Circadian clocks enable organisms to define subjective time, that is, to anticipate diurnal day and night cycles. Endogenous circadian rhythms regulate many aspects of an organism's physiological and ...morphological growth and development. These daily oscillations are synchronized to the environment by external cues such as light and temperature, resulting in enhanced fitness and growth vigor in plants. Recent findings concerning biochemical properties of central oscillators in Arabidopsis thaliana have advanced our understanding of circadian clock function. Central oscillators are composed of three classes of transcriptional repressors. The interactions among them include a repressilator structure. Output from the circadian clock is transduced through regulating transcription of downstream genes directly by the oscillator components. The essential role of the output pathway in the circadian system is to make different elementary steps responsible for daily cellular processes exert maximum effects at specific times of the day. Recently, significant progress was made in defining the mechanisms by which plant growth on a day-to-day basis is activated at specific times of the day in a manner dependent on photoperiod and temperature conditions. Plant growth is controlled by the clock through interactions with light and phytohormone signaling. This review focuses on the node that connects clock output to light and phytohormone signaling that coordinates plant growth with rhythmic changes in the environment.
How cell size and number are determined during organ development remains a fundamental question in cell biology. Here, we identified a GRAS family transcription factor, called SCARECROW-LIKE28 ...(SCL28), with a critical role in determining cell size in Arabidopsis. SCL28 is part of a transcriptional regulatory network downstream of the central MYB3Rs that regulate G2 to M phase cell cycle transition. We show that SCL28 forms a dimer with the AP2-type transcription factor, AtSMOS1, which defines the specificity for promoter binding and directly activates transcription of a specific set of SIAMESE-RELATED (SMR) family genes, encoding plant-specific inhibitors of cyclin-dependent kinases and thus inhibiting cell cycle progression at G2 and promoting the onset of endoreplication. Through this dose-dependent regulation of SMR transcription, SCL28 quantitatively sets the balance between cell size and number without dramatically changing final organ size. We propose that this hierarchical transcriptional network constitutes a cell cycle regulatory mechanism that allows to adjust cell size and number to attain robust organ growth.
The circadian clock is an endogenous time-keeping mechanism that enables organisms to adapt to external daily cycles. The clock coordinates biological activities with these cycles, mainly through ...genome-wide gene expression. However, the exact mechanism underlying regulation of circadian gene expression is poorly understood. Here we demonstrated that an Arabidopsis PSEUDO-RESPONSE REGULATOR 5 (PRR5), which acts in the clock genetic circuit, directly regulates expression timing of key transcription factors involved in clock-output pathways. A transient expression assay and ChIP-quantitative PCR assay using mutated PRR5 indicated that PRR5 associates with target DNA through binding at the CCT motif in vivo. ChIP followed by deep sequencing coupled with genome-wide expression profiling revealed the direct-target genes of PRR5. PRR5 direct-targets include genes encoding transcription factors involved in flowering-time regulation, hypocotyl elongation, and cold-stress responses. PRR5-target gene expression followed a circadian rhythm pattern with low, basal expression from noon until midnight, when PRR9, PRR7, and PRR5 were expressed. ChIP-quantitative PCR assays indicated that PRR7 and PRR9 bind to the direct-targets of PRR5. Genome-wide expression profiling using a prr9 prr7 prr5 triple mutant suggests that PRR5, PRR7, and PRR9 repress these targets. Taken together, our results illustrate a genetic network in which PRR5, PRR7, and PRR9 directly regulate expression timing of key transcription factors to coordinate physiological processes with daily cycles.
The plant circadian clock generates rhythms with a period close to 24 h, and it controls a wide range of physiological and developmental oscillations in habitats under natural light/dark cycles. ...Among clock-controlled developmental events, the best characterized is the photoperiodic control of flowering time in Arabidopsis thaliana. Recently, it was also reported that the clock regulates a daily and rhythmic elongation of hypocotyls. Here, we report that the promotion of hypocotyl elongation is in fact dependent on changes in photoperiods in such a way that an accelerated hypocotyl elongation occurs especially under short-day conditions. In this regard, we provide genetic evidence to show that the circadian clock regulates the photoperiodic (or seasonal) elongation of hypocotyls by modulating the expression profiles of the PIF4 and PIF5 genes encoding phytochrome-interacting bHLH (basic helix–loop–helix) factors, in such a manner that certain short-day conditions are necessary to enhance the expression of these genes during the night-time. In other words, long-day conditions are insufficient to open the clock-gate for triggering the expression of PIF4 and PIF5 during the night-time. Based on these and other results, the photoperiodic control of hypocotyl elongation is best explained by the accumulation of PIF4 and PIF5 during the night-time of short days, due to coincidence between the internal (circadian rhythm) and external (photoperiod) time cues. This mechanism is a mirror image of the photoperiod-dependent promotion of flowering in that plants should experience long-day conditions to initiate flowering promptly. Both of these clock-mediated coincidence mechanisms may coordinately confer ecological fitness to plants growing in natural habitats with varied photoperiods.
The circadian clock enables plants to adapt to their environment and control numerous physiological processes, including plant-pathogen interactions. However, it is unknown if the circadian clock ...controls nonhost resistance (NHR) in plants. To find out, we analyzed microarray data with the web-based tool DIURNAL to reveal that NHR-related genes show rhythmic expression patterns in the absence of a pathogen challenge. Our clock mutant analyses found that cca1-1 lhy-11 double mutant showed compromised NHR to Pyricularia oryzae, suggesting that two components of the circadian clock, CCA1 and LHY, are involved in regulating penetration resistance in Arabidopsis thaliana. By analyzing pen2 double mutants, we revealed that CCA1 contributes to time-of-day-dependent penetration resistance as a positive regulator and that LHY regulates post-penetration resistance as a positive regulator. Taken together, our results suggest that the circadian clock regulates the time-of-day-dependent NHR to P. oryzae and thus enables A. thaliana to counteract pathogen attacks.
Abbreviations: EE: evening element; ETI: effector-triggered immunity; NHR: nonhost resistance; PAMP: pathogen-associated molecular pattern; PTI: PAMP-triggered immunity; SAR: systemic acquired resistance.
In pen2 mutant, CCA1 contributes to time-of-day-dependent penetration resistance as a positive regulator and LHY regulates post-penetration resistance as a positive regulator. The circadian clock regulates the time-of-day-dependent NHR to P. oryzae and thus enables A. thaliana to counteract pathogen attacks.
The plant circadian clock generates rhythms with a period close to 24 h, and it controls a wide variety of physiological and developmental events. Among clock-controlled developmental events, the ...best characterized is the photoperiodic control of flowering time, which is mediated through the CONSTANS (CO)-FLOWERING LOCUS T (FT) pathway in Arabidopsis thaliana. The clock also regulates the diurnal plant growth including the elongation of hypocotyls in a short day (SDs)-specific manner. In this mechanism, phytochromes (mainly phyB) and the PHYTOCHROME-INTERACTING FACTOR4 (PIF4) and PIF5, encoding phytochrome-interacting basic helix-loop-helix (bHLH) transcription factors, play crucial roles. The time of day-specific and photoperiodic control of hypocotyl elongation is best explained by the accumulation of the PIF4 and PIF5 proteins during night-time before dawn, especially under SDs, due to coincidence between the internal (circadian rhythm) and external (photoperiod) time cues. However, the PIF4- and/or PIF5-controlled downstream factors have not yet been identified. Here, we provide evidence that ARABIDOPSIS THALIANA HOMEOBOX PROTEIN2 (ATHB2), together with auxin-inducible IAA29, is diurnally expressed with a peak at dawn under the control of PIF4 and PIF5 specifically in SDs. This coincidentally expressed transcription factor serves as a positive regulator for the elongation of hypocotyls. The expression profiles of ATHB2 were markedly altered in certain clock and phytochrome mutants, all of which show anomalous phenotypes with regard to the photoperiodic control of hypocotyl elongation. Taken together, we propose that an external coincidence model involving the clock-controlled PIF4/PIF5-ATHB2 pathway is crucial for the diurnal and photoperiodic control of plant growth in A. thaliana.
Symmetric tissue alignment is pivotal to the functions of plant vascular tissue, such as long-distance molecular transport and lateral organ formation. During the vascular development of the ...Arabidopsis roots, cytokinins initially determine cell-type boundaries among vascular stem cells and subsequently promote cell proliferation to establish vascular tissue symmetry. Although it is unknown whether and how the symmetry of initially defined boundaries is progressively refined under tissue growth in plants, such boundary shapes in animal tissues are regulated by cell fluidity, e.g., cell migration and intercalation, lacking in plant tissues. Here, we uncover that cell proliferation during vascular development produces anisotropic compressive stress, smoothing, and symmetrizing cell arrangement of the vascular-cell-type boundary. Mechanistically, the GATA transcription factor HANABA-TARANU cooperates with the type-B Arabidopsis response regulators to form an incoherent feedforward loop in cytokinin signaling. The incoherent feedforward loop fine-tunes the position and frequency of vascular cell proliferation, which in turn restricts the source of mechanical stress to the position distal and symmetric to the boundary. By combinatorial analyses of mechanical simulations and laser cell ablation, we show that the spatially constrained environment of vascular tissue efficiently entrains the stress orientation among the cells to produce a tissue-wide stress field. Together, our data indicate that the localized proliferation regulated by the cytokinin signaling circuit is decoded into a globally oriented mechanical stress to shape the vascular tissue symmetry, representing a reasonable mechanism controlling the boundary alignment and symmetry in tissue lacking cell fluidity.
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•Xylem-procambium boundary is refined with vascular tissue growth•HANABA-TARANU/cytokinin circuit fine-tunes the proliferation position and frequency•Biased vascular proliferation orients compressive stress among vascular cells•Proliferation-induced stress symmetrizes and smoothens less fluidic tissue boundary
How is the symmetry of a multicellular organ elaborated in a plant? Fujiwara et al. show that cytokinin-directed patterned proliferation produces coherently oriented mechanical stress during vascular tissue growth in Arabidopsis roots. This tissue-wide stress field efficiently symmetrizes the arrangement of immobile cells, refining organ symmetry.
Arabidopsis PSEUDO RESPONSE REGULATOR (PRR) genes are components of the circadian clock mechanism. In order to understand the scope of genome-wide transcriptional regulation by PRR genes, a ...comparison survey of gene expression in wild-type Arabidopsis and a prr9-11 prr7-10 prr5-10 triple mutant (d975) using mRNA collected during late daytime was conducted using an Affymetrix ATH-1 GeneChipsup(R). The expression of 'night genes' increased and the expression of 'day genes' decreased toward the end of the diurnal tight phase, but expression of these genes was essentially constant in d975. The expression levels of 'night genes' were lower, whereas the expression of 'day genes' was higher in d975 than in the wild type. Bioinformatics approaches have indicated that the set of up-regulated genes in d975 and the set of cold-responsive genes have significant overlap. We found that d975 is more tolerant to cold, high salinity and drought stresses than the wild type. In addition, dehydration-responsive element B1/C-repeat-binding factor (DREB1/CBF), which is expressed around mid-day, is more highly expressed in d975. Raffinose and L-proline accumulated at higher levels in d975 even when plants were grown under normal conditions. These results suggest that PRR9, PRR7 and PRR5 are involved in a mechanism that anticipates diurnal cold stress and which initiates a stress response by mediating cyclic expression of stress response genes, including DREB1/CBF.
Arabidopsis thaliana has 11 members belonging to the typical type-B ARR (authentic response regulator) family. Among them, seven highly homologous members appear also to be conserved in rice (Oryza ...sativa), but others are not. It was suggested that these seven ARRs are commonly implicated as DNA-binding transcription factors in the phosphorelay-mediated cytokinin signal transduction network in higher plants. To gain an insight into the functions of the cytokinin-associated type-B ARRs, we previously investigated an arr1 arr10 arr12 triple mutant and reported that it exhibited stunted growth and abnormality in vascular development. Based on this fact, here we attempted to characterize the mutant intensively with reference to cytokinin-associated phenotypes through the life cycle. We showed that the observed cytokinin-associated phenotypes of arr1 arr10 arr12 were very severe and highly analogous to those observed for certain ahk2 ahk3 ahk4/cre1 triple mutants, which have virtually no cytokinin receptor to propagate the phosphorelay signal transduction network. Among the seven ARR members belonging to the cytokinin-associated type-B ARR subfamily, it was thus suggested that ARR1, ARR10 and ARR12 together play essential (or general) roles in cytokinin signal transduction. It is therefore conceivable that the other type-B ARRs (ARR2, ARR11, ARR14 and ARR18) might play more specific roles spatially and temporally in plants.
In Arabidopsis thaliana, the circadian clock regulates diurnal and photoperiodic plant growth including the elongation of hypocotyls in a time-of-day-specific and short-day (SD)-specific manner. The ...clock-controlled PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) encoding a basic helix-loop-helix (bHLH) transcription factor plays crucial roles in this regulation. PIF4 is transcribed precociously at the end of the night in SDs, under which conditions the protein product is stably accumulated, while PIF4 is expressed exclusively during the daytime in long days (LDs), under which conditions the protein product is degraded by light-activated phytochrome B. The dawn- and SD-specific elongation of hypocotyls is best explained by the coincident accumulation of the active PIF4 protein during the night-time before dawn specifically in SDs. However, this coincidence model was challenged with the recent finding that the elongation of hypocotyls is markedly promoted at high growth temperature (i.e. 28°C) even under LDs in a PIF4-dependent manner. Here, we reconciled these apparently conflicting facts by showing that the transcription of PIF4 occurs precociously at the end of the night-time at 28°C in LDs, similarly to in SDs. Both the events resulted in the same consequence, i.e. that a set of PIF4 target genes (ATHB2, GH3.5, IAA19, IAA29, BRox2, GAI, ACS8 and CKX5) was induced accordingly in a time-of-day-specific manner. Taken together, we propose an extended double coincidence mechanism, by which the two environmental cues (i.e. photoperiods and temperatures), both of which vary on a season to season basis, are integrated into the same clock- and PIF4-mediated output pathway and regulate a hormone signaling network to fit plant architectures properly to domestic habitats.
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