A point mutation in Phytochromobilin Synthase alters the circadian clock and photoperiodic flowering of Medicago truncatula

Plants use seasonal cues to initiate flowering at an appropriate time of year to ensure optimal reproductive success. The circadian clock integrates these daily and seasonal cues with internal cues to initiate flowering. The molecular pathways that control the sensitivity of flowering to photoperiod (daylength) are well described in the model plant Arabidopsis. However, much less is known in crop species, such as the legume family species. Here we performed a flowering time screen of a TILLING population of Medicago truncatula and found a line with late-flowering and altered light-sensing phenotypes. Using RNA-sequencing, we identified a nonsense mutation in the Phytochromobilin Synthase (MtPΦBS) gene, which encodes an enzyme that carries out the final step in the biosynthesis of the chromophore required for phytochrome (PHY) activity. The analysis of the circadian clock in the MtpΦbs mutant revealed a shorter circadian period, which was shared with the phyA mutant. The MtpΦbs and MtphyA mutants showed downregulation of FT floral regulators MtFTa1, MtFTb1/b2 and a shift in phase for morning and night core clock genes. Our findings show that PHYA is necessary to synchronize the circadian clock and integration of light signaling to promote expression of the MtFT genes to precisely time flowering.

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SPF45-related splicing factor for phytochrome signaling promotes photomorphogenesis by regulating pre-mRNA splicing in Arabidopsis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1706379114 ◽

2017 ◽

Vol 114 (33) ◽

pp. E7018-E7027 ◽

Cited By ~ 18

Author(s):

Ruijiao Xin ◽

Ling Zhu ◽

Patrice A. Salomé ◽

Estefania Mancini ◽

Carine M. Marshall ◽

...

Keyword(s):

Gene Expression ◽

Circadian Clock ◽

Molecular Mechanisms ◽

Fluorescent Protein ◽

Clock Genes ◽

Mrna Processing ◽

Mrna Splicing ◽

Splicing Factor ◽

Light Signaling ◽

Small Nuclear Ribonucleoprotein

Light signals regulate plant growth and development by controlling a plethora of gene expression changes. Posttranscriptional regulation, especially pre-mRNA processing, is a key modulator of gene expression; however, the molecular mechanisms linking pre-mRNA processing and light signaling are not well understood. Here we report a protein related to the human splicing factor 45 (SPF45) named splicing factor for phytochrome signaling (SFPS), which directly interacts with the photoreceptor phytochrome B (phyB). In response to light, SFPS-RFP (red fluorescent protein) colocalizes with phyB-GFP in photobodies. sfps loss-of-function plants are hyposensitive to red, far-red, and blue light, and flower precociously. SFPS colocalizes with U2 small nuclear ribonucleoprotein-associated factors including U2AF65B, U2A′, and U2AF35A in nuclear speckles, suggesting SFPS might be involved in the 3′ splice site determination. SFPS regulates pre-mRNA splicing of a large number of genes, of which many are involved in regulating light signaling, photosynthesis, and the circadian clock under both dark and light conditions. In vivo RNA immunoprecipitation (RIP) assays revealed that SFPS associates with EARLY FLOWERING 3 (ELF3) mRNA, a critical link between light signaling and the circadian clock. Moreover, PHYTOCHROME INTERACTING FACTORS (PIFs) transcription factor genes act downstream of SFPS, as the quadruple pif mutant pifq suppresses defects of sfps mutants. Taken together, these data strongly suggest SFPS modulates light-regulated developmental processes by controlling pre-mRNA splicing of light signaling and circadian clock genes.

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Roles of Neuropeptides, VIP and AVP, in the Mammalian Central Circadian Clock

Frontiers in Neuroscience ◽

10.3389/fnins.2021.650154 ◽

2021 ◽

Vol 15 ◽

Author(s):

Daisuke Ono ◽

Ken-ichi Honma ◽

Sato Honma

Keyword(s):

Transcription Factors ◽

Circadian Rhythms ◽

Circadian Clock ◽

Cellular Networks ◽

Clock Genes ◽

Circadian System ◽

Developmental Changes ◽

Circadian Period ◽

Functional Roles ◽

Environmental Light

In mammals, the central circadian clock is located in the suprachiasmatic nucleus (SCN) of the hypothalamus. Individual SCN cells exhibit intrinsic oscillations, and their circadian period and robustness are different cell by cell in the absence of cellular coupling, indicating that cellular coupling is important for coherent circadian rhythms in the SCN. Several neuropeptides such as arginine vasopressin (AVP) and vasoactive intestinal polypeptide (VIP) are expressed in the SCN, where these neuropeptides function as synchronizers and are important for entrainment to environmental light and for determining the circadian period. These neuropeptides are also related to developmental changes of the circadian system of the SCN. Transcription factors are required for the formation of neuropeptide-related neuronal networks. Although VIP is critical for synchrony of circadian rhythms in the neonatal SCN, it is not required for synchrony in the embryonic SCN. During postnatal development, the clock genes cryptochrome (Cry)1 and Cry2 are involved in the maturation of cellular networks, and AVP is involved in SCN networks. This mini-review focuses on the functional roles of neuropeptides in the SCN based on recent findings in the literature.

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GhLUX1 and GhELF3 Are Two Components of the Circadian Clock That Regulate Flowering Time of Gossypium hirsutum

Frontiers in Plant Science ◽

10.3389/fpls.2021.691489 ◽

2021 ◽

Vol 12 ◽

Author(s):

Pengbo Hao ◽

Aimin Wu ◽

Pengyun Chen ◽

Hantao Wang ◽

Liang Ma ◽

...

Keyword(s):

Circadian Clock ◽

Flowering Time ◽

Clock Genes ◽

Early Flowering ◽

Rhythmic Expression ◽

Photoperiodic Flowering ◽

Early Maturing ◽

Circadian Clock Genes ◽

Delayed Flowering ◽

Physicochemical And Structural Properties

Photoperiod is an important external factor that regulates flowering time, the core mechanism of which lies in the circadian clock-controlled expression of FLOWERING LOCUS T (FT) and its upstream regulators. However, the roles of the circadian clock in regulating cotton flowering time are largely unknown. In this study, we cloned two circadian clock genes in cotton, GhLUX1 and GhELF3. The physicochemical and structural properties of their putative proteins could satisfy the prerequisites for the interaction between them, which was proved by yeast two-hybrid (Y2H) and Bimolecular Fluorescent Complimentary (BiFC) assays. Phylogenetic analysis of LUXs and ELF3s indicated that the origin of LUXs was earlier than that of ELF3s, but ELF3s were more divergent and might perform more diverse functions. GhLUX1, GhELF3, GhCOL1, and GhFT exhibited rhythmic expression and were differentially expressed in the early flowering and late-flowering cotton varieties under different photoperiod conditions. Both overexpression of GhLUX1 and overexpression of GhELF3 in Arabidopsis delayed flowering probably by changing the oscillation phases and amplitudes of the key genes in the photoperiodic flowering pathway. Both silencing of GhLUX1 and silencing of GhELF3 in cotton increased the expression of GhCOL1 and GhFT and resulted in early flowering. In summary, the circadian clock genes were involved in regulating cotton flowering time and could be the candidate targets for breeding early maturing cotton varieties.

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Circadian Clock Components Offer Targets for Crop Domestication and Improvement

Genes ◽

10.3390/genes12030374 ◽

2021 ◽

Vol 12 (3) ◽

pp. 374

Author(s):

C. Robertson McClung

Keyword(s):

Circadian Clock ◽

Clock Genes ◽

Crop Improvement ◽

Geographic Area ◽

Plant Performance ◽

Plant Domestication ◽

Abiotic And Biotic Stresses ◽

Biotic Stresses ◽

Photoperiodic Flowering ◽

Circadian Clock Genes

During plant domestication and improvement, farmers select for alleles present in wild species that improve performance in new selective environments associated with cultivation and use. The selected alleles become enriched and other alleles depleted in elite cultivars. One important aspect of crop improvement is expansion of the geographic area suitable for cultivation; this frequently includes growth at higher or lower latitudes, requiring the plant to adapt to novel photoperiodic environments. Many crops exhibit photoperiodic control of flowering and altered photoperiodic sensitivity is commonly required for optimal performance at novel latitudes. Alleles of a number of circadian clock genes have been selected for their effects on photoperiodic flowering in multiple crops. The circadian clock coordinates many additional aspects of plant growth, metabolism and physiology, including responses to abiotic and biotic stresses. Many of these clock-regulated processes contribute to plant performance. Examples of selection for altered clock function in tomato demonstrate that with domestication, the phasing of the clock is delayed with respect to the light–dark cycle and the period is lengthened; this modified clock is associated with increased chlorophyll content in long days. These and other data suggest the circadian clock is an attractive target during breeding for crop improvement.

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Cross-species complementation reveals conserved functions for EARLY FLOWERING 3 between monocots and dicots

10.1101/131185 ◽

2017 ◽

Author(s):

He Huang ◽

Malia A. Gehan ◽

Sarah E. Huss ◽

Sophie Alvarez ◽

Cesar Lizarraga ◽

...

Keyword(s):

Circadian Clock ◽

Clock Genes ◽

Expression Profiles ◽

Affinity Purification ◽

Brachypodium Distachyon ◽

Sequence Divergence ◽

Plant Responses ◽

Crop Species ◽

Physiological Level ◽

High Sequence Divergence

ABSTRACTPlant responses to the environment are shaped by external stimuli and internal signaling pathways. In both the model plant Arabidopsis thaliana and crop species, circadian clock factors have been identified as critical for growth, flowering and circadian rhythms. Outside of A. thaliana, however, little is known about the molecular function of clock genes. Therefore, we sought to compare the function of Brachypodium distachyon and Seteria viridis orthologs of EARLY FLOWERING3, a key clock gene in A. thaliana. To identify both cycling genes and putative ELF3 functional orthologs in S. viridis, a circadian RNA-seq dataset and online query tool (Diel Explorer) was generated as a community resource to explore expression profiles of Setaria genes under constant conditions after photo- or thermo-entrainment. The function of ELF3 orthologs from A. thaliana, B. distachyon, and S. viridis were tested for complementation of an elf3 mutation in A. thaliana. Despite comparably low sequence identity versus AtELF3 (less than 37%), both monocot orthologs were capable of rescuing hypocotyl elongation, flowering time and arrhythmic clock phenotypes. Molecular analysis using affinity purification and mass spectrometry to compare physical interactions also found that BdELF3 and SvELF3 could be integrated into similar complexes and networks as AtELF3, including forming a composite evening complex. Thus, we find that, despite 180 million years of separation, BdELF3 and SvELF3 can functionally complement loss of ELF3 at the molecular and physiological level.One Sentence SummaryOrthologs of a key circadian clock component ELF3 from grasses functionally complement the Arabidopsis counterpart at the molecular and physiological level, in spite of high sequence divergence.

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ASK family kinases mediate cellular stress and redox signaling to circadian clock

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1719298115 ◽

2018 ◽

Vol 115 (14) ◽

pp. 3646-3651 ◽

Cited By ~ 12

Author(s):

Kiyomichi Imamura ◽

Hikari Yoshitane ◽

Kazuki Hattori ◽

Mitsuo Yamaguchi ◽

Kento Yoshida ◽

...

Keyword(s):

Circadian Clock ◽

Cultured Cells ◽

Clock Genes ◽

Cellular Stress ◽

Underlying Mechanism ◽

Circadian Period ◽

Redox States ◽

Rhythmic Expression ◽

Physiological Impact ◽

Intracellular Redox

Daily rhythms of behaviors and physiologies are generated by the circadian clock, which is composed of clock genes and the encoded proteins forming transcriptional/translational feedback loops (TTFLs). The circadian clock is a self-sustained oscillator and flexibly responds to various time cues to synchronize with environmental 24-h cycles. However, the key molecule that transmits cellular stress to the circadian clockwork is unknown. Here we identified apoptosis signal-regulating kinase (ASK), a member of the MAPKKK family, as an essential mediator determining the circadian period and phase of cultured cells in response to osmotic changes of the medium. The physiological impact of ASK signaling was demonstrated by a response of the clock to changes in intracellular redox states. Intriguingly, the TTFLs drive rhythmic expression of Ask genes, indicating ASK-mediated association of the TTFLs with intracellular redox. In behavioral analysis, Ask1, Ask2, and Ask3 triple-KO mice exhibited compromised light responses of the circadian period and phase in their activity rhythms. LC-MS/MS–based proteomic analysis identified a series of ASK-dependent and osmotic stress-responsive phosphorylations of proteins, among which CLOCK, a key component of the molecular clockwork, was phosphorylated at Thr843 or Ser845 in the carboxyl-terminal region. These findings reveal the ASK-dependent stress response as an underlying mechanism of circadian clock flexibility.

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Circadian Clock Genes and the Transcriptional Architecture of the Clock Mechanism

Endocrine Abstracts ◽

10.1530/endoabs.59.pl4 ◽

2018 ◽

Cited By ~ 1

Author(s):

Joseph Takahashi

Keyword(s):

Circadian Clock ◽

Clock Genes ◽

Circadian Clock Genes ◽

Clock Mechanism

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Faculty Opinions recommendation of The Arabidopsis SPA1 gene is required for circadian clock function and photoperiodic flowering.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1001654.374751 ◽

2006 ◽

Author(s):

Xing Wang Deng

Keyword(s):

Circadian Clock ◽

Photoperiodic Flowering

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Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars

BMC Genomics ◽

10.1186/s12864-021-07869-8 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Yanlei Yue ◽

Ze Jiang ◽

Enoch Sapey ◽

Tingting Wu ◽

Shi Sun ◽

...

Keyword(s):

Gene Expression ◽

Circadian Clock ◽

Chromosome Structure ◽

Clock Genes ◽

Expression Profiles ◽

Circadian Rhythmicity ◽

Rna Seq ◽

Night Time ◽

Time Points ◽

Circadian Clock Genes

Abstract Background In soybean, some circadian clock genes have been identified as loci for maturity traits. However, the effects of these genes on soybean circadian rhythmicity and their impacts on maturity are unclear. Results We used two geographically, phenotypically and genetically distinct cultivars, conventional juvenile Zhonghuang 24 (with functional J/GmELF3a, a homolog of the circadian clock indispensable component EARLY FLOWERING 3) and long juvenile Huaxia 3 (with dysfunctional j/Gmelf3a) to dissect the soybean circadian clock with time-series transcriptomal RNA-Seq analysis of unifoliate leaves on a day scale. The results showed that several known circadian clock components, including RVE1, GI, LUX and TOC1, phase differently in soybean than in Arabidopsis, demonstrating that the soybean circadian clock is obviously different from the canonical model in Arabidopsis. In contrast to the observation that ELF3 dysfunction results in clock arrhythmia in Arabidopsis, the circadian clock is conserved in soybean regardless of the functional status of J/GmELF3a. Soybean exhibits a circadian rhythmicity in both gene expression and alternative splicing. Genes can be grouped into six clusters, C1-C6, with different expression profiles. Many more genes are grouped into the night clusters (C4-C6) than in the day cluster (C2), showing that night is essential for gene expression and regulation. Moreover, soybean chromosomes are activated with a circadian rhythmicity, indicating that high-order chromosome structure might impact circadian rhythmicity. Interestingly, night time points were clustered in one group, while day time points were separated into two groups, morning and afternoon, demonstrating that morning and afternoon are representative of different environments for soybean growth and development. However, no genes were consistently differentially expressed over different time-points, indicating that it is necessary to perform a circadian rhythmicity analysis to more thoroughly dissect the function of a gene. Moreover, the analysis of the circadian rhythmicity of the GmFT family showed that GmELF3a might phase- and amplitude-modulate the GmFT family to regulate the juvenility and maturity traits of soybean. Conclusions These results and the resultant RNA-seq data should be helpful in understanding the soybean circadian clock and elucidating the connection between the circadian clock and soybean maturity.

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