Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock

Anwer, Muhammad; Boikoglou, Eleni; Herrero, Eva; Hallstein, Marc; Davis, Amanda M; James, Geo Velikkakam; Nagy, Ferenc; Davis, Seth J

doi:10.7554/elife.02206

Cited by 76 publications

(93 citation statements)

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“…The functional relevance of these domains remain largely unknown, but recent evidence suggests that block II is required for interaction with the ELF4 protein (Herrero et al, 2012;Saini et al, 2013), and mutations within block II have been shown to alter ELF3 function and cellular distribution (Anwer et al, 2014;Kolmos et al, 2011). We also assembled a more extensive collection of legume ELF3 sequences and examined the resulting alignment (Supplemental Fig.…”

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confidence: 99%

“…While the overall architecture of the clock is complex and the details are still a matter of debate (Nagel and Kay, 2012;McClung, 2014), one group of genes has emerged as being particularly significant for clock entrainment and photoperiodism. The myb transcription factor gene LUX ARRHYTHMO (LUX; also known as PHYTOCLOCK1) and two other plant-specific genes EARLY FLOWERING3 (ELF3) and ELF4 have similar mutant phenotypes, exemplified by early, photoperiod-insensitive flowering, elongated hypocotyls, and loss of circadian rhythmicity under constant conditions Doyle et al, 2002;Hazen et al, 2005;Onai and Ishiura, 2005;Anwer et al, 2014). The proteins encoded by these genes form a complex termed the evening complex (EC), in which the ELF3 protein is suggested to act as a molecular scaffold and signaling hub, connecting ELF4 with LUX ).…”

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EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

et al. 2017

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Three pea (Pisum sativum) loci controlling photoperiod sensitivity, HIGH RESPONSE (HR), DIE NEUTRALIS (DNE), and STERILE NODES (SN), have recently been shown to correspond to orthologs of Arabidopsis (Arabidopsis thaliana) circadian clock genes EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHMO, respectively. A fourth pea locus, PHOTOPERIOD (PPD), also contributes to the photoperiod response in a similar manner to SN and DNE, and recessive ppd mutants on a springflowering hr mutant background show early, photoperiod-insensitive flowering. However, the molecular identity of PPD has so far remained elusive. Here, we show that the PPD locus also has a role in maintenance of diurnal and circadian gene expression rhythms and identify PPD as an ELF3 co-ortholog, termed ELF3b. Genetic interactions between pea ELF3 genes suggest that loss of PPD function does not affect flowering time in the presence of functional HR, whereas PPD can compensate only partially for the lack of HR. These results provide an illustration of how gene duplication and divergence can generate potential for the emergence of more subtle variations in phenotype that may be adaptively significant.

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confidence: 99%

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EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

et al. 2017

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“…Plant circadian clocks comprise multiple interlocked feedback loops (7)(8)(9). There is natural variation in clock function in both weedy and cultivated species (10)(11)(12)(13)(14)(15), although few of the genes responsible for these quantitative trait loci (QTL) have been identified. We identified QTL for circadian period in a population of Recombinant Inbred Lines (RIL) of Brassica rapa (14).…”

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Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa

Xie

Lou

Hermand

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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GIGANTEA (GI) was originally identified by a late-flowering mutant in Arabidopsis, but subsequently has been shown to act in circadian period determination, light inhibition of hypocotyl elongation, and responses to multiple abiotic stresses, including tolerance to high salt and cold (freezing) temperature. Genetic mapping and analysis of families of heterogeneous inbred lines showed that natural variation in GI is responsible for a major quantitative trait locus in circadian period in Brassica rapa. We confirmed this conclusion by transgenic rescue of an Arabidopsis gi-201 loss of function mutant. The two B. rapa GI alleles each fully rescued the delayed flowering of Arabidopsis gi-201 but showed differential rescue of perturbations in red light inhibition of hypocotyl elongation and altered cold and salt tolerance. The B. rapa R500 GI allele, which failed to rescue the hypocotyl and abiotic stress phenotypes, disrupted circadian period determination in Arabidopsis. Analysis of chimeric B. rapa GI alleles identified the causal nucleotide polymorphism, which results in an amino acid substitution (S264A) between the two GI proteins. This polymorphism underlies variation in circadian period, cold and salt tolerance, and red light inhibition of hypocotyl elongation. Loss-of-function mutations of B. rapa GI confer delayed flowering, perturbed circadian rhythms in leaf movement, and increased freezing and increased salt tolerance, consistent with effects of similar mutations in Arabidopsis. Collectively, these data suggest that allelic variation of GI-and possibly of clock genes in general-offers an attractive target for molecular breeding for enhanced stress tolerance and potentially for improved crop yield.abiotic stress tolerance | circadian clock | hypocotyl elongation | flowering time | natural variation T he last half-century has seen dramatic increases in agricultural productivity. Despite the approximate doubling in world population since 1964, the proportion with insufficient food has dropped by ∼75%, although ∼1 billion remain underfed, and twice that many suffer from micronutrient deficiencies (1). Predicted growth in population and in per capita consumption will require an estimated doubling of crop production by 2050 (2). However, yield trends for maize, rice, wheat, and soybean-four major crops that currently produce nearly two-thirds of global agricultural calories-are insufficient to achieve this doubling (3). Therefore, there is a pressing need not simply to sustain, but actually to accelerate yield improvement.One strategy to increase yield is to identify genetic variation in plant regulatory networks that limit yield to define targets for programs of marker-assisted (molecular) breeding. The circadian clock has been implicated as a target for increasing yield (4-6). Plant circadian clocks comprise multiple interlocked feedback loops (7-9). There is natural variation in clock function in both weedy and cultivated species (10-15), although few of the genes responsible for these quantitative trait loc...

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“…The latter point is of particular relevance because natural variation in rhythms has mainly been studied in artificial continuous conditions that are used to determine certain circadian parameters. Natural variation of period length, defined as the length of the circadian cycle, was quantified in constant environmental conditions by measuring rhythms of leaf movements or oscillations of gene expression (4,(18)(19)(20)(21). Phase, or the time at which an event occurs within a cycle, also varies extensively when determined in constant conditions (4,22).…”

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Natural diversity in daily rhythms of gene expression contributes to phenotypic variation

Montaigu

Giakountis

Rubin

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Daily rhythms of gene expression provide a benefit to most organisms by ensuring that biological processes are activated at the optimal time of day. Although temporal patterns of expression control plant traits of agricultural importance, how natural genetic variation modifies these patterns during the day and how precisely these patterns influence phenotypes is poorly understood. The circadian clock regulates the timing of gene expression, and natural variation in circadian rhythms has been described, but circadian rhythms are measured in artificial continuous conditions that do not reflect the complexity of biologically relevant day/ night cycles. By studying transcriptional rhythms of the eveningexpressed gene GIGANTEA (GI) at high temporal resolution and during day/night cycles, we show that natural variation in the timing of GI expression occurs mostly under long days in 77 Arabidopsis accessions. This variation is explained by natural alleles that alter light sensitivity of GI, specifically in the evening, and that act at least partly independent of circadian rhythms. Natural alleles induce precise changes in the temporal waveform of GI expression, and these changes have detectable effects on PHYTOCHROME INTERACTING FACTOR 4 expression and growth. Our findings provide a paradigm for how natural alleles act within day/night cycles to precisely modify temporal gene expression waveforms and cause phenotypic diversity. Such alleles could confer an advantage by adjusting the activity of temporally regulated processes without severely disrupting the circadian system. diurnal | circadian | rhythms | Arabidopsis | GIGANTEA

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Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock

Cited by 76 publications

References 70 publications

EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa

Natural diversity in daily rhythms of gene expression contributes to phenotypic variation

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