Concurring with published work, our data show that HY5 transcript and protein levels increase steadily following exposure to 1 h then 6 h red light Figure 2D , Figure S3 [39]. In the dark, HY5 transcript and protein levels were low and not particularly affected by temperature in our study range.
Thus, HY5 - abundance correlates well with both the light and the temperature requirement for HY5 control of photopigment levels Figure 2A—C. To establish whether G-box element convergence represented a generic mechanism through which HY5 and PIF operate, we tested the impact of pifQ and hy5 mutations on the expression of other genes central to carotenoid or chlorophyll biosynthesis and function with G-box elements in their promoters.
These genes were chosen from genome wide transcriptional analyses specific to PIFs or HY5 [14] , [21] , [35] , [44]. The transcript levels of these genes tightly correlated with the carotenoid and chlorophyll accumulation data compare Figure 3 with Figure 2A, B. In these experiments seedlings were grown in more natural 12LD cycles sampling at 2 or 3 h post dawn T2, T3 or 8 h post dusk T20 Figures 4 and Figure S2.
Levels of binding to the VDE promoter, were very low which prevented detailed analysis data not shown. G-box cis element convergence therefore appears to represent a common mechanism through which HY5 and PIFs regulate some carotenoid and chlorophyll biosynthetic genes Figure 4. Expression is represented relative to Actin7.
Measurements were taken for biological triplicates. A non-antibody control sample was processed in parallel in each case white bars. Immunoprecipitated DNA was analysed by qPCR using specific primers covering the G-box containing region in the promoters for the indicated genes see Table S1 for primer information. The assay was carried out in triplicates. This may reflect a change in HY5 protein abundance that is detectable after exposure to 6 h of red light Figure 2D.
Previously we showed that heat leads to an accumulation of phosphorylated PIF4. This process appears to be extremely temperature sensitive as stepped increases in temperature lead to incremental rises of modified forms of PIF4 Figure S5 A.
Our results show the relative binding, particularly of HY5 and PIF1, at the G-box motifs in the promoters of several photopigment genes varies according to the ambient temperature regime. Analysing binding during the daytime compared to the night allowed us to establish whether the documented diurnal changes in HY5, PIF4 and PIF1 abundance [16] , [22] — [24] , [35] , [42] led to corresponding changes in binding.
This trend was also evident, but less marked, for PIF4. We then conducted EMSA to test whether a change in protein abundance is sufficient to drive a switch in binding to the G-box promoter fragment. This indicates that when provided in excess HY5 or PIF1 can indeed prevent the other protein from binding.
The hy5 and pifQ mRNA profiles appear to approach or on occasion converge with the wild type at distinct phases in the cycle, suggesting that HY5 and PIF control of this gene set is gated by the clock Figure 5. Unexpectedly, we found that this is not the case, as both hy5 and pifQ cause a shift in transcript levels during the day and the night Figure 5.
This indicates that during a diurnal cycle there is not a simple relationship between our recorded changes in promoter binding and the transcriptional response. Such cross-regulation is predicted to increase the amplitude of expression in pifQ and conversely, reduce the amplitude in hy5 Figure 5.
Gene expression was analysed by qPCR. Black bars represent the dark period and red ones the illuminated times. The observation that the relative action of HY5 and PIF did not change during a diurnal cycle appeared to be at odds with our finding that light or temperature stabilisation of HY5 led to concomitant rises in binding activity and gene regulation Figures 1 , 3 , 4 and Figure S4.
This suggested that a sudden or sizeable increase in HY5 levels relative to PIFs may activate gene expression. To test this hypothesis we next manipulated HY5 and PIF1 levels in vivo to establish whether we observed corresponding changes in promoter binding and gene regulation.
Triplicate Immunoblots were carried out using 2 week old seedlings. Protein was extracted at T15 and quantified against UGPase signal. Plants were grown as indicated in A and in material and methods. Samples were grown as in Figure 6 , and used for gene expression measurements by qPCR. Our data illustrate that HY5 acts antagonistically with PIFs to control photosynthetic pigment genes through a common cis element, particularly at cooler temperatures.
As this work was conducted in seedlings we wanted to establish the significance of this regulation in older plants. Our previous studies of pifQ demonstrated that PIFs also influence the accumulation of carotenoids and chlorophylls under photoperiodic conditions [17]. It therefore appears that the HY5 and PIF driven transcriptional switch is important for controlling the production of photosynthetic pigments beyond the seedling stage. This indicates the process is dynamic and that HY5 is required to actively maintain chlorophyll content in response to changing external light and temperature signals.
CO 2 assimilation was measured in parts per million ppm. Flux was calculated per unit area m 2 and results expressed relative to Col Measurements were conducted in duplicates for two independent sets of 48 plants. B Chlorophyll content for plants used in the CO 2 assimilation experiment. Chlorophyll was extracted for 12 randomly selected plants. Plants were grown as described in A.
Bars represent SE of two sets of 48 plants. Despite the knowledge that light and temperature are among the most relevant environmental signals modulating photosynthetic pigment production, there is no integrative view on how these adjustments are achieved.
We have shown that by responding to external light and temperature signals, HY5 opposes PIF action to deliver environmental control of common target genes involved in photosynthesis and photoprotection. This dual control system appears to operate in conjunction with the circadian oscillator to adjust levels of rhythmic photosynthetic gene expression. Our previous work, and that of others, identified the PIFs as negative regulators of chlorophyll and carotenoid accumulation [8] , [17] , [51] , [58].
However, optimization of these essential responses would require an additional regulator that acts antagonistically to PIFs. Here we have shown that HY5 fulfils this role as a positive regulator of photosynthetic pigment synthesis Figure 1.
This is achieved by directly binding to G-box motifs in the PSY promoter [17]. This regulation is not confined to PSY , as we presented evidence that other central carotenoid and chlorophyll pathway genes are regulated through the same dual input mechanism. HY5 and PIFs do not always act antagonistically. In the case of anthocyanin biosynthesis, PIF3 and HY5 both positively regulate the pathway by activating transcription of the same biosynthetic genes by binding to distinct cis -promoter elements G-box and another ACE motif respectively [19].
In this instance PIF3 binding is facilitated by the presence of HY5, suggesting cooperativity of action. HY5 protein accumulates in the light and is degraded in the dark [39] , [41].
In contrast, PIFs accumulate in the dark to promote dark development, and light induces rapid phytochrome dependent phosphorylation, degradation and deactivation [22] , [60] , [62] — [64]. This, analysis illustrated that the change in relative HY5:PIF promoter binding could at least partly be driven by alterations in protein abundance.
A potential explanation is that cross-regulation between HY5 and PIFs may dampen the diurnal swings in response. Such a mechanism has been recently reported by Chen and coworkers [7]. Alternatively, an independent regulator such as the circadian clock may be modulating the level or activity of HY5 or PIFs at the promoter. It is not yet known how PIFs interface with the oscillator.
Further analysis will be required to evaluate these and other possible links between HY5, PIFs and the clock. The diurnal switch between HY5- and PIF- dominant promoter binding did not lead to correlative diurnal shifts in transcriptional regulation Figures 4 , 5 and Figure S4. These results illustrate that abrupt changes in HY5 or PIF levels can lead to corresponding adjustments in signalling. Sizeable adjustments in HY5 and PIF levels and activity are known to occur in etiolated seedlings following exposure to light, and are predicted in plants exposed to abrupt changes in temperature [1] , [28] , [29] , [35] , [41] , [43] , [61] , [62] , [72] , [73].
Earlier work illustrated that HY5 is important for cold acclimation responses and enhancement of freezing tolerance [43] — [45]. Exposure of etiolated seedlings to light leads to a rapid depletion in PIF levels and increase in HY5 Figure 2D [1] , [16] , [35] , [41] , [62]. The sudden change from PIF to HY5 dominance induces a switch from transcriptional repression to activation of target photopigment genes Figure 3.
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Abstract Introduction Properties of light and solar radiation Perception of light by plants Effect of light intensity on flavonoid biosynthesis in fruits Regulation of fruit flavonoid biosynthesis by light Effect of light quality on flavonoid biosynthesis in fruits Photoperiod Concluding remarks Acknowledgments References.
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Based on this transcriptomic analysis and previous studies, a putative regulatory network of HRW-promoted anthocyanin accumulation in radish sprouts under UV-A radiation was proposed Fig.
HY5 can interact with MBW complex or other transcription factors to regulate the transcription of structural genes. Supplementation of HRW significantly increased the H 2 concentration. Further physiological and molecular experiments should be conducted to provide more precise insight into the mechanisms of HRW-promoted anthocyanin biosynthesis under UV-A, as well as the production of endogenous H 2. Four sets of transcriptome data comprising 80, unigenes were identified in radish sprouts by Illumina sequencing.
A total of 14, DEGs were identified through pairwise comparisons. Genes encoding light signal transduction elements, anthocyanin biosynthesis-related TFs and structural genes, and anthocyanin biosynthesis-related signaling pathways were also identified. The transcriptome data provided valuable information and gene sequences to accelerate the process of revealing the regulatory mechanism of HRW-promoted anthocyanin biosynthesis under UV-A in radish sprouts.
In addition, further studies are needed to confirm the precise mechanisms by which H 2 regulates physiological processes. Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem. Effects of sulfur fertilization on the accumulation of health-promoting phytochemicals in radish sprouts.
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J Plant Physiol. Hydrogen-rich water reestablishes ROS homeostasis but exerts differential effects on anthocyanin synthesis in two varieties of radish sprouts under UV-A irradiation.
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