Distinct Light and Clock Modulation of Cytosolic Free Ca2+ Oscillations and Rhythmic<i>CHLOROPHYLL A/B BINDING PROTEIN2</i>Promoter Activity in<i>Arabidopsis</i>

Xu, Xiaodong; Hotta, Carlos Takeshi; Dodd, Antony N.; Love, John; Sharrock, Robert A.; Lee, Young Wha; Xie, Qiguang; Johnson, Carl Hirschie; Webb, Alex A. R.

doi:10.1105/tpc.106.046011

Cited by 78 publications

(97 citation statements)

References 76 publications

(138 reference statements)

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“…However, it is also possible that the genes assessed ( CCR2 and LHY ) and mutant backgrounds ( toc1‐4 and toc1‐10 ) used contribute to the anomaly; toc1‐4 is a null mutant in Col with a stop codon close to the N‐terminus (Para et al ., 2007), while toc1‐10 in Ws has a large deletion after S255 (Locke et al ., 2006). Similarly, toc1‐2 affects the period of both CAB2 promoter activity and cytosolic Ca 2+ rhythms, whereas toc1‐1 only affects CAB2 promoter activity (Xu et al ., 2007). …”

Section: Discussionmentioning

confidence: 99%

Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks

et al. 2016

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Summary Circadian clocks allow the temporal compartmentalization of biological processes. In Arabidopsis, circadian rhythms display organ specificity but the underlying molecular causes have not been identified. We investigated the mechanisms responsible for the similarities and differences between the clocks of mature shoots and roots in constant conditions and in light : dark cycles.We developed an imaging system to monitor clock gene expression in shoots and light‐ or dark‐grown roots, modified a recent mathematical model of the Arabidopsis clock and used this to simulate our new data.We showed that the shoot and root circadian clocks have different rhythmic properties (period and amplitude) and respond differently to light quality. The root clock was entrained by direct exposure to low‐intensity light, even in antiphase to the illumination of shoots. Differences between the clocks were more pronounced in conditions where light was present than in constant darkness, and persisted in the presence of sucrose. We simulated the data successfully by modifying those parameters of a clock model that are related to light inputs.We conclude that differences and similarities between the shoot and root clocks can largely be explained by organ‐specific light inputs. This provides mechanistic insight into the developing field of organ‐specific clocks.

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Section: Discussionmentioning

confidence: 99%

Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks

et al. 2016

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“…There is evidence of tissue-specific circadian behavior; for example, the vascular bundle circadian clock appears to have a different genetic architecture compared with other tissues (Para et al, 2007). We previously reported that in the timing of chlorophyll a/b binding protein expression1-1 mutant the circadian rhythms of [Ca 2+ ] cyt become uncoupled from those of CHLOROPHYLL A/B BINDING PROTEIN2 expression, demonstrating the presence of at least two circadian oscillators running at different speeds (Xu et al, 2007). We speculated that these different circadian oscillators might be located in different cell types (Xu et al, 2007).…”

Section: Localization Of Nycthemeral and Circadian Oscillations Of [Cmentioning

confidence: 99%

“…The daily oscillations of [Ca 2+ ] cyt peak at around 300 nM about 8 h after dawn (Love et al, 2004). The circadian clock and PHYTOCHROME A-, CRYPTOCHROME1-, and CRYPTOCHROME2-dependent signaling pathways drive daily rhythms of [Ca 2+ ] cyt (Dalchau et al, 2010) with cyclic ADP ribose (cADPR) acting as an intermediary Xu et al, 2007).…”

Section: Camentioning

confidence: 99%

“…We previously reported that in the timing of chlorophyll a/b binding protein expression1-1 mutant the circadian rhythms of [Ca 2+ ] cyt become uncoupled from those of CHLOROPHYLL A/B BINDING PROTEIN2 expression, demonstrating the presence of at least two circadian oscillators running at different speeds (Xu et al, 2007). We speculated that these different circadian oscillators might be located in different cell types (Xu et al, 2007). Here, using GAL4 transactivation, we demonstrate that the predominant aequorin signal in the measurement of circadian oscillations of [Ca 2+ ] i arises from the spongy mesophyll (Fig.…”

Section: Localization Of Nycthemeral and Circadian Oscillations Of [Cmentioning

confidence: 99%

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Cell- and Stimulus Type-Specific Intracellular Free Ca2+ Signals in Arabidopsis

2013

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Appropriate stimulus-response coupling requires that each signal induces a characteristic response, distinct from that induced by other signals, and that there is the potential for individual signals to initiate different downstream responses dependent on cell type. How such specificity is encoded in plant signaling is not known. One possibility is that information is encoded in signal transduction pathways to ensure stimulus-and cell type-specific responses. The calcium ion acts as a second messenger in response to mechanical stimulation, hydrogen peroxide, NaCl, and cold in plants and also in circadian timing. We use GAL4 transactivation of aequorin in enhancer trap lines of Arabidopsis (Arabidopsis thaliana) to test the hypothesis that stimulus-and cell-specific information can be encoded in the pattern of dynamic alterations in the concentration of intracellular free Ca 2+ ( ] i dynamics in response to touch, cold, and hydrogen peroxide, which in the case of the latter two signals are common to all cell types tested. GAL4 transactivation of aequorin in specific leaf cell types has allowed us to bypass the technical limitations associated with fluorescent Ca 2+ reporter dyes in chlorophyll-containing tissues to identify the cell-and stimulus-specific complexity of [Ca 2+ ] i dynamics in leaves of Arabidopsis and to determine from which tissues stress-and circadian-regulated [Ca 2+ ] i signals arise. Ca2+ is an important second messenger involved in a wide range of responses in plants (Dodd et al., 2010 (Dodd et al., 2010). However, the utility of fluorescent Ca 2+ indicators in plants has been usually restricted to a few specific cell types, including the guard cells, root hairs, and pollen tubes, because these tissues are low in chlorophyll. In other tissues, chlorophyll fluorescence reduces the signal-to-noise ratio to unacceptable levels. Furthermore, in situ measurements of cytosolic-free Ca 2+ concentration ([Ca 2+

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“…7 On the other hand, the mutant toc1-2 has short period of both rhythms of CAB2 promoter activity and circadian [Ca 2+ ] cyt oscillations (~21 h). 1,7 This allele has a base pair change that results in changes to preferential mRNA splicing, resulting in a truncated protein with only 59 residues. 7 Thus, the mutated CCT domain in toc1-1 might lead to the uncoupling of rhythms of CAB2 promoter activity and circadian [Ca 2+ ] cyt oscillations while the absence of TOC1 in toc1-2 causes the shortening of the period of both rhythms.…”

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confidence: 99%

Are there multiple circadian clocks in plants?

Hotta

Xie³

et al. 2008

Plant Signaling & Behavior

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The plant circadian clock controls a multitude of physiological processes such as photosynthesis, organ and stomatal movements and transition to reproductive growth. A plant clock that is correctly matched to the rhythms in the environment brings about a photosynthetic advantage that results in more chlorophyll, more carbon assimilation and faster growth. 3 One of the first circadian clock mutants to be described in plants was the short period timing of cab1-1 (toc1-1), which was identified using the rhythms of luciferase under a CHLOROPHYLL A/B BINDING PROTEIN2 (CAB2) promoter as a marker for circadian period. 4 Circadian rhythms of both CAB2 promoter activity and cytosolicfree Ca 2+ ([Ca 2+ ] cyt ) oscillations depend on the function of a TOC1, CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL (TOC1/CCA1/LHY) negative feedback loop. 5 In tobacco seedlings, CAB2:luciferase (CAB2:luc) rhythms and circadian [Ca 2+ ] cyt oscillations can be uncoupled in undifferentiated calli. 6 In Arabidopsis, we reported that toc1-1 has different periods of rhythms of CAB2 promoter activity (~21 h) and circadian [Ca 2+ ] cyt oscillations (~24 h). The mutant allele toc1-1 has a base pair change that leads to a full protein that has an amino acid change from Ala to Val in the CCT domain (CONSTANS, CONSTANS-LIKE and TOC1). 7 On the other hand, the mutant toc1-2 has short period of both rhythms of CAB2 promoter activity and circadian [Ca 2+ ] cyt oscillations (~21 h). 1,7 This allele has a base pair change that results in changes to preferential mRNA splicing, resulting in a truncated protein with only 59 residues. 7 Thus, the mutated CCT domain in toc1-1 might lead to the uncoupling of rhythms of CAB2 promoter activity and circadian [Ca 2+ ] cyt oscillations while the absence of TOC1 in toc1-2 causes the shortening of the period of both rhythms. Indeed, zeitlupe-1 (ztl-1) mutants, that have higher levels of TOC1, have long periods of both rhythms of CAB2 promoter activity and circadian [Ca 2+ ] cyt oscillations. 1 The biochemical function of the CCT domain is unknown but it is predicted to play an important role in protein-protein interactions 8 and nuclear localization. 9 One model to explain the period difference of CAB2:luc expression and circadian [Ca 2+ ] cyt oscillation is that the toc1-1 mutation has uncoupled two oscillators in the same cell. Uncoupled oscillators are a predicted outcome of certain mutations in the recently described three-loop mathematical model. 10-11 However, both rhythms of TOC1 and CCA1/LHY expression, which would be in uncoupled oscillators accordingly to the model, are described as short-period in toc1-1. 5 Thus, we have favored the model in which CAB2:luc expression and circadian [Ca 2+ ] cyt oscillation are reporting cell-types with different oscillators that are affected differently by toc1-1.It is possible that TOC1 could interact with a family of cell-type specific proteins. The interaction of TOC1 with each member of the family could be affected differently by the mutation in the...

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Distinct Light and Clock Modulation of Cytosolic Free Ca2+ Oscillations and RhythmicCHLOROPHYLL A/B BINDING PROTEIN2Promoter Activity inArabidopsis

Cited by 78 publications

References 76 publications

Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks

Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks

Cell- and Stimulus Type-Specific Intracellular Free Ca2+ Signals in Arabidopsis

Are there multiple circadian clocks in plants?

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