BIG Regulates Dynamic Adjustment of Circadian Period in <i>Arabidopsis thaliana</i>

Hearn, Timothy J.; Ruiz, M. R.; Abdul-Awal, SM; Wimalasekera, Rinukshi; Stanton, Camilla; Haydon, Michael J.; Theodoulou, F. L.; Hannah, Matthew A.; Webb, Alex A. R.

doi:10.1104/pp.18.00571

Cited by 22 publications

(30 citation statements)

References 73 publications

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“…The clock, in its role as master regulator, must balance these two competing requirements. Recently it has been proposed that the clock in plants is dynamically plastic, able to respond to changes in environmental inputs by altering phase and period (54,55). A decentralized structure, with organ specific inputs to clocks that are coupled together, could allow some flexibility in sensing the environment whilst ensuring robust timing.…”

Section: Discussionmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Greenwood

Domijan

Gould

et al. 2019

Preprint

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29Every plant cell has a genetic circuit, the circadian clock, that times key processes 30 to the day-night cycle. These clocks are aligned to the day-night cycle by multiple 31 environmental signals that vary across the plant. How does the plant integrate 32 clock rhythms, both within and between organs, to ensure coordinated timing? 33To address this question, we examined the clock at the sub-tissue level across 34Arabidopsis thaliana seedlings under multiple environmental conditions and 35 genetic backgrounds. Our results show that the clock runs at different speeds 36 (periods) in each organ, which causes the clock to peak at different times across 37 the plant in both constant environmental conditions and light-dark cycles. Closer 38 examination reveals that spatial waves of clock gene expression propagate both 39 within and between organs. Using a combination of modeling and experiment, 40we reveal that these spatial waves are the result of the period differences 41 between organs and local coupling, rather than long distance signaling. With 42 further experiments we show that the endogenous period differences, and thus 43 the spatial waves, are caused by the organ specificity of inputs into the clock. We 44 demonstrate this by modulating periods using light and metabolic signals, as 45 well as with genetic perturbations. Our results reveal that plant clocks are set 46 locally by organ specific inputs, but coordinated globally via spatial waves of 47 clock gene expression. 48 49

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Section: Discussionmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Greenwood

Domijan

Gould

et al. 2019

Preprint

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“…The clock, in its role as master regulator, must balance the competing requirements of flexibility and robustness. Recently, it has been proposed that the clock in plants is dynamically plastic, able to respond to changes in environmental inputs by altering its period and phase [77,78]. Cell-cell coupling increases the synchrony and robustness of oscillations, influencing how easy it is for clocks to entrain to the environment [79].…”

Section: Discussionmentioning

confidence: 99%

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

et al. 2019

View full text Add to dashboard Cite

Individual plant cells have a genetic circuit, the circadian clock, that times key processes to the day-night cycle. These clocks are aligned to the day-night cycle by multiple environmental signals that vary across the plant. How does the plant integrate clock rhythms, both within and between organs, to ensure coordinated timing? To address this question, we examined the clock at the sub-tissue level across Arabidopsis thaliana seedlings under multiple environmental conditions and genetic backgrounds. Our results show that the clock runs at different speeds (periods) in each organ, which causes the clock to peak at different times across the plant in both constant environmental conditions and light-dark (LD) cycles. Closer examination reveals that spatial waves of clock gene expression propagate both within and between organs. Using a combination of modeling and experiment, we reveal that these spatial waves are the result of the period differences between organs and local coupling, rather than long-distance signaling. With further experiments we show that the endogenous period differences, and thus the spatial waves, can be generated by the organ specificity of inputs into the clock. We demonstrate this by modulating periods using light and metabolic signals, as well as with genetic perturbations. Our results reveal that plant clocks can be set locally by organ-specific inputs but coordinated globally via spatial waves of clock gene expression.PLOS Biology | https://doi.org/10.days at near-cellular resolution (Materials and methods). This reporter line was chosen because of its strong expression level and its similar spatial expression to other clock components [5].In order to observe the endogenous component of the rhythms, we first imaged seedlings under LL, having previously grown them under LD cycles (LD-to-LL; Fig 2A and Materials and methods). Under the LD-to-LL condition we observed phase differences of GI::LUC expression between organs ( Fig 2B and 2C). The cotyledon and hypocotyl peaked before the root, but the tip of the root peaked before the middle region of the root (Fig 2C, S1 Fig, and S1 Video). Furthermore, we observed a decrease in coherence between regions over time, with a range between the earliest and latest peaking region of 4.92 ± 3.79 h (mean ± standard deviation) in the first and 18.36 ± 5.67 h in the final oscillation. This is due to the emergence of period differences between all regions ( Fig 2D). The cotyledon maintained a mean period of 23.82 ± 0.60 h, whereas the hypocotyl and root ran at 25.41 ± 0.91 h and 28.04 ± 0.86 h, respectively. However, the root tip ran slightly faster than the middle of the root, with a mean period of 26.90 ± 0.45 h, demonstrating the presence of endogenous period differences across all regions. We verified that our results were not specific to the GI::LUC reporter, as we observed similar differences in periods and phases across the plant using luciferase reporters for promoter activity of the core clock genes PSEUDO-RESPONSE REGULATOR 9 (PRR9) [31], TI...

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“…How BIG can control PCD mediated by the MIPS1 pathway is difficult to decipher because the molecular function of BIG is still unknown. Indeed, the BIG gene encodes a 5078-aa protein with several functional domains and has been implicated in numerous hormonal and light pathways [19][20][21]25,27,32,36 . One hypothesis could have been that the MI content was restored in the mips1 somi2 double mutant.…”

Section: Discussionmentioning

confidence: 99%

“…Other big mutants were subsequently identified, exhibiting a variety of morphological defects and resistance to the auxin's effect on endocytosis 19,20 ; reduced response to cytokinin, ethylene, and gibberellins 21 ; corymb-like inflorescences 22,23 ; or characterized by mis-regulation of mitochondrial stress signalling 24 . BIG has been also described for its involvement in the circadian clock control 25 and in elevated CO 2 -induced stomatal closure 26 . Recently 27 , demonstrated that BIG represents a new regulator of the Jasmonic Acid (JA) pathway and a point of convergence for the interactions of JA and others hormones.…”

mentioning

confidence: 99%

Involvement of Arabidopsis BIG protein in cell death mediated by Myo-inositol homeostasis

Bruggeman

Piron‐Prunier

Tellier

et al. 2020

Sci Rep

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Programmed cell death (PCD) is essential for several aspects of plant life. We previously identified the mips1 mutant of Arabidopsis thaliana, which is deficient for the enzyme catalysing myo-inositol synthesis, and that displays light-dependent formation of lesions on leaves due to Salicylic Acid (SA) over-accumulation. Rationale of this work was to identify novel regulators of plant pcD using a genetic approach. A screen for secondary mutations that abolish the mips1 PCD phenotype identified a mutation in the BIG gene, encoding a factor of unknown molecular function that was previously shown to play pleiotropic roles in plant development and defence. physiological analyses showed that BiG is required for lesion formation in mips1 via SA-dependant signalling. big mutations partly rescued transcriptomic and metabolomics perturbations as stress-related phytohormones homeostasis. in addition, since loss of function of the ceramide synthase LOH2 was not able to abolish cell death induction in mips1, we show that pcD induction is not fully dependent of sphingolipid accumulation as previously suggested. our results provide further insights into the role of the BiG protein in the control of MIPS1-dependent cell death and also into the impact of sphingolipid homeostasis in this pathway. Myo-inositol (MI) is a ubiquitous molecule and the precursor for biosynthesis of many inositol-derivatives such as inositol phosphates, phosphatidylinositol (PtdIns) phosphate, or specific classes of sphingolipids that play critical and diverse roles in vesicle trafficking, hormone signalling, and biotic and abiotic stress responses 1, 2. The rate-limiting step of MI synthesis is catalysed by l-myo-inositol 1-phosphate synthase (MIPS), using Glucose-6-P as a substrate. This reaction is followed by dephosphorylation of l-myo-inositol 1-phosphate into MI. These two reactions together, called the Loewus pathway, are the only known route for MI biosynthesis 3. Three genes encoding MIPS isoforms have been identified in the Arabidopsis genome 4, 5 , among them MIPS1 is responsible for most of MI biosynthesis in leaves. Pleiotropic developmental defects such as reduced root growth or altered venation in cotyledons have been described for the mips1 loss of function mutant 6-8. One of its most striking features is the light intensity-dependent formation of leaf lesions due to Salicylic acid (SA)dependent Programmed Cell Death (PCD), revealing the importance of MI or inositol derivatives in the regulation of these processes. However, how light affects MIPS transcript level and inositol biosynthesis was an open question for a long time until the demonstration that the two light signalling proteins, FAR-RED ELONGATED HYPOCOTYL 3 (FHY3) and its homolog, FAR-RED IMPAIRED RESPONSE 1 (FAR1), were able to directly bind MIPS1 promoter and to activate its expression, thereby promoting inositol biosynthesis to prevent lightinduced SA-dependent cell death 9. Because MI is used to synthetize numerous compounds in the cell, including PtdIns, a link between mip...

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BIG Regulates Dynamic Adjustment of Circadian Period in Arabidopsis thaliana

Cited by 22 publications

References 73 publications

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana

Involvement of Arabidopsis BIG protein in cell death mediated by Myo-inositol homeostasis

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