The Circadian Clock That Controls Gene Expression in Arabidopsis Is Tissue Specific

Abstract

The expression of CHALCONE SYNTHASE (CHS) expression is an important control step in the biosynthesis of flavonoids, which are major photoprotectants in plants. CHS transcription is regulated by endogenous programs and in response to environmental signals. Luciferase reporter gene fusions showed that the CHS promoter is controlled by the circadian clock both in roots and in aerial organs of transgenic Arabidopsis plants. The period of rhythmic CHS expression differs from the previously described rhythm of chlorophyll a/b-binding protein (CAB) gene expression, indicating that CHS is controlled by a distinct circadian clock. The difference in period is maintained in the wild-type Arabidopsis accessions tested and in the de-etiolated 1 and timing of CAB expression 1 mutants. These clock-affecting mutations alter the rhythms of both CAB and CHS markers, indicating that a similar (if not identical) circadian clock mechanism controls these rhythms. The distinct tissue distribution of CAB and CHS expression suggests that the properties of the circadian clock differ among plant tissues. Several animal organs also exhibit heterogeneous circadian properties in culture but are believed to be synchronized in vivo. The fact that differing periods are manifest in intact plants supports our proposal that spatially separated copies of the plant circadian clock are at most weakly coupled, if not functionally independent. This autonomy has apparently permitted tissue-specific specialization of circadian timing.Light is a key environmental signal for plants, regulating gene expression and development (Neff et al., 2000). Changes in fluence rate and light quality can occur unpredictably and rapidly during the day but have an underlying day-night cycle. Plants have evolved a circadian timing system that allows the anticipation of this predictable rhythm. When plants are deprived of environmental time cues and placed in constant ("free running") environmental conditions, circadian rhythms persist with a period of around 24 h, often for many days (Millar, 1999; McClung, 2000;Murtas and Millar, 2000;Johnson, 2001). Within the circadian system of the whole organism, the term "circadian oscillator" has been used to denote the parts of the system responsible for rhythm generation. Light-dark signals entrain the oscillator via input phototransduction pathways, synchronizing its phase with the environmental light-dark cycle and also affecting its period. Rhythmic output from the oscillator controls a large number of physiological processes in plants ( Lumsden and Millar, 1998). The abundance of 2% to 6% of RNA transcripts in Arabidopsis plants was scored as circadian-regulated in two recent microarray analyses, for example (Harmer et al., 2000;Schaffer et al., 2001).The rhythmic expression of chlorophyll a/bbinding protein (CAB or Light-Harvesting Complex [LHCB]) genes has often been used as a marker for circadian regulation in plants (for review, see Fejes and Nagy, 1998), especially using firefly (Photinus pyralis) luciferase (LUC) repor...

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

“…Thain et al . (2002) also observed period shortening in light‐grown roots of a toc1 mutant. These results are in contrast to those of James et al .…”

“…Early work suggested that plant cells contain independent and autonomous copies of the clock (Thain et al ., 2000), although some tissue specificity of period was noted (Thain et al ., 2002). Exposure of seedling roots to LD cycles entrained them independently of shoots (Thain et al ., 2000).…”

Possible Involvement of Leaf Gibberellins in the Clock-Controlled Expression of XSP30, a Gene Encoding a Xylem Sap Lectin, in Cucumber Roots

“…However, a few examples of diurnally oscillating gene expression in roots have been reported. The genes that encode certain enzymes involved in nitrogen fixation are expressed in a diurnal pattern (Lejay et al, 1999;Abd-el Baki et al, 2000), as are the histone H1 and chalcone synthase transcripts (Corlett et al, 1998;Thain et al, 2002). Apart from the report that (A and D), as well as the ratio of the intensity of hybridization to XSP30 and rRNA (B and E).…”

Rapid Assessment of Gene Function in the Circadian Clock Using Artificial MicroRNA in Arabidopsis Mesophyll Protoplasts

“…However, this does not exclude the possibility of additional intercellular regulation or the existence of cell-or tissue-specific clock components (Thain et al, 2002;James et al, 2008). Additional cellbased clock studies may suggest how similarly or differently the protoplast clock functions to that of intact plants.…”