Seed germination and postgerminative growth require the precise coordination of multiple intrinsic and environmental signals. The phytohormone abscisic acid (ABA) suppresses these processes in Arabidopsis thaliana and the circadian clock contributes to the regulation of ABA signaling. However, the molecular mechanism underlying circadian clock-mediated ABA signaling remains largely unknown. Here, we found that the core circadian clock proteins PSEUDO-RESPONSE REGULATOR5 (PRR5) and PRR7 physically associate with ABSCISIC ACID-INSENSITIVE5 (ABI5), a crucial transcription factor of ABA signaling. PRR5 and PRR7 positively modulate ABA signaling redundantly during seed germination. Disrupting PRR5 and PRR7 simultaneously rendered germinating seeds hyposensitive to ABA, whereas the overexpression of PRR5 enhanced ABA signaling to inhibit seed germination. Consistent with this, the expression of several ABA-responsive genes is upregulated by PRR proteins. Genetic analysis demonstrated that PRR5 promotes ABA signaling mainly dependently on ABI5. Further mechanistic investigation revealed that PRR5 stimulates the transcriptional function of ABI5 without affecting its stability. Collectively, our results indicate that these PRR proteins function synergistically with ABI5 to activate ABA responses during seed germination, thus providing a mechanistic understanding of how ABA signaling and the circadian clock are directly integrated through a transcriptional complex involving ABI5 and central circadian clock components.

The Arabidopsis circadian clock protein PRR5 interacts with and stimulates ABI5 to modulate abscisic acid signaling during seed germination.

Endogenous circadian clock integrates cyclic signals of environment and daily and seasonal behaviors of organism to achieve spatiotemporal synchronization, which greatly improves genetic diversity and fitness of species. This review addresses recent studies on plant circadian system in the field of Chronobiology, covering topics on molecular mechanisms, internal and external Zeitgebers, and hierarchical regulation of physiological outputs. The architecture of the circadian clock involves the autoregulatory transcriptional feedback loops, post-translational modifications of core oscillators, and epigenetic modifications of DNA and histones. Here, light, temperature, humidity, and internal elemental nutrients are summarized to illustrate the sensitivity of the circadian clock to timing cues. In addition, the circadian clock runs cell-autonomously, driving independent circadian rhythms in various tissues. The core oscillator responds to each other with biochemical factors including calcium ions, mineral nutrients, photosynthetic products, and hormones. We describe clock components sequentially expressed during a 24-h day that regulate rhythmic growth, aging, immune response, and resistance to biotic and abiotic stresses. Notably, more data have suggested the circadian clock linking chrono-culture to key agronomic traits in crops. This article is protected by copyright. All rights reserved.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/jipb.13230

Circadian clock in plants: Linking timing to fitness.

Abstract The circadian clock, a time-keeping mechanism, drives nearly 24-h self-sustaining rhythms at the physiological, cellular, and molecular levels, keeping them synchronized with the cyclic changes of environmental signals. The plant clock is sensitive to external and internal stress signals that act as timing cues to influence the circadian rhythms through input pathways of the circadian clock system. In order to cope with environmental stresses, many core oscillators are involved in defense while maintaining daily growth in various ways. Recent studies have shown that a hierarchical multi-oscillator network orchestrates the defense through rhythmic accumulation of gene transcripts, alternative splicing of mRNA precursors, modification and turnover of proteins, subcellular localization, stimuli-induced phase separation, and long-distance transport of proteins. This review summarizes the essential role of circadian core oscillators in response to stresses in Arabidopsis thaliana and crops, including daily and seasonal abiotic stresses (low or high temperature, drought, high salinity, and nutrition deficiency) and biotic stresses (pathogens and herbivorous insects). By integrating time-keeping mechanisms, circadian rhythms and stress resistance, we provide a temporal perspective for scientists to better understand plant environmental adaptation and breed high-quality crop germplasm for agricultural production. 

https://link.springer.com/content/pdf/10.1007/s44154-022-00040-7.pdf

The circadian clock ticks in plant stress responses

Two central circadian oscillators OsPRR59 and OsPRR95 modulate magnesium homeostasis and carbon fixation by regulating rhythmic expression of OsMGT3 in rice.

Plants require an endogenous regulatory network and mechanism to cope with diurnal environmental changes and compensate for their sessile nature. Plants use the circadian clock to anticipate diurnal changes. Circadian rhythm predicts a 24-h cycle with 16 h of light and 8 h of darkness in response to abiotic and biotic factors as well as the appropriate temperature. For a plant’s fitness, proper growth, and development, these rhythms synchronize the diurnal photoperiodic changes. Input pathway, central oscillator, and output pathway are the three components that make up the endogenous clock. There are also transcriptional and translational feedback loops (TTFLs) in the clock, which are dependent on the results of gene expression. Several physiological processes, such as stress acclimatization, hormone signaling, morphogenesis, carbon metabolism, and defense response, are currently being investigated for their interactions with the circadian clock using phenotypic, genomic, and metabolic studies. This review examines the role of circadian rhythms in the regulation of plant metabolic pathways, such as photosynthesis and carbon metabolism, as well as developmental and degenerative processes, such as flowering and senescence. Furthermore, we summarized signaling pathways related to circadian rhythms, such as defense response and gene regulatory pathways.

/pdf/role-of-circadian-rhythms-in-major-plant-metabolic-and-dluae0mc.pdf

Role of Circadian Rhythms in Major Plant Metabolic and Signaling Pathways

The core plant circadian oscillator is composed of multiple interlocked transcriptional-translational feedback loops, which synchronize endogenous diel physiological rhythms to the cyclic changes of environmental cues. PSEUDO-RESPONSE REGULATORS (PRRs) have been identified as negative components in the circadian clock, though their underlying molecular mechanisms remain largely unknown. Here, we found that a subfamily of zinc finger transcription factors, B-box (BBX)-containing proteins, have a critical role in fine-tuning circadian rhythm. We demonstrated that overexpressing Arabidopsis thaliana BBX19 and BBX18 significantly lengthened the circadian period, while the null mutation of BBX19 accelerated the circadian speed. Moreover, BBX19 and BBX18, which are expressed during the day, physically interacted with PRR9, PRR7, and PRR5 in the nucleus in precise temporal ordering from dawn to dusk, consistent with the respective protein accumulation pattern of PRRs. Our transcriptomic and genetic analysis indicated that BBX19 and PRR9, PRR7, and PRR5 cooperatively inhibited the expression of morning-phased clock genes. PRR proteins affected BBX19 recruitment to the CCA1, LHY, and RVE8 promoters. Collectively, our findings show that BBX19 interacts with PRRs to orchestrate circadian rhythms, and suggest the indispensable role of transcriptional regulators in fine-tuning the circadian clock.

/pdf/bbx19-fine-tunes-the-circadian-rhythm-by-interacting-with-2rp5rs2qk7.pdf

BBX19 fine-tunes the circadian rhythm by interacting with PSEUDO-RESPONSE REGULATOR proteins to facilitate their repressive effect on morning-phased clock genes.

To enhance plant fitness under natural conditions, the circadian clock is synchronized and entrained by light via photoreceptors. In turn, the circadian clock exquisitely regulates the abundance and activity of photoreceptors via largely uncharacterized mechanisms. Here we show that the clock regulator TIME FOR COFFEE (TIC) controls the activity of the far-red light photoreceptor phytochrome A (phyA) at multiple levels in Arabidopsis thaliana. Null mutants of TIC displayed dramatically increased sensitivity to light irradiation with respect to hypocotyl growth, especially to far-red light. RNA-sequencing demonstrated that TIC and phyA play largely opposing roles in controlling light-regulated gene expression at dawn. Additionally, TIC physically interacts with the transcriptional repressor TOPLESS (TPL), which was associated with the significantly increased PHYA transcript levels in the tic-2 and tpl-1 mutants. Moreover, TIC interacts with phyA in the nucleus, thereby affecting phyA protein turnover and the formation of phyA nuclear speckles following light irradiation. Genetically, phyA was found to act downstream of TIC in regulating far red light-inhibited growth. Taken together, these findings indicate that TIC acts as a major negative regulator of phyA by integrating transcriptional and post-translational mechanisms at multiple levels.

TIME FOR COFFEE regulates phytochrome A-mediated hypocotyl growth through dawn-phased signaling.

Abstract Circadian pace is modulated by light intensity, known as the Aschoff’s rule, with largely unrevealed mechanisms. Here we report that photoreceptor CRY2 mediates blue light input to the circadian clock by directly interacting with clock core component PRR9 in blue light dependent manner. This physical interaction dually blocks the accessibility of PRR9 protein to its co-repressor TPL/TPRs and the resulting kinase PPKs. Notably, phosphorylation of PRR9 by PPKs is critical for its DNA binding and repressive activity, hence to ensure proper circadian speed. Given the labile nature of CRY2 in strong blue light, our findings provide a mechanistic explanation for Aschoff’s rule in plants, i.e., blue light triggers CRY2 turnover in proportional to its intensity, which accordingly releasing PRR9 to fine tune circadian speed. Our findings not only reveal a network mediating light input into the circadian clock, but also unmask a mechanism by which the Arabidopsis circadian clock senses light intensity. 

/pdf/aschoffs-rule-on-circadian-rhythms-orchestrated-by-blue-ky54v7op.pdf

Aschoff’s rule on circadian rhythms orchestrated by blue light sensor CRY2 and clock component PRR9

As an endogenous time-keeping mechanism, the circadian clock benefits plant fitness and adaptation to the rhythmically changed diel environments. The key components within the core oscillator of plant circadian clock have been extensively characterised, however, the fine-tuning circadian regulators are still less identified. Here, we demonstrated that BBX28 and BBX29, the two B-Box V subfamily members lacking DNA-binding motifs, are involved in the regulation of Arabidopsis circadian clock. Over-expressing either BBX28 or BBX29 significantly lengthened circadian period, whereas loss-of-function of BBX28 rather than BBX29 displayed a modestly long period in free-running condition. Mechanistically, BBX28 and BBX29 interacted with core clock components PRR5, PRR7 and PRR9 in nucleus to augment their transcriptional repressive activities. RNA-sequencing analysis further revealed that BBX28 and BBX29 shared 686 common differentially expressed genes (DEGs) including a subset of known direct transcriptional targets of PRR proteins within core oscillator, including CCA1, LHY, LNKs and RVE8 etc. Intriguingly, PRR proteins can feedback repress BBX28 and BBX29 transcription by associating with their promoters. Together, our findings unmasked an exquisite mechanism in which BBX28 and BBX29 interplay with PRR proteins to fine-tune the circadian pace.

Yingjun Yu

Papers

BBX19 fine-tunes the circadian rhythm by interacting with PSEUDO-RESPONSE REGULATOR proteins to facilitate their repressive effect on morning-phased clock genes.

TIME FOR COFFEE regulates phytochrome A-mediated hypocotyl growth through dawn-phased signaling.

Aschoff’s rule on circadian rhythms orchestrated by blue light sensor CRY2 and clock component PRR9

B-Box proteins BBX28 and BBX29 interplay with PSEUDO-RESPONSE REGULATORS to fine-tune circadian clock in Arabidopsis.