Download Light signals and flowering

Journal of Experimental Botany, Vol. 57, No. 13, pp. 3387–3393, 2006
Major Themes in Flowering Research Special Issue
doi:10.1093/jxb/erl071 Advance Access publication 15 September, 2006
Light signals and flowering
Brian Thomas*
Warwick HRI, University of Warwick, Wellesbourne CV35 9EF, UK
Received 14 March 2006; Accepted 31 May 2006
Abstract
Physiological studies over a long period have shown
that light acts to regulate flowering through the three
main variables of quality, quantity, and duration.
Intensive molecular genetic and genomic studies with
the model plant Arabidopsis have given considerable
insight into the mechanisms involved, particularly
with regard to quality and photoperiod. For photoperiodism light, acting through phytochromes and
cryptochromes, the main photomorphogenetic photoreceptors, acts to entrain and interact with a circadian
rhythm of CONSTANS (CO) expression leading to
transcription of the mobile floral integrator, FLOWERING LOCUS T (FT). The action of phytochromes
and cryptochromes in photoperiodism is augmented
by ZEITLUPE (ZTL) and FLAVIN-BINDING, KELCH REPEAT, F-BOX (FKF1) acting as accessory photoreceptors on entrainment and interaction, respectively.
Light quality acts independently of the circadian
system through Phytochromes B, D, and E to regulate
FT. Light quantity effects, on the other hand, are still
incompletely understood but are likely to be linked
either directly or indirectly to patterns of assimilate
partitioning and resource utilization within the plant.
considered both with regard to light acting directly through
photomorphogenetic mechanisms, or alterations in photosynthetic assimilation or as part of the more complex
regulatory mechanisms of photoperiodism. Much of the
body of literature on physiological studies will be assumed
although it is worth noting that many of the revelations
from recent molecular genetic studies were presaged by
careful whole plant studies. Thus, concepts of photoperiodic control of flowering, based on physiological studies,
envisaged an external coincidence circadian model with
multiple photoreceptors acting in the leaf to generate
a complex mobile flowering signal (Thomas and VincePrue, 1997). The explosion of knowledge and resources in
Arabidopsis thaliana has resulted in much of the fine detail
beneath the model being teased out to confirm and extend
this basic concept. For light to affect a particular biological
process it must be detected through the excitation of a lightabsorbing pigment (or photoreceptor) which then passes on
the light as energy or as a signal through highly refined
regulatory pathways or networks. A consideration of light
signalling is therefore inseparable from a consideration of
the roles of photoreceptors in the process of flowering.
Light and photoperiodism
Key words: Arabidopsis, cryptochrome, flowering, light, photoreceptors, photoperiodism phytochrome.
Introduction
As with almost all aspects of plant development, the
flowering behaviour of higher plants is modified by
environmental signals. Light is foremost among these
environmental signals and can modify flowering in several
different ways. This is not particularly surprising as plants
need to adapt to precise ecological niches defined both
spatially and temporally in terms of a favourable environmental envelope. In this review the action of light is
Daylength is a major regulator of flowering time and allows
sexual reproduction to take place at an appropriate time or
times of the year and helps ensure that flowering is coordinated to enable cross-pollination where this forms part
of the plant’s adaptive strategy. Studies on Arabidopsis
have enabled the framework of understanding, based on
physiological studies over more than half a century, to be
supported by detailed information on the cellular and
molecular genetic processes that give rise to the occurrence
of photoperiodism. It is worth remembering that Arabidopsis is typical of a particular photoperiodic class, namely
a facultative cruciferous, light-dominant, long-day plant
(LDP). This is only one of a range of patterns of response
* E-mail: [email protected]
ª The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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3388 Thomas
that plants show to daylength (Thomas and Vince-Prue,
1997). Resolving the relationship of the Arabidopsis model
to species with contrasting physiological responses, for
example, short-day plants (SDP) is an area that is currently
being addressed by a range of research groups. As these
other species almost always lack the exquisite combination
of genetic properties and resources that make Arabidopsis
such a powerful model, resolving their photoperiodic
mechanisms is a considerable challenge, but will almost
certainly add levels of subtlety and complexity to our
understanding.
Light and clock entrainment
As a starting point for examining the role of light, daylength
measurement will be taken to result from an external
coincidence model based on a circadian clock (Carre,
2001; Yanovsky and Kay, 2002). In this model, light has
two roles. Firstly, it acts to entrain the circadian clock and,
secondly, it interacts with an output from the clock at critical phases to allow or prevent flowering. Reconciliation
of earlier physiological and more recent genetic models has
been achieved through the findings that the clock acts to
establish a rhythm of the CONSTANS (CO) gene expression, at least partially mediated by the flowering time gene
GIGANTEA (GI) (Mizoguchi et al., 2005). CO levels are
high towards the end of a long-day (LD) and the interaction with light results in the transcriptional activation of
FLOWERING LOCUS T (FT) (Kardailsky et al., 1999;
Samach et al., 2000; Yanovsky and Kay, 2002). The
regulation of FT takes place in leaves from which FT
mRNA travels to the apex to interact with FD and initiate
floral development (Huang et al., 2005; Abe et al., 2005;
Wigge et al., 2005).
Much of the basic information on the circadian clock
underlying daylength measurement derives from transgenic
plants using reporters of circadian regulated photosynthetic
genes fused to a luciferase reporter. It is assumed that
essentially the same clock elements will form the basis of
the photoperiodic clock. In general, this is supported by
the fact that under the right conditions mutations that
alter expression of components of the circadian clock alter
flowering time (Somers et al., 1998a; Doyle et al., 2002;
Matsushika et al., 2002; Sato et al., 2002; Yamamoto et al.,
2003). For example, the EARLY FLOWERING 3 mutation
ELF3 exhibits light-dependent arrhythmia of the clock and
the gene product is thought to modulate the action of photoreceptors on the input to the clock. Entrainment of the
circadian clock to cycles of light and darkness involves
the action of multiple photoreceptors. There are five members of the phytochrome gene family in Arabidopsis and
equivalent gene families in other species (Izawa et al.,
2002; Kendrick and Weller, 2004). In Arabidopsis, at least
four of the five PHYTOCHROMES (PHYA, B, D, and E)
and both CRYPTROCHROMES (CRY1,2) have been
shown to contribute input to the clock (Somers et al.,
1998b; Devlin and Kay, 2000). A suite of photoreceptors
acting singly or together enables the clock to be entrained
by light at a range of wavelengths and irradiances. PHYB,
PHYD, and PHYE are primarily responsible for mediating
red light at high irradiances while CRY1 and CRY2
mediate high irradiance blue light. Perception of low
irradiance red and blue light is mediated by PHYA. Devlin
and Kay (2000) also provided evidence that cryptochrome
may act downstream of PHYA on the input to the clock.
Light affects components of the circadian oscillator at
several levels. First, light promotes transcription of the
LATE ELONGATED HYPOCOTYL (LHY), and CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) genes in the
early part of the day (Martinez-Garcia et al., 2000; Kim
et al., 2003). Light also acts through through the effect of
ZEITLUPE (ZTL) to modulate the accumulation of the
TIMING OF CAB1 (TOC1) protein (Somers et al., 2000;
Mas et al., 2003). ZTL containins a LOV domain which is
highly similar to the flavin chromophore binding site in
PHOTOTROPINS, which act as blue light photoreceptors
for phototropism and other orientation responses. ZTL is
also an F-box protein that acts to target specific molecules,
for example, TOC1 for degradation via the 26S proteasome.
Light and the clock output
The multiple effects of light on the timing mechanism that
act to set the phase of the photoperiodic response rhythm
and the separate effects of light acting downstream of the
clock to mediate floral response can be distinguished. As
with light input to the clock, phytochromes, cryptochromes,
and potentially novel photoreceptors all appear to have
a role. All five phytochromes contain identical tetrapyrrole
chromophores (Lagarias and Rapoport, 1980; Kendrick and
Weller, 2004). Mutants or transgenic plants in which
chromophore biosynthesis is impaired, will be incapacitated with regard to all of the functional phytochromes.
Such plants show altered daylength responses, flowering
earlier than wild types in both LDP and SDP ( Montgomery
et al., 2001; Izawa et al., 2002; Sawers et al., 2002)
although, as different phytochromes may have opposing
actions, it is difficult to draw any real significance from this.
PHYA typically acts to detect light rich in far-red in deetiolating seedlings (Whitelam et al., 1993; Weller et al.,
2001). Low irradiance treatments with far-red rich incandescent lamps are routinely given as photoperiod
extension treatments in daylength experiments and found
to be highly effective, implying a potential role for PHYA
in daylength sensing. Supporting evidence for a role for
PHYA in promoting flowering in LDP came from the
action spectrum for flowering in wheat which shows a farred peak similar to the far-red high irradiance response in
dark-grown seedlings and which is mediated by PHYA
(Carr-Smith et al., 1989, 1994). This has been confirmed
Light signals and flowering 3389
and extended by more recent genetic studies. PHYA is
required for normal perception of long days in Arabidopsis
and in the LDP, pea (Johnson et al., 1994; Neff and Chory,
1998; Weller et al., 2001). PHYA acts principally through
the photoperiod pathway as it has no effect on flowering
time under short days. Arabidopsis mutants deficient in
PHYB flower earlier than the wild type in both SD and LD,
but retain sensitivity to daylength (Reed et al., 1994).
PHYB, along with PHYD and PHYE mediates early
flowering in Arabidopsis in response to low red to far-red
ratios (Franklin et al., 2003; Halliday et al., 2003). This
response plays a role in shade avoidance and is distinct
from the role of PHYB in photoperiodism (see section on
Light Quality and Flowering below). By contrast, PHYB is
essential for daylength perception in barley since the
BMDR-1 mutant of Barley, which contains a defective
PHYB is insensitive to photoperiod (Hanumappa et al.,
1999) and similarly the PHYB mutant of pea is aphotoperiodic (Weller et al., 2001).
Cryptochromes are flavoproteins that act as blue light
photoreceptors. The participation of cryptochromes in the
control of flowering in Arabidopsis is consistent with
physiological studies that have shown that blue light has
a promotive effect on flowering for LDP of the Cruciferae
although this is not necessarily true for other families
(Thomas and Vince-Prue, 1997; Runkle and Heins, 2001).
Two members of the cryptochrome gene family (CRY1 and
CRY2) are present in Arabidopsis (Lin and Shalitin, 2003).
CRY2 is thought to be the major blue photoreceptor for
flowering in Arabidopsis (Guo et al., 1998), although cry1
cry2 double mutants flowered earlier in blue light than the
single mutants, indicating that both cryptochromes play
a role to promote flowering (Mockler et al., 1999). CRY1
and CRY 2 act along with PHYA to stabilize CO protein
synthesized towards the end of a LD treatment (Valverde
et al., 2004), which provides a mechanism for an external
coincidence model of day length regulation. There is
evidence that allelic diversity in cryptochromes contribute
to the natural variation in the response of Arabidopsis to
daylength. A QTL for flowering time was accounted for by
an allele of CRY2 (El-Assal et al., 2001) indicating that the
blue light photoreceptor has a significant role in daylength
sensing under natural conditions. The early flowering
phenotype resulted from a single amino acid substitution
that reduces the light-induced turnover of the CRY2 protein
under short photoperiods. There is as yet no physiological
evidence for a specific role for blue light, and by inference,
cryptochromes, in SDP, but this remains to be confirmed in
genetic and comparative genomic studies.
A further novel photoreceptor may play an additional
role in the Arabidopsis photoperiodic mechanism. A
FLAVIN-BINDING, KELCH REPEAT, F-BOX (FKF1)
(Nelson et al., 2000) protein is required to generate peak the
of CO transcription observed towards the end of a long day.
The mRNA is under circadian control and the protein binds
flavin mononucleotide and is photoactive. In addition,
FKF1’s action to regulate CO requires light and it may,
therefore, act as an auxiliary blue light photoreceptor
(Imaizumi et al., 2003). It has been recently shown that
FKF1 controls daily CO expression in part by degrading
CDF1, a repressor of CO transcription, to boost CO
production at the critical point in the photoperiod for long
day sensing (Imaizumi et al., 2005).
Light and short-day plants
The bulk of published information on photoperiodic mechanisms is derived from Arabidopsis, a facultative LDP.
There is accumulating evidence that elements of the LDsensing model also form part of the mechanism in SDP (Liu
et al., 2001; Searle and Coupland, 2004). Genetic analysis
has identified that in species that act as SDPs, common
components to those found in Arabidopsis are involved
in the photoperiodic response. In rice, a SDP, Hd1, an
orthologue of CO, and Hd3a, an orthologue of FT, are
required for flowering in response to short-days (Yano
et al., 2000; Hayama et al., 2003). The relationship
between the CO and FT orthologues is, however, reversed
from that found in Arabidopsis. In rice Hd1 is under
circadian regulation and Hd1 mRNA accumulates towards
the end of the day in LD. Coincidental exposure to light at
this time acts to suppress transcription of Hd3a (Hayama
and Coupland, 2004) and consequently inhibits flowering in LD. Orthologues of CO have been isolated from the
SDP Pharbitis nil and show diurnal regulation of expression (Liu et al., 2001), consistent with a general mechanism for daylength regulation.
A consequence of these opposite actions of CO and
orthologues in different species is that mutants lacking CO
default to late flowering in LDP and early flowering in SDP.
Mutants of FT on the other hand would be expected always
to be late flowering, irrespective of response type. If it is
further assumed that FT is the mobile florigenic signal,
this reversible relationship between CO and FT provides an
explanation for the observations from grafting experiments
that the flowering stimulus is interchangeable between
response types as well as between species and in some
cases, genera (Thomas and Vince-Prue, 1997).
Light quality and flowering
Plants grown under canopy shade conditions or in the
proximity of other plants show a range of responses to the
change in red (R) to far-red (FR) ratio of the ambient light.
This response, known as the shade-avoidance or near
neighbour detection response is characterized by increased
internode extension, reduced leaf area and acceleration of
flowering (Halliday et al., 1994). Many of the characteristics
of the shade avoidance response can be mimicked by a
3390 Thomas
short end-of-day FR treatment, implicating light-stable
phytochrome as the photoregulator. PHYB is a major player
in this response, but there is redundancy with PHYD and
PHYE such that double or triple mutants show increasingly
extreme phenotypes (Halliday et al., 1994; Aukerman
et al., 1997; Devlin et al., 1998, 1999). Mutants in PHYB in
Arabidopsis flower earlier than WT in both LD and SD but
retain a differential response to daylength indicating a lightdependent non-photoperiodic regulatory pathway. Both
light-dependent pathways, photoperiodic and light quality,
act through the regulation of FT. Regulation of FT by PHYB
occurs through the nuclear protein, PHYTOCHROME
AND FLOWERING TIME 1 (PFT1) (Cerdan and Chory,
2003). Another characteristic of this pathway is that the
early flowering phenotype in the absence of PHYB is temperature sensitive (Halliday et al., 2003). As other aspects
of the shade-avoidance response do not show the same
response to temperature, sensitivity lies in a floweringspecific branch of the PHYB signalling pathway.
PHYB acts through FT, implying that the light quality
pathway is leaf-based. This is supported by experiments
with enhancer trap lines that showed suppression of FT
expression by PHYB expressed in mesophyll cells
(Endo et al., 2005). In pea, however, the inhibitory effect of PHYB on flowering was found not to be grafttransmissible, in contrast to the photoperiodic effect of
PHYA (Weller et al., 1997). One difference between pea
and Arabidopsis appears to be that, in pea, a transmissible
inhibitor is linked to the effect of PHYA whereas in
Arabidopsis, control by events in the leaf is mediated
entirely through FT, a floral promoter.
Light quantity responses
While increased light levels are usually accepted as having
a positive effect on flowering, the plant response to light
quantity for flowering is very variable. In a study of 41
herbaceous species, 10 were found to have a facultative
irradiance response while 28 were unaffected (Mattson and
Erwin, 2005). Interestingly, three species in this study had
a negative response to increasing irradiance. In general,
light quantity responses are assumed to be linked to
photosynthesis and the availability of assimilates, the
photoreceptors in this case being chlorophylls and other
photosynthetic pigments. This idea is supported by experiments in which a strong irradiance dependence on
flowering in Brassica campestris could be eliminated
by supplying sucrose (Friend, 1984). Bagnall and King
(2001) found that flowering was delayed under low
irradiance in PHYA mutants, but not at higher irradiances,
and suggested that part of PHYA action was mediated
indirectly through photosynthesis although it is not clear
how such a mechanism might operate.
Light quantity seems to be particularly important during
early development, particularly with herbaceous species
that show a clear juvenile phase (Perilleux and Bernier,
2002). It is proposed that the inability to flower during this
juvenile period is because of a foliar inability to produce
floral signals and/or of the competence of the apex to
respond (Zeevaart, 1985; McDaniel, 1996; McDaniel et al.,
1996). The length of the juvenile phase in photoperiodsensitive plants can be revealed by reciprocal transfers
between permissive and non-permissive daylengths. Such
experiments with Petunia showed that the length of the
Fig. 1. Multiple actions of light affect flowering. The diagram indicates the main targets of light and the photoreceptors involved. Photoperiodic control
involves the entrainment of the circadian rhythm and interaction with the output, primarily through CO to regulate FT. Light acts directly through
phytochromes in the leaf via FT. In addition, light acts indirectly through chlorophyll (Chla/b) via photosynthesis and the availability of assimilates
which are translocated to the apex with FT. (Modified from Thomas B, Carré I, Jackson SD. 2006. Photoperiodism and flowering. In: Jordan BR, ed. The
molecular biology and biotechnology of flowering, 2nd edn. CAB International, 3–25, and reproduced by kind permission of CAB International.)
Light signals and flowering 3391
juvenile phase is prolonged at lower irradiances (Adams,
1999).
What is not clear is the precise molecular mechanisms by
which irradiance, if acting through photosynthetic assimilation, can modify the length of the juvenile phase. It may
well be that assimilates themselves act as part of a complex
flowering signal (Perilleux and Bernier, 2002; Bernier and
Perilleux, 2005) or it may be that the delivery of the mobile
flowering signals such as FT is dependent upon a sufficient
mass flow of assimilates. One factor inhibiting a resolution
of this issue is that the juvenile phase is very short in
Arabidopsis and experimental separation of source–sink
relationships in very young seedlings is difficult to achieve
in a manner that is comparable to the extended juvenile
phase of many herbaceous species.
Conclusions
Physiological studies over a long period have shown that
light acts to regulate flowering through the three main
variables of quality, quantity, and duration (Fig. 1).
Intensive molecular genetic and genomic studies with the
model plant Arabidopsis have given considerable insight
into the mechanisms involved, particularly with regard
to quality and duration. The Arabidopsis model is now
being extended to other plants, including crops and different response types and a range of variations can be
expected to emerge as more studies are undertaken. Light
quantity effects, on the other hand, are still incompletely
understood but are likely to be linked either directly or
indirectly to patterns of assimilate partitioning and resource
utilization within the plant.
Acknowledgements
The author would like to acknowledge support from the Department
for Environment, Food and Rural Affairs (Defra) in preparing this
review.
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