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Floral Responses to Photoperiod Are Correlated with the Timing of Rhythmic Expression Relative to Dawn and Dusk in Arabidopsis

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Floral Responses to Photoperiod Are Correlated with the Timing of Rhythmic Expression Relative to Dawn and Dusk in Arabidopsis Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis Laura C. Roden*†, Hae-Ryong Song*, Stephen Jackson‡, Karl Morris‡, and Isabelle A. Carre*§ *Department of Biological Sciences, University of Warwick, Coventry CV4 9DZ, United Kingdom; and ‡Horticulture Research International, Wellesbourne, Warwick CV35 9EF, United Kingdom Edited by Maarten Koornneef, Wageningen University and Research Centre, Wageningen, The Netherlands, and approved August 2, 2002 (received for review June 19, 2002) Daylength, or photoperiod, is perceived as a seasonal signal for the external signal (light) coincides with a photoinducible phase of control of flowering of many plants. The measurement of day- the circadian cycle (Fig. 1A). The photoinducible phase may be length is thought to be mediated through the interaction of determined by the diurnal oscillation of a key regulator, and the phototransduction pathways with a circadian rhythm, so that rhythmic expression of the flowering time gene CONSTANS flowering is induced (in long-day plants) or repressed (in short-day (CO) has recently been proposed to play such a role in Arabi- plants) when light coincides with a sensitive phase of the circadian dopsis (8). An alternative hypothesis, known as the internal cycle. To test this hypothesis in the facultative long-day plant, coincidence model, suggests that inductive photoperiods may Arabidopsis thaliana, we used varying, non-24-hr light͞dark cycles drive expression of two endogenous rhythms to a more favorable to alter the timing of circadian rhythms of gene expression relative place relationship (Fig. 1B; ref. 7). to dawn and dusk. Effects on circadian rhythms were correlated Arabidopsis thaliana is a facultative long-day plant. Long days with those on flowering times. We show that conditions that are not strictly required for floral induction, but flowering occurs displaced subjective night events, such as expression of the flow- much later under short-day conditions. Recent genetic analyses ering time regulator CONSTANS into the light portion of the cycle, demonstrated that altered function of the circadian clock in this were perceived as longer days. This work demonstrates that the plant correlates with abnormal responses to daylength. For perception of daylength in Arabidopsis relies on adjustments of example, flowering of the short-period mutant timing of cab-1 the phase angle of circadian rhythms relative to the light͞dark (toc1) was not delayed significantly under inhibitory short-day cycle, rather than on the measurement of the absolute duration of conditions (9). The arrhythmic mutants early-flowering 3 (elf3) light and darkness. and late elongated hypocotyl (lhy) were completely insensitive to photoperiod (10, 11). Surprisingly, however, the elf3 mutant flowering ͉ photoperiodism ͉ circadian ͉ CONSTANS flowered much faster and produced considerably fewer leaves than the lhy mutant. Different, short- and long-period alleles of he sexual reproduction of many plants and animals occurs on the gigantea (gi) mutation all delayed flowering under long days Ta seasonal basis and is triggered by changes in daylength, or (12, 13). The lack of direct correlation between alterations of photoperiod. In plants, floral responses to photoperiod vary free-running rhythms and flowering-time phenotypes suggests that some (or perhaps all) of the mutations discussed above widely between species and have been classified into three broad affect flowering time independently of their effects on the clock. categories. Short-day plants are induced to flower when the Consequently, the mechanism by which alterations in circadian photoperiod is shorter than a critical daylength, whereas long- rhythms change perception of photoperiod remains unclear. day plants flower under photoperiods that are longer than The work presented here aimed to test whether photoperiodic their critical daylength; day-neutral plants are insensitive to responses are mediated through external coincidence in Arabi- photoperiod. dopsis. Daylength perception in the external coincidence model Measurement of day- or night-length could, in theory, be relies on the appropriate timing of a photoperiodic response performed by an hourglass-type of timer, measuring time from rhythm relative to the light͞dark cycle. Altered entrainment of either dawn or dusk, or even the relative amounts of light and the circadian clock to environmental light͞dark cycles should, darkness. For example, flowering of cocklebur (Xanthium)is therefore, result in light coinciding with different phases of the essentially determined by the absolute duration of darkness (1, photoperiodic response rhythm and translate into altered flow- 2), and induction of diapause in the aphid Megoura viciae relies ering times. Variable phase relationships of circadian rhythms on measuring time from dusk (3). However, the total duration of relative to dawn and dusk are observed under environmental light or darkness was not the critical factor determining the cycles of different total periods (7). Here, we used this funda- response in other plant and animal species. For example, when mental property of circadian clocks to test the effects of varying Japanese morning glory (Ipomea nil, also described as Pharbitis the phase-angle of gene expression rhythms on the flowering nil) were transferred to extended nights, appropriately timed times of wild-type Arabidopsis plants. night breaks mimicked the effects of long days and inhibited flowering (4). Remarkably, sensitivity to night breaks varied with Materials and Methods a 24-hr period. Gonadal development in birds and induction of Plant Materials and Growth Conditions. For flowering-time exper- diapause in insects also exhibited rhythmic responsiveness to iments, Arabidopsis thaliana ecotype Columbia were sown in a short light signals in constant darkness (3, 5). These and other similar findings (reviewed in ref. 2) suggested that photoperiodic time measurement may involve a circadian This paper was submitted directly (Track II) to the PNAS office. rhythm of responsiveness to light, known as the photoperiodic Abbreviations: xLyD, x hours light͞y hours dark cycle; T cycles, light͞dark cycles of variable response rhythm (6). Two possible mechanisms have been total duration; NH cycles, Nanda–Hamner cycles. proposed, by which a circadian clock might mediate perception †Current address: IACR-Broom’s Barn, Higham, Bury St. Edmunds IP28 6NP, United of photoperiod (7). According to the external coincidence Kingdom. PLANT BIOLOGY model, a photoperiodic response may be induced when an §To whom reprint requests should be addressed. E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.192365599 PNAS ͉ October 1, 2002 ͉ vol. 99 ͉ no. 20 ͉ 13313–13318 Downloaded by guest on October 2, 2021 with the Columbia ecotype. Parallel sets of experiments were carried out with the Ws and Ler ecotypes, with similar results. Detection of CONSTANS mRNA Rhythms. Plants were grown for 10 days under different T cycles, then harvested every 2 hr for a 40-hr period. Total RNA was extracted by using the RNeasy kit (Qiagen, Chatsworth, CA) according to the instructions of the manufacturer. The RNA was treated with RNase-free DNase for 10 min at 37°C, and the DNase was inactivated at 96°C for 10 min. cDNA synthesis was performed on 2 ␮g RNA by using Omni- script reverse transcriptase (Qiagen) and a mixture of oligo-dT and random hexamers, according to the manufacturer’s instruc- tions. The cDNA was diluted 10-fold prior to quantitative PCR. Five microliters were used in each reaction consisting of 2.5 ␮l Fig. 1. Models for the mechanism of photoperiodic timing. (A)Inthe SybrGreen (1͞10,000 dilution), 0.3 ␮l of each CO primer at a external coincidence model, responses may be triggered when light coincides concentration of 10 mM (CO53 and Cooli9; ref. 8), 12.5 ␮lof2ϫ with a photoinducible phase. This photoinducible phase may be determined Platinum Quantitative PCR SuperMix-UDG (Invitrogen) in a by the diurnal pattern of expression of a regulatory molecule, represented by final volume of 25 ␮l. Only 0.1 ␮l of the 18S control primers the solid wavy line. Expression of this molecule is expected to be restricted to (Applied Biosystems) were used for the 18S RT-PCR reactions. the dark period under short days, but to coincide with light under long-day All reactions were performed in triplicate. The reactions were conditions (arrows). (B) In the internal coincidence model, the effect of photoperiod is to alter the phase angle between two endogenous rhythms incubated at 50°C for 3 min for the uracil-N-glycosylase reaction, (represented by the solid and dotted lines). Oscillations in the levels of two then heated to 95°C for 10 min followed by 55 cycles of 10 s at regulatory molecules that require each other for activity may allow a response 95°C, 30 s at 58°C, and 30 s at 72°C. Melt curve analyses (from when brought into coincidence, under long-day conditions, for example. 45 to 95°C) were performed on the end products of the PCR White and black boxes at the top of the diagrams represent periods of light reaction to show that only a single product was being amplified and darkness, respectively. in the PCR reactions. Reactions were optimized so that effi- ciencies were 70% or above. 50% (vol͞vol) compost–vermiculite mixture. Plants were grown Results ͞ at 22°C under the light dark cycles indicated, in cooled incu- LHY and CCR2 as Circadian Phase-Markers. The mechanism
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