PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock

Dartmouth College, Department of Biological Sciences, Hanover, New Hampshire 03755-3576, USA.
The Plant Cell (Impact Factor: 9.34). 04/2005; 17(3):791-803. DOI: 10.1105/tpc.104.029504
Source: PubMed


Environmental time cues, such as photocycles (light/dark) and thermocycles (warm/cold), synchronize (entrain) endogenous biological clocks to local time. Although much is known about entrainment of the Arabidopsis thaliana clock to photocycles, the determinants of thermoperception and entrainment to thermocycles are not known. The Arabidopsis PSEUDO-RESPONSE REGULATOR (PRR) genes, including the clock component TIMING OF CAB EXPRESSION 1/PRR1, are related to bacterial, fungal, and plant response regulators but lack the conserved Asp that is normally phosphorylated by an upstream sensory kinase. Here, we show that two PRR family members, PRR7 and PRR9, are partially redundant; single prr7-3 or prr9-1 mutants exhibit modest period lengthening, but the prr7-3 prr9-1 double mutant shows dramatic and more than additive period lengthening in the light and becomes arrhythmic in constant darkness. The prr7-3 prr9-1 mutant fails both to maintain an oscillation after entrainment to thermocycles and to reset its clock in response to cold pulses and thus represents an important mutant strongly affected in temperature entrainment in higher plants. We conclude that PRR7 and PRR9 are critical components of a temperature-sensitive circadian system. PRR7 and PRR9 could function in temperature and light input pathways or they could represent elements of an oscillator necessary for the clock to respond to temperature signals.

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    • "Arabidopsis PRR7, an ortholog of rice PRR37, functions as an important component of the circadian clock (Nakamichi et al., 2005; 2007; Salome and McClung, 2005). In monocot plants, such as rice, wheat, barley, and sorghum, natural mutations of PRR37 orthologs affect seasonal or regional adaptation by modulating photoperiod sensitivity and flowering time, to maximize plant survival and grain yield (Beales et al., 2007; Koo et al., 2013; Murphy et al., 2011; Turner et al., 2005). "
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    ABSTRACT: Flowering time (or heading date) is controlled by intrinsic genetic programs in response to environmental cues, such as photoperiod and temperature. Rice, a facultative shortday (SD) plant, flowers early in SD and late in long-day (LD) conditions. Casein kinases (CKs) generally act as positive regulators in many signaling pathways in plants. In rice, Heading date 6 (Hd6) and Hd16 encode CK2α and CKI, respectively, and mainly function to delay flowering time. Additionally, the major LD-dependent floral repressors Hd2/Oryza sativa Pseudo-Response Regulator 37 (OsPRR37; hereafter PRR37) andGhd7 also confer strong photoperiod sensitivity. In floral induction, Hd16 acts upstream of Ghd7 and CKI interacts with and phosphorylates Ghd7. In addition, Hd6 and Hd16 also act upstream of Hd2. However, whether CKI and CK2α directly regulate the function of PRR37 remains unclear. Here, we use in vitro pull-down and in vivo bimolecular fluorescence complementation assays to show that CKI and CK2α interact with PRR37. We further use in vitro kinase assays to show that CKI and CK2α phosphorylate different regions of PRR37. Our results indicate that direct posttranslational modification of PRR37 mediates the genetic interactions between these two protein kinases and PRR37. The significance of CK-mediated phosphorylation for PRR37 and Ghd7 function is discussed.
    Molecules and Cells 11/2014; 38(1). DOI:10.14348/molcells.2015.2254 · 2.09 Impact Factor
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    • "PRR37 is most similar to Arabidopsis PRR7. Arabidopsis PRR5, PRR7, and PRR9 were shown to integrate low temperature signaling with the circadian clock, and it was proposed that they would be involved in both photoperiod and temperature regulation of floral induction [71], [72]. However, mutations in the barley PRR37 were reported to affect only photoperiodic flowering and not the circadian clock, indicative of functional differences between the Arabidopsis PRR7 and the cereal PRR37 genes [73]. "
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    ABSTRACT: Vernalization is a key requirement for the induction of flowering in perennial ryegrass (Lolium perenne L.). The transcriptome of two genotypes with contrasting vernalization requirement was studied during primary (vernalization and short day conditions) and secondary induction (higher temperature and long day conditions) using an RNA-Seq approach. This revealed transcripts with expression profiles indicative of a role in floral induction, both in the promotion and repression of flowering. We observed similarities and specific differences between the two genotypes related to cold response, carbohydrate metabolism, and photoperiod regulation. Components of the photoperiod pathway showed regulation during vernalization, pointing to possible interactions between elements of the photoperiod and vernalization pathways. The results provide a global picture of the processes ongoing during the transition from vegetative to reproductive phase of perennial ryegrass genotypes with and without a vernalization requirement.
    PLoS ONE 09/2014; 9(9):e107365. DOI:10.1371/journal.pone.0107365 · 3.23 Impact Factor
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    • "The Arabidopsis lines prr7-3, prr9-1, prr79 (prr7-3 prr9-1), prr79 CCR2::LUC (Farre et al., 2005), prr7-3 PRR7::HA-PRR7 #151 (Farre and Kay, 2007), 35S::HA-PRR7 #54 (Farre and Kay, 2007), 35S::PRR7 #5 (Farre and Kay, 2007), CCA1ox (35S::CCA1 #34) (Wang and Tobin, 1998), cca1lhy (cca1-11 lhy-21 CS9380; Dong et al., 2011), npq2-1 (Niyogi et al., 1998), fer123 (Ravet et al., 2009) were previously described. The lines prr7 prr9 (prr7,9) and prr7,9 amiR-CCA1-LHY are in the Col-2 CCA1::LUC background (Salome and McClung, 2005). The lines prr57 (prr5-1 prr7-3) and prr579 (prr5-1 prr7-3 prr9-1) were generated by crossing. "
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    ABSTRACT: Up to 30% of the plant transcriptome is circadian regulated in different species. However, we still lack a good understanding of the mechanisms involved in these genome-wide oscillations in gene expression. Here we show that PSEUDO-RESPONSE REGULATOR 7 (PRR7), a central component of the Arabidopsis clock, is directly involved in the repression of master regulators of plant growth, light signaling and stress responses. The expression levels of most PRR7 target genes peak around dawn, in an antiphasic manner to PRR7 protein levels and were repressed by PRR7. These findings indicate that PRR7 is important for cyclic gene expression by repressing the transcription of morning-expressed genes. In particular we found an enrichment in genes involved in abiotic stress responses and in accordance we observed that PRR7 is involved in the oxidative stress response and the regulation of stomata conductance. This article is protected by copyright. All rights reserved.
    The Plant Journal 06/2013; 76(1). DOI:10.1111/tpj.12276 · 5.97 Impact Factor
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