperms, such as the Magnoliales, also share this common clock architecture.
Sub- and neo-functionalization among clock genes
In Arabidopsis, the PRR3 gene offers an example of acquisition of a novel function. PRR9, PRR7, and PRR5 all have a similar role in negatively regulating CCA1 and LHY, suggesting that this represents the ancestral function (Figure 2). PRR3 appears, instead, to have acquired a novel and specialized function in the vascular tissue, where PRR3 binds to TOC1 and, in doing so, blocks the interaction of TOC1 with ZTL, the F-box protein that targets TOC1 for proteasomal degradation . Thus, PRR3 exhibits a restricted domain of expression and has acquired a novel function, the regulation of TOC1 stability through protein-protein interaction (Figure 2). In Arabidopsis, loss of PRR3 function confers only a very small shortening of circadian period , which is consistent with the apparent loss of PRR3 in poplar, without concomitant perturbation of clock function.
There are additional suggestions of evolving function in the PRR7 lineage. In Arabidopsis, PRR7 contributes to the determination of flowering time, although the effects are not large and PRR7 is not a major determinant of flowering time among natural populations . In contrast, in the monocots barley and wheat, PRR7 (Ppd-H1 and Ppd-D1, respectively) is one of the major determinants of photoperiod sensitivity and flowering time [15, 16]. Whether this represents a true acquisition of novel function in the monocots or a loss of function in the eudicots remains uncertain and will require more detailed dissection of the roles of PRR7 in the flowering pathways of monocots and eudicots.
There remains a great deal of work to achieve a mechanistic understanding of how the circadian clock keeps time. Four of the five PRR proteins are recruited to DNA yet they do not possess recognized DNA-binding domains and are not known to bind DNA directly. How are they recruited to the CCA1 and LHY promoters and what makes TOC1 a positive regulator while PRR5, PRR7, and PRR9 are repressors? Takata et al. [2, 9] establish that the common ancestor of monocots and eudicots had PRR and CCA1/LHY genes and, therefore, the materials with which to construct a functional circadian clock. How has the differential amplification of these two gene families in the angiosperm lineages allowed modulation of circadian timekeeping? How well does the outline presented in Figures 1 and 2 apply across the angiosperms and to more primitive plants? Within species, has variation among clock genes contributed to fitness? There is no shortage of questions and the increasing availability of genome sequences and tools to probe gene function in many species make this a wonderful time to study the basis of circadian timing.
Work in my laboratory on circadian rhythms is supported by grants from the National Science Foundation (IOS 0605736 and IOS 0960803) and Binational Science Foundation (2005223). I apologize to those authors whose work, due to space constraints, was not directly cited.
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