The G-Box Transcriptional Regulatory Code in Arabidopsis

Ezer, Daphne; Shepherd, Samuel J.K.; Brestovitsky, Anna; Dickinson, Patrick; Cortijo, Sandra; Charoensawan, Varodom; Box, Mathew S.; Biswas, Sandhyarani; Jaeger, Katja E.; Wigge, Philip A.

doi:10.1104/pp.17.01086

Cited by 117 publications

(78 citation statements)

References 80 publications

(101 reference statements)

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“…We hypothesized that the transcription factor (TF) bZIP63 might regulate PRR7 because bZIP63 is regulated by the SnRK1 energy sensor and bZIP63 transcripts peak before PRR7 in constant light ( Figure S1 A). bZIP63 is a strong candidate for sugar-mediated regulation of the circadian oscillator because it binds ACGT core element motifs [ 16 ], and the PRR7 promoter contains five ACGT-core bZIP TF-binding motifs within 300 bp of its transcription start site, including a canonical G-box at −254 bp [ 11 , 17 , 18 , 19 ] ( Figure 1 A). bZIP63 binds a PRR7 promoter region spanning −276 to −182 ( Figures 1 A and 1B; primer pair 1).…”

Section: Resultsmentioning

confidence: 99%

Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63

et al. 2018

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SummarySynchronization of circadian clocks to the day-night cycle ensures the correct timing of biological events. This entrainment process is essential to ensure that the phase of the circadian oscillator is synchronized with daily events within the environment [1], to permit accurate anticipation of environmental changes [2, 3]. Entrainment in plants requires phase changes in the circadian oscillator, through unidentified pathways, which alter circadian oscillator gene expression in response to light, temperature, and sugars [4, 5, 6]. To determine how circadian clocks respond to metabolic rhythms, we investigated the mechanisms by which sugars adjust the circadian phase in Arabidopsis [5]. We focused upon metabolic regulation because interactions occur between circadian oscillators and metabolism in several experimental systems [5, 7, 8, 9], but the molecular mechanisms are unidentified. Here, we demonstrate that the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) regulates the circadian oscillator gene PSEUDO RESPONSE REGULATOR7 (PRR7) to change the circadian phase in response to sugars. We find that SnRK1, a sugar-sensing kinase that regulates bZIP63 activity and circadian period [10, 11, 12, 13, 14] is required for sucrose-induced changes in circadian phase. Furthermore, TREHALOSE-6-PHOSPHATE SYNTHASE1 (TPS1), which synthesizes the signaling sugar trehalose-6-phosphate, is required for circadian phase adjustment in response to sucrose. We demonstrate that daily rhythms of energy availability can entrain the circadian oscillator through the function of bZIP63, TPS1, and the KIN10 subunit of the SnRK1 energy sensor. This identifies a molecular mechanism that adjusts the circadian phase in response to sugars.

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Section: Resultsmentioning

confidence: 99%

Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63

et al. 2018

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“…Making used of publicly available transcriptomic data, we further expanded our investigation of the transcriptional relationship among the flowering-time-relating genes of interest, namely PIF4 , PIF5 , ELF3 , and FLC , and their immediate up- and downstream regulatory genes, based on the Flowering Interactive Database (FLOR-ID) (Bouche et al, 2016) (Table S2, see Methods), under different temperature conditions (low temperature, normal temperature, high temperature, temperature shift and heat shock), different light conditions (short-day photoperiod and long-day photoperiod) and different tissue types (whole seedling, rosette leaves, mature pollen grain, root and shoot apical meristem) (see Table S3 for complete information of transcriptomic datasets obtained). In total, we extracted 62 flowering-time-relating genes ( PIF4 , PIF5 , ELF3 , and FLC and their immediate neighbours) from the Flowering Interactive Database (FLOR-ID) (Bouche et al, 2016) (Table S2, see Methods), and their transcriptional levels from 152 RNA-seq experiments (Cortijo et al, 2017; Dickinson et al, 2018; Durufle et al, 2017; Ezer, Jung, et al, 2017; Ezer, Shepherd, et al, 2017; Martins et al, 2017; Pajoro et al, 2017; Rahmati Ishka et al, 2018; Tasset et al, 2018; Zhu et al, 2015) (Table S4).…”

Section: Resultsmentioning

confidence: 99%

Role of PIF4 and FLC in controlling flowering time under daily variable temperature profile

Jenkitkonchai

Marriott

Yang

et al. 2020

Preprint

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Initiation of flowering is a crucial developmental event that requires both internal and environmental signals to determine when floral transition should occur to maximize reproductive success. Ambient temperature is one of the key environmental signals that highly influence flowering time, not only seasonally but also in the context of drastic temperature fluctuation due to global warming. Molecular mechanisms of how high or low constant temperatures affect the flowering time have been largely characterized in the model plant Arabidopsis thaliana; however, the effect of natural daily variable temperature outside laboratories is only partly explored. Several groups of flowering genes have been shown to play important roles in temperature responses, including two temperature-responsive transcription factors (TFs), namely PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and FLOWERING LOCUS C (FLC), that act antagonistically to regulate flowering time by activating or repressing floral integrator FLOWERING LOCUS T (FT). In this study, we have demonstrated that the daily variable temperature (VAR) causes early flowering in both natural accessions Col-0, C24 and their late flowering hybrid C24xCol, which carries both functional floral repressor FLC and its activator FRIGIDA (FRI), as compared to a constant temperature (CON). The loss-of-function mutation of PIF4 exhibits later flowering in VAR, suggesting that PIF4 at least in part, contributes to acceleration of flowering in response to the daily variable temperature. We find that VAR increases PIF4 transcription at the end of the day when temperature peaks at 32°C. The FT transcription is also elevated in VAR, as compared to CON, in agreement with earlier flowering observed in VAR. In addition, VAR causes a decrease in FLC transcription in 4-week-old plants, and we further show that overexpression of PIF4 can reduce FLC transcription, suggesting that PIF4 might also regulate FT indirectly through the repression of FLC. To further conceptualize an overall model of gene regulatory mechanisms involving PIF4 and FLC in controlling flowering in response to temperature changes, we construct a co-expression - transcriptional regulatory network by combining publicly available transcriptomic data and gene regulatory interactions of our flowering genes of interest and their partners. The network model reveals the conserved and tissue-specific regulatory functions of 62 flowering-time-relating genes, namely PIF4, PIF5, FLC, ELF3 and their immediate neighboring genes, which can be useful for confirming and predicting the functions and regulatory interactions between the key flowering genes.

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“…Four copies of the G-box (CACGTG) cis acting element was identified in the promoter sequences of cAGP4, classical AGP9, and AGP13 indicating contribution in the transcriptional regulation of these genes (Table 1 ). The G-box motif is bound by the large TF superfamilies of basic helix-loop-helix (bHLH) and basic Leu zipper (bZIP) 59 . Expression of two tomato bZIP TFs, SlbZIP1, and SlbZIP2, under the control of the E8 fruit specific promoter were shown to increase the sugar content in tomato fruits 60 , while three tomato SlbHLH genes were associated with fruit ripening 61 and an atypical bHLH TF, SlPRE2, affected plant morphology and pigment accumulation 62 .…”

Section: Discussionmentioning

confidence: 99%

The role of arabinogalactan proteins (AGPs) in fruit ripening—a review

et al. 2020

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Arabinogalactan proteins (AGPs) are proteoglycans challenging researchers for decades. However, despite the extremely interesting polydispersity of their structure and essential application potential, studies of AGPs in fruit are limited, and only a few groups deal with this scientific subject. Here, we summarise the results of pioneering studies on AGPs in fruit tissue with their structure, specific localization pattern, stress factors influencing their presence, and a focus on recent advances. We discuss the properties of AGPs, i.e., binding calcium ions, ability to aggregate, adhesive nature, and crosslinking with other cell wall components that may also be implicated in fruit metabolism. The aim of this review is an attempt to associate well-known features and properties of AGPs with their putative roles in fruit ripening. The putative physiological significance of AGPs might provide additional targets of regulation for fruit developmental programme. A comprehensive understanding of the AGP expression, structure, and untypical features may give new information for agronomic, horticulture, and renewable biomaterial applications.

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The G-Box Transcriptional Regulatory Code in Arabidopsis

Cited by 117 publications

References 80 publications

Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63

Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63

Role of PIF4 and FLC in controlling flowering time under daily variable temperature profile

The role of arabinogalactan proteins (AGPs) in fruit ripening—a review

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