Tissue-specific clocks in Arabidopsis show asymmetric coupling

Endo, Motomu; Shimizu, Hiroki; Nohales, María A.; Araki, Takashi; Kay, Steve A.

doi:10.1038/nature13919

Cited by 262 publications

(332 citation statements)

References 36 publications

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“…These results clearly indicate that P. hybrida plants likely possess circadian clocks that have different properties in flowers and leaves. Although tissue specificity of the circadian clock has been shown in Arabidopsis previously (33)(34)(35), current examples in other plant species are still limited (36). Of note is the fact that the common study organism for FVBP research, P. hybrida, is a hybrid of Petunia axillaris and Petunia integrifolia.…”

Section: Discussionmentioning

confidence: 99%

Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia

Fenske

Hazelton

Hempton

et al. 2015

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

104

118

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Flowers present a complex display of signals to attract pollinators, including the emission of floral volatiles. Volatile emission is highly regulated, and many species restrict emissions to specific times of the day. This rhythmic emission of scent is regulated by the circadian clock; however, the mechanisms have remained unknown. In Petunia hybrida, volatile emissions are dominated by products of the floral volatile benzenoid/phenylpropanoid (FVBP) metabolic pathway. Here we demonstrate that the circadian clock gene P. hybrida LATE ELONGATED HYPOCOTYL (LHY; PhLHY) regulates the daily expression patterns of the FVBP pathway genes and floral volatile production. PhLHY expression peaks in the morning, antiphasic to the expression of P. hybrida GIGANTEA (PhGI), the master scent regulator ODORANT1 (ODO1), and many other evening-expressed FVBP genes. Overexpression phenotypes of PhLHY in Arabidopsis caused an arrhythmic clock phenotype, which resembles those of LHY overexpressors. In Petunia, constitutive expression of PhLHY depressed the expression levels of PhGI, ODO1, evening-expressed FVBP pathway genes, and FVBP emission in flowers. Additionally, in the Petunia lines in which PhLHY expression was reduced, the timing of peak expression of PhGI, ODO1, and the FVBP pathway genes advanced to the morning. Moreover, PhLHY protein binds to cis-regulatory elements called evening elements that exist in promoters of ODO1 and other FVBP genes. Thus, our results imply that PhLHY directly sets the timing of floral volatile emission by restricting the expression of ODO1 and other FVBP genes to the evening in Petunia.circadian rhythm | floral volatile | benzenoids | Petunia hybrida | LHY P lant development and physiology are extensively influenced by the circadian clock (1). The precise timing of a single plant behavioral output often requires a suite of internal mechanisms to occur in coincidence or in quick succession before the behavior taking place. Transcriptome analysis revealed that the circadian clock controls transcription of one third of genes in Arabidopsis (2). In this way, the clock can exert a holistic effect on a complex mechanism at a precise moment in time. The effectiveness of the clock's ability to coordinate complex behaviors has been used by many aspects of plant physiology, such as photosynthesis, stem and leaf growth, and flowering (3, 4).The precise timing of sexual reproductive events is critical, as plants are sessile and individuals are often spread over large distances. In addition to regulating the timing of flower formation, when they have opened, many flowers emit floral scents to lure pollinators. Attractive floral volatiles are often emitted in a rhythmic fashion, with peaks of emission coinciding with the primary pollinator's period of activity (5). Although studies have shown that rhythmic emission of scent requires the influence of a circadian clock (6-8), no study of which we are aware has shown a mechanistic link between clock function and floral volatile production.Research on floral vol...

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Section: Discussionmentioning

confidence: 99%

Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia

Fenske

Hazelton

Hempton

et al. 2015

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

104

118

View full text Add to dashboard Cite

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“…S6), suggesting that their difference in function could reflect an inherent difference in the activity of the two proteins. Alternatively, it is also possible that these broad expression patterns in whole leaves may not accurately reflect localized differences in expression in specific leaf tissues critical for their influence on flowering, as recently observed for a number of evening genes in the Arabidopsis clock (Endo et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

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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“…Given that there are EE (AAAATATCT) and EE-like elements (AATATCT) in the COR27 promoter region (Mikkelsen and Thomashow, 2009) and that it was reported that the promoter of COR27 was occupied by CCA1 in a ChIP-seq analysis of plants expressing CCA1-GFP (Nagel et al, 2015), we measured transcription of COR27 and COR28 in the cca1 lhy double mutant. ACTIN7 (ACT7), ASPARTIC PROTEINASE A1 (APA1), and ISOPENTENYL PYROPHOSPHATE: DIMETHYLALLYL PYROPHOSPHATEISOMETASE2 (IPP2) (Endo et al, 2014) were used as internal controls for normalization in our qPCR analysis. Transcription of both COR27 and COR28 was upregulated in the cca1 lhy double mutant in the morning (ZT4 and ZT8) (Figures 5C and 5D;Supplemental Figures 7A to 7D) in LD conditions.…”

Section: Mutation Of Cor27 and Cor28 Enhances Freezing Tolerancementioning

confidence: 99%

Blue Light- and Low Temperature-Regulated COR27 and COR28 Play Roles in the Arabidopsis Circadian Clock

et al. 2016

Plant Cell

117

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Light and temperature are two key environmental signals that profoundly affect plant growth and development, but underlying molecular mechanisms of how light and temperature signals affect the circadian clock are largely unknown. Here, we report that COR27 and COR28 are regulated not only by low temperatures but also by light signals. COR27 and COR28 are negative regulators of freezing tolerance but positive regulators of flowering, possibly representing a trade-off between freezing tolerance and flowering. Furthermore, loss-of-function mutations in COR27 and COR28 result in period lengthening of various circadian output rhythms and affect central clock gene expression. Also, the cor27 cor28 double mutation affects the pace of the circadian clock. Additionally, COR27 and COR28 are direct targets of CCA1, which represses their transcription via chromatin binding. Finally, we report that COR27 and COR28 bind to the chromatin of TOC1 and PRR5 to repress their transcription, suggesting that their effects on rhythms are in part due to their regulation of TOC1 and PRR5. These data demonstrate that blue light and low temperature-regulated COR27 and COR28 regulate the circadian clock as well as freezing tolerance and flowering time.

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Tissue-specific clocks in Arabidopsis show asymmetric coupling

Cited by 262 publications

References 36 publications

Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia

Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia

EARLY FLOWERING3 Redundancy Fine-Tunes Photoperiod Sensitivity

Blue Light- and Low Temperature-Regulated COR27 and COR28 Play Roles in the Arabidopsis Circadian Clock

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