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First published online September 12, 2008; 10.1104/pp.108.125468 Plant Physiology 148:1681-1694 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Acceleration of Flowering during Shade Avoidance in Arabidopsis Alters the Balance between FLOWERING LOCUS C-Mediated Repression and Photoperiodic Induction of Flowering1,[W],[OA]Graduate Program in Cellular and Molecular Biology, University of Wisconsin, Madison, Wisconsin 53706 (A.C.W.); Fundación Instituto Leloir, 1405 Ciudad de Buenos Aires, Argentina (B.S., P.D.C.); Consejo Nacional de Investigaciones Científicas y Técnicas, Ciudad de Buenos Aires, Argentina (P.D.C.); and Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706 (R.M.A.)
The timing of the floral transition in Arabidopsis (Arabidopsis thaliana) is influenced by a number of environmental signals. Here, we have focused on acceleration of flowering in response to vegetative shade, a condition that is perceived as a decrease in the ratio of red to far-red radiation. We have investigated the contributions of several known flowering-time pathways to this acceleration. The vernalization pathway promotes flowering in response to extended cold via transcriptional repression of the floral inhibitor FLOWERING LOCUS C (FLC); we found that a low red to far-red ratio, unlike cold treatment, lessened the effects of FLC despite continued FLC expression. A low red to far-red ratio required the photoperiod-pathway genes GIGANTEA (GI) and CONSTANS (CO) to fully accelerate flowering in long days and did not promote flowering in short days. Together, these results suggest a model in which far-red enrichment can bypass FLC-mediated late flowering by shifting the balance between FLC-mediated repression and photoperiodic induction of flowering to favor the latter. The extent of this shift was dependent upon environmental parameters, such as the length of far-red exposure. At the molecular level, we found that far-red enrichment generated a phase delay in GI expression and enhanced CO expression and activity at both dawn and dusk. Finally, our analysis of the contribution of PHYTOCHROME AND FLOWERING TIME1 (PFT1) to shade-mediated rapid flowering has led us to suggest a new model for the involvement of PFT1 in light signaling.
As sessile organisms, plants cannot move away from environmental pressures. Evolution has thus favored a flexible developmental plan that allows plants to tailor their growth to particular conditions. This flexibility is reflected not only in variable patterns of vegetative growth but often in variable timing of the floral transition. By adjusting flowering time to maximize seed set in a given environment, a plant optimizes its reproductive and evolutionary success.
The effects of seasonal cues, particularly daylength and temperature, on flowering time have been well studied. Arabidopsis (Arabidopsis thaliana) is a facultative long-day (LD) plant, initiating flowering sooner under longer photoperiods, but eventually flowering under short days as well. Daylength is sensed through an external coincidence mechanism (for review, see Searle and Coupland, 2004
Although most Arabidopsis accessions used for laboratory work do not require a long period of cold (vernalization) to promote rapid flowering, many natural accessions are late flowering even in inductive long days unless they are first vernalized (Napp-Zinn, 1961
In addition to sensing seasonal cues, Arabidopsis is sensitive to the presence of competing plants. The proximity of other plants, either overhead casting direct shade or nearby forecasting future shade, is perceived as a change in light quality. Red wavelengths (
Red and far-red radiation are perceived by PHYTOCHROME (PHY) photoreceptors, which are encoded by a family of five genes (PHYA–PHYE) in Arabidopsis (Sharrock and Quail, 1989
Microarrays and genetic screens have advanced our understanding of the downstream pathways that lead from far-red perception to vegetative shade-avoidance phenotypes (Carabelli et al., 1993
A Low R:FR Ratio Bypasses FLC-Mediated Late Flowering without Lowering FLC Expression
Far-red enrichment is similar to vernalization in that it can promote rapid flowering in lines that are late flowering due to high FLC levels (Martinez-Zapater and Somerville, 1990
FLC belongs to a clade of MADS box genes that repress the floral transition; like FLC, several members of this clade are down-regulated during vernalization (Ratcliffe et al., 2001  , 2003; Scortecci et al., 2001, 2003). We examined mRNA levels of these FLC clade members and of another MADS box transcription factor that represses flowering (SVP) after 2 d of far-red enrichment and found that their transcript levels were unaltered by this exposure (Fig. 1C).
Under both white light and far-red-enriched conditions, the presence of FLC delayed flowering in a dose-dependent manner (Fig. 1A). This indicated that the repressive effects of FLC compete with the promotive effects of a low R:FR ratio despite being eventually bypassed. We tested whether FLC might completely block the far-red-mediated acceleration of flowering during a shorter far-red enrichment, as opposed to the continuous exposure shown in Figure 1A. We grew Col-FRI seedlings either with or without functional FLC for 5 d in low R:FR conditions before shifting them to high R:FR conditions and compared this transient treatment with continuous low or high R:FR conditions. Whereas 5 d of exposure to a low R:FR ratio accelerated flowering to the same degree as continuous far-red enrichment in flc null seedlings, transient exposure did not accelerate flowering in FLC-expressing seedlings (Fig. 1D). Although the flowering behavior of Col-FRI in white light sometimes varied between experiments (Fig. 1, compare A and D), we found that within each experiment, a short period of far-red exposure was insufficient to bypass FLC-mediated repression of flowering. The ability of Col-FRI seedlings to withstand a period of far-red treatment without commitment to flowering may be due to insufficient FT/TSF accumulation in such FLC-expressing plants during a short far-red exposure. Alternatively, it is possible that elevated FLC levels result in a more efficient reduction in FT expression after the removal of the far-red stimulus.
The ability of a low R:FR ratio to promote flowering despite high FLC expression suggested that a reduction in Pfr activity could override FLC-mediated repression. Such a reduction can be generated not only through far-red enrichment but also through mutational loss of PHY genes. We thus introgressed phyB, phyD, and phyE mutations into the Col-FRI background. The phyB;D;E triple mutant suppressed the late flowering of Col-FRI in white light to a similar degree as did our far-red enrichment (Fig. 2, A and B ). As was observed for far-red exposure (Figs. 1C and 2C), the rapid flowering of Col-FRI caused by loss of PHYB, PHYD, and PHYE Pfr was not associated with a decrease in FLC mRNA levels, nor did a combination of loss of PHYB, PHYD, and PHYE and a low R:FR ratio affect FLC mRNA levels (Fig. 2C). Consistent with the induction of FT expression during far-red exposure despite high FLC levels (Figs. 1C and 2C), FT levels were elevated by the loss of PHYB, PHYD, and PHYE despite the continued presence of FLC transcript (Fig. 2C). This again indicates that loss of Pfr function overrides FLC-mediated repression to activate FT expression and accelerate flowering.
GI and CO Are Required for a Robust Rapid-Flowering Response to a Low R:FR Ratio
As presented above, a low R:FR ratio does not appear to cause rapid flowering via the same pathway as does vernalization; rather, it overrides the block on flowering created by high FLC levels. One way to override FLC repression would be to strengthen the photoperiod pathway, because FLC and the photoperiod pathway antagonistically regulate the same downstream targets (Hepworth et al., 2002
We examined the responses of the photoperiod mutants gi-2 and co-9 to a low R:FR ratio. With respect to vegetative shade-avoidance phenotypes such as petiole elongation (Fig. 3A
) and hyponasty (Fig. 3B), the two mutants resembled Col and Col-FRI. However, both mutants displayed an attenuated ability to accelerate flowering in response to low R:FR exposure (Fig. 3C). This attenuation was most striking in a comparison with Col-FRI: whereas gi-2 and co-9 flowered earlier than Col-FRI in white light, they flowered later than Col-FRI in far-red-enriched light. This reversal in relative lateness indicates that the attenuated responses of the photoperiod mutants to far-red enrichment were not simply a by-product of their late-flowering phenotypes in white light but rather a demonstration of the importance of photoperiod pathway signaling in far-red-mediated acceleration of flowering. Because several gi mutants have allele-specific phenotypes (Park et al., 1999
Light-induced degradation of PHYA Pfr results in very low levels of PHYA protein in white light-grown plants (Kircher et al., 2002 ; Sharrock and Clack, 2002), and phyA mutants in Arabidopsis do not have adult phenotypes in continuous white light (Whitelam et al., 1993). Nevertheless, because PHYA may play a greater role during far-red-enriched light/dark cycles and is needed for photoperiod-mediated acceleration of flowering under certain conditions (Johnson et al., 1994; Yanovsky and Kay, 2002; Mockler et al., 2003; Valverde et al., 2004) and in certain species (Weller et al., 1997), we felt it important to assess whether PHYA was required for the CO-mediated rapid-flowering response to the low R:FR ratio in our chambers. The response of phyA was similar to that of the wild type (Fig. 3D), consistent with earlier genetic results showing that PHYA is not required for the early flowering of phyB mutants (Reed et al., 1994; Devlin et al., 1996). We note that the far-red-rich light sources under which phyA mutants are late flowering (e.g. monochromatic far-red, incandescent, or red plus far-red radiation) are also relatively poor in blue light; under such conditions, PHYA may indeed play a larger role in the acceleration of flowering.
The attenuated flowering responses of gi-2 and co-9 mutants grown under low R:FR conditions (Fig. 3C) indicated that a low R:FR ratio accelerates flowering in part by enhancing the ability of GI and CO to promote flowering. CO protein levels are elevated in the phyB mutant, but little is known about the effects of a low R:FR ratio on the well-documented rhythms of GI, CO, and FT expression. Accordingly, we used quantitative reverse transcription (RT)-PCR to measure mRNA abundance in Col seedlings over a diurnal, LD time course both with and without far-red enrichment. We first examined FT abundance over a 5-d time course (Fig. 4A ). Seedlings were exposed to either 5 d of white light or 3 d of far-red-enriched light followed by 2 d of white light (Fig. 4A). FT expression retained a daily rhythm during far-red treatment with a peak at the end of the day, but the extent of the evening induction was much greater in low R:FR conditions. This increase was lost by the first evening after the shift back to white light.
In addition to the evening peak in FT abundance, we detected a morning peak that appeared on the 2nd d of far-red exposure and disappeared gradually upon return to white light. This disappearance was caused by the change in light quality: when seedlings were kept in far-red conditions through the 5th d, the morning peak in FT abundance was maintained (Fig. 4B). Figure 4B also demonstrates that FT levels continued to rise over the 5-d period: both the morning and the evening peaks were approximately 2- to 5-fold higher on the 5th d than on the 2nd d of far-red exposure. Trough FT levels also increased, so that by the 5th d they were three to five times higher than peak FT levels in white light. Neither the morning peak nor the evening peak was present in co-9 mutant seedlings by the 3rd d of far-red exposure (Fig. 4C, compare circles [co-9] with triangles [Col]), indicating that FT induction in response to a low R:FR ratio requires CO and does not occur via a recently proposed CO-independent microRNA pathway (Jung et al., 2007 ).
We examined CO mRNA abundance on the 5th d of far-red treatment (Fig. 4D), a length of exposure that we have shown saturates the flowering response of seedlings with low FLC expression (Fig. 1D). Consistent with previous reports (Suarez-Lopez et al., 2001 Over the time course first described in Figure 4A for FT expression, peak GI levels showed no increase in response to far-red enrichment; instead, peak expression occurred 4 h later in the day (Fig. 4E). This striking delay was apparent on the 1st d of far-red exposure: by 8 h after dawn, GI levels had peaked in white-light-grown seedlings but were still fairly low in far-red-exposed seedlings; by 12 h after dawn, GI levels had dropped in white-light-grown plants but had continued to increase in far-red-exposed plants. When far-red-treated seedlings were shifted back to white light conditions on the 4th d of the time course, the phase of GI expression was rapidly adjusted, so that there was a decrease rather than an increase in GI mRNA abundance between 8 and 12 h after dawn. Seedlings that were exposed to far-red enrichment in short days (8 h of light) showed no change in GI expression even on the 2nd d of far-red treatment (Fig. 4F), indicating that the distinctive far-red-mediated shift in peak GI expression during long days was photoperiod dependent.
Having shown that components of the photoperiod pathway are required for a robust rapid-flowering response to far-red light (Fig. 3) and exhibit altered expression patterns under far-red-enriched conditions (Fig. 4), we wished to investigate the effect of a low R:FR ratio under conditions where the photoperiod pathway is less active: a short day of 8 h of light. Previous short-day (SD) studies have investigated the response to a monochromatic far-red pulse given at dusk, referred to as an end-of-day far-red treatment; such twilight enrichment for far-red wavelengths is thought to be a seasonal cue at high latitudes. In contrast, we examined the response to far-red enrichment provided throughout the light period, a continuous treatment that simulates vegetative shade. A low R:FR ratio that elicited a maximal response in LD conditions (Fig. 3C) did not accelerate flowering during short days in Col, Wassilewskija, or Landsberg erecta (Ler) wild types (Fig. 5
). The phyB;D;E mutant in Col (no functional FRI allele, low FLC expression) did flower early in short days, as was reported previously in Ler (Franklin et al., 2003
Surprisingly, far-red enrichment during SD conditions delayed flowering of the phyB;D;E triple mutant (Fig. 5). This effect was background specific, occurring in the Col phyB;D;E triple mutant but not in the Ler phyB;D;E triple mutant (A.C. Wollenberg and R.M. Amasino, unpublished data). Although we do not yet have a molecular explanation for this result, it indicates that a low R:FR ratio under SD photoperiods activates a floral repressor that is more active in Col than in Ler.
Two conditions often used to simulate shade are short days with end-of-day far-red exposure and the phyB mutant background. pft1 suppresses rapid flowering in both, indicating that PFT1 may promote flowering in response to shade (Cerdan and Chory, 2003
A low R:FR ratio, which is indicative of shady or crowded conditions, promotes flowering in Arabidopsis (for review, see Franklin and Whitelam, 2005 ). We set out to characterize the relationship between far-red-mediated flowering and the pathways that promote flowering in response to vernalization or inductive photoperiods.
Our initial focus was to explore the pathway by which a low R:FR ratio promotes flowering in plants in which FLC levels are elevated by the presence of FRI. Such FLC-expressing plants are likely to display a winter-annual growth habit in many environments, with high FLC levels suppressing flowering prior to vernalization. These lines represent the ancestral genetic state in Arabidopsis; many of the constitutively rapid-flowering accessions were derived via mutations in FRI and/or FLC (Johanson et al., 2000
The ability of far-red enrichment to bypass FLC-mediated late flowering seems to result largely from the removal of the Pfr form of PHYB and its light-stable relatives, as the phyB;D;E triple mutant suppressed the late flowering of Col-FRI in white light to a similar extent as did our far-red enrichment in long days. As was the case with far-red enrichment, acceleration of flowering due to the loss of PHYB, PHYD, and PHYE was not associated with a decrease in FLC mRNA levels. A large number of loss-of-function mutants that suppress FLC-mediated late flowering in winter-annual types have been identified (for review, see Dennis and Peacock, 2007
Having established that a low R:FR ratio accelerates flowering in spite of high FLC levels, we turned our attention to the role of the photoperiod pathway in shade-mediated floral promotion. In our conditions, GI and CO were necessary for a robust rapid-flowering response to far-red enrichment, as indicated by the attenuated flowering responses of gi-2 and co-9. These data are in good agreement with previous reports noting the relative lateness of gi and co mutants grown under incandescent light (Martinez-Zapater and Somerville, 1990
Although photoperiod signaling was necessary for the acceleration of flowering by far-red enrichment in this study, neither LD conditions nor CO is required for rapid flowering of Col and Ler mutants that lack functional PHYB (Goto et al., 1991
Recent models for environmental regulation of flowering time have incorporated a photoperiod-independent pathway, acting through PFT1, that promotes flowering in response to changes in light quality (Cerdan and Chory, 2003
Our results indicate that the photoperiod response, rather than down-regulation of FLC or signaling through PFT1, is important in generating the rapid-flowering response of the SAS. We thus examined the molecular impact of far-red enrichment on the expression of key components of the photoperiod pathway. By examining gene expression over several days of far-red treatment, we demonstrated two new features of the far-red enhancement of CO function. First, peak CO mRNA levels were up-regulated during far-red exposure. There was no increase at times of trough CO levels, which may explain the absence of increased CO mRNA in the phyB mutant at 8 h after dawn (Blazquez and Weigel, 1999 ). Second, we found that CO function (measured by CO-dependent FT induction) was not only enhanced at dusk but also derepressed at dawn. There has been one other report of a large increase in FT levels during the morning in a wild-type background (Corbesier et al., 2007). Intriguingly, this increase was observed after a shift from short days to long days; perhaps morning expression of FT is especially apparent after a sharp transition from noninductive (short days or high R:FR) to inductive (long days or low R:FR) conditions. Surprisingly, a morning peak in FT mRNA abundance is not observed in phyB mutants (Blazquez and Weigel, 1999; Cerdan and Chory, 2003) or phyB;D;E mutants (A.C. Wollenberg and R.M. Amasino, unpublished data) grown in white light. We are currently characterizing the window of far-red exposure necessary to generate this morning peak as well as determining its relevance to floral promotion (see discussion on gating below).
Elevated morning and evening FT expression was observed after a period of far-red exposure that did not generate a consistent increase in CO mRNA levels (A.C. Wollenberg and R.M. Amasino, unpublished data); because this increase in FT abundance was nevertheless dependent upon CO function (Fig. 4C), we favor a model in which enhanced CO protein stabilization occurs rapidly in response to a low R:FR ratio, whereas increased CO expression occurs as a response to more prolonged shade. Although the factors responsible for these far-red-mediated changes in CO regulation are not yet known, there are several candidates. The E3 ubiquitin ligase COP1 promotes the degradation of CO at dusk and during the night and may also contribute to CO degradation in the early morning (Jang et al., 2008
The observed increase in CO transcript levels by the 5th d of far-red exposure may be related to the far-red-mediated phase delay in peak GI expression. A similar phase delay in GI expression was reported when LD-entrained seedlings were shifted into darkness for 1 d (Paltiel et al., 2006
The persistence of diurnal rhythms in GI, CO, and FT expression during far-red enrichment may indicate that a low R:FR ratio can enhance the expression of flowering-time genes only at certain times in the circadian cycle. Such gating of the SAS by the circadian clock has been reported: depending on the response being studied, far-red enrichment is most effective at dawn (Salter et al., 2003
In our model for the promotion of flowering by far-red enrichment (Fig. 7), reduction of Pfr levels under a low R:FR ratio lifts repression of the photoperiod pathway not only via stabilization of the CO protein (Valverde et al., 2004 Regardless of whether FLC protein is inactivated or simply outcompeted during far-red exposure, its repressive abilities are bypassed only when the far-red enrichment is sufficiently strong. In particular, we have demonstrated two scenarios in which a reduction in Pfr that is sufficient to accelerate flowering in the absence of FLC does not promote flowering in FLC-expressing plants. First, a short exposure to far-red enrichment, which was strong enough to elicit a maximal response in flc plants, had no effect on the flowering time of plants with high FLC levels. Second, the phyB;D;E triple mutant accelerated flowering in short days in the Col background (with low FLC expression) but could not do so in a Col-FRI background (with elevated FLC expression). It appears that the extent of rapid flowering in response to vegetative shade is determined not by the presence or absence of a single cue but rather by the cumulative effect of multiple opposing and quantitative influences, including the specific shade treatment and resulting degree of Pfr reduction, the amount of floral repression created by the particular genetic background, and the strength of other environmental cues, such as daylength. By integrating information regarding many different features of the environment, the plant may be better able to modify its rapid-flowering response to shade and thus maximize its fitness.
Plant Material
Unless otherwise noted, all experiments were carried out in the Arabidopsis (Arabidopsis thaliana) Col background. Genotypes and alleles were as follows: Col-FRI (Lee and Amasino, 1995
Arabidopsis seeds were plated on agar-solidified medium as described previously (Schmitz et al., 2005
Plant material for all experiments except those involving semiquantitative RT-PCR (Figs. 1C and 2C) was generated in light/dark cycling reach-in chambers (Percival Scientific I-60LX; 22°C) fitted with T12 fluorescent bulbs (Philips Lighting; R:FR approximately 5, PPFD approximately 60–70 µmol m–2 s–1) set for long days (16 h of light/8 h of dark) or short days (8 h of light/16 h of dark). One shelf of each chamber contained arrays of far-red light-emitting diodes (Plasma Ireland;
Approximately 20 seedlings for each genotype/treatment were frozen in liquid nitrogen. RNA extraction was as described (Abe et al., 2005
For each genotype/treatment, 8 to 12 soil-grown plants were measured. On the 12th day after the shift to low R:FR conditions, the first four true leaves from each plant were removed, taped to paper, and scanned using a flat-bed scanner. The pixel length of each petiole was measured using ImageJ (available at http://rsb.info.nih.gov/ij/) and used to calculate length in millimeters.
The following materials are available in the online version of this article.
We thank Joanne Chory, Stacy Harmer, Enamul Huq, and Jason Reed for the gift of seeds. The 35S::FLC cDNA construct was created by Yuehui He. We are grateful to Bob Gaeta, Stephanie Ellison, and Ginny Powers for reagents and helpful advice regarding the quantitative PCR experiments and to Mark Doyle for critical reading of the manuscript. Received June 27, 2008; accepted September 2, 2008; published September 12, 2008.
1 This work was supported by the College of Agricultural and Life Sciences and the Graduate School of the University of Wisconsin, the National Institutes of Health (grant no. 1R01GM079525), the National Science Foundation (grant no. 0446440), and the GRL Program from the MEST/KICOS. A.C.W. was supported by a fellowship from the National Science Foundation.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Richard M. Amasino (amasino{at}biochem.wisc.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.125468 * Corresponding author; e-mail amasino{at}biochem.wisc.edu.
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max approximately 660 nm) are absorbed by the chlorophyll of surrounding plants, but far-red wavelengths (
