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Molecular Interactions Between Flowering Time and

Abiotic Stress Pathways
Chapter in International review of cell and molecular biology · September 2016

DOI: 10.1016/bs.ircmb.2016.07.001
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Molecular Interactions Between

Flowering Time and Abiotic Stress
Pathways
H.J. Park1, W.-Y. Kim1,2, J.M. Pardo3, D.-J. Yun1,*
1
Division of Applied Life Science (BK21plus Program), Plant Molecular Biology and Biotechnology Research
Center, Gyeongsang National University, Jinju, South Korea
2
Institute of Agriculture & Life Sciences, Graduate School of Gyeongsang National University, Jinju,
South Korea
3
Instituto de Recursos Naturales y Agrobiologı́a, Consejo Superior de Investigaciones Cientı́ficas, Sevilla, Spain
*Corresponding author. E-mail address: djyun@gnu.ac.kr
Contents
1. Introduction 2
2. Developmental and Seasonal Control of Flowering Time 3
3. Key Molecular Regulators of Flowering Time 5
4. Abiotic Stresses Affecting Flowering Time 7
4.1 Temperature 8
4.2 Drought and ABA 10
4.3 Salinity 10
4.4 Nutrients 12
5. Stress-Signal Integration by Major Flowering Time Regulators 14
5.1 FLC Integrating Cold and ABA Into Autonomous and Vernalization Pathways 14
5.2 CO Integrating Light Signaling and Photoperiod Pathways With Salt 17
and Cold Stresses
5.3 DELLAs Integrating GA Regulation of Flowering With Salt and Cold Stresses 19
5.4 GI Integrating Photoperiod With Drought, Cold, and Salt Stresses 21
6. Role of GI in Influencing Flowering Time and Circadian Clock Components 26
7. Conclusions 29
Acknowledgments 30
References 30
Abstract
Plants have adapted to environmental changes and stresses over generations. The
decision of transition from the vegetative to reproductive stage is critical, particularly
under unfavorable conditions. Thus, plants appear to have developed mechanisms by
which environmental factors or inputs are transmitted to stress response signaling
International Review of Cell and Molecular Biology,

ISSN 1937-6448 © 2016 Elsevier Inc.
http://dx.doi.org/10.1016/bs.ircmb.2016.07.001 All rights reserved. 1
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2 H.J. Park et al.
pathways to confer tolerance and are simultaneously integrated into flowering reg-
ulation pathways (photoperiod, vernalization, autonomous, and gibberellic acid sig-
naling) to propagate the next generation. In this review, we summarize how abiotic
stresses influence, induce, or delay flowering time, particularly in the long-day plant
Arabidopsis. Four major modes including FLOWERING LOCUS C (FLC), CONSTANS (CO),
DELLA, and GIGANTEA (GI), which serve as hubs that integrate stress signals for
regulating flowering time, are introduced. GI, a mediator of the photoperiod floral
pathway and circadian clock, is involved in various biological processes and thus
controls stress response directly through interaction with stress-responsive compo-
nents and indirectly through association with circadian clock components.
1. INTRODUCTION
Plants species, primarily crops, most of which originated in the sub-

tropical areas of the earth, have had to adjust to changes in the environment
over geological times or adapt to niche environments characterized by
extreme, unfavorable conditions for survival. They have evolved to thrive
in a range of geographical latitudes under different light intensities and
periods as well as different temperatures, humidity levels, and soil types.
The seasonal progression that includes changes in day length and weather
guides the duration of the vegetative growth phase and onset of flowering,
seed or fruit setting, and fruit ripening.
Successful seed production ensures the persistence of a plant species; thus,
flowering is tightly controlled by a combination of developmental and
environmental cues that are integrated and relayed by ad hoc regulatory
routes known as flowering pathways (Amasino and Michaels, 2010).
Endogenous or autonomous pathways control flowering time independently
of environmental signals and are related to the developmental stage and age of
the plant. Annual plants can flower shortly after producing a few leaves,
whereas perennials can have a long juvenile phase in which they are not
competent to flower despite receiving inductive environmental input that
would otherwise promote flowering. In a broad sense, the role of the auton-
omous pathway is to prevent precocious flowering and act as a rheostat that
determines the capacity of plants to respond to environmental cues that
promote flowering (Andres and Coupland, 2012; Simpson, 2004).
In ecological terms, the main outcome of vegetative growth is the tran-
sition to the reproductive stage and production of the next generation of
plants. However, plants are endowed with a remarkable developmental
plasticity that allows them to modify flowering time in response to
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Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 3
environmental cues to ensure successful reproduction. In this review, we will

summarize how the environmental or abiotic stresses affect the flowering
time, especially in Arabidopsis model plant, and how the signals are integrated
to floral pathway to regulate the flowering time.
2. DEVELOPMENTAL AND SEASONAL CONTROL OF

FLOWERING TIME
Among the many environmental stimuli that plants are subjected to,
variation in day length (transition from long summer days to short winter
days and vice versa) is the most reliable input that plants can use to anticipate
forthcoming seasonal changes. Consequently, plants measure day length to
decide on flowering time and initiate the transition from the vegetative
to reproductive stage. Moreover, daily light–darkness cycles entrain plants
to synchronize numerous physiological processes to day length. An internal
biological clock, the circadian clock, is the basis of this photoperiodism. This
clock is also a known prerequisite for plants to cope with changing light
and temperature environments and to sustain several biological functions.
The integration of light and circadian inputs constitutes the photoperiodic
pathway of flowering. Seasonal ambient temperature also fluctuates consis-
tently in temperate zones, and many plant species use this additional envi-
ronmental input to distinguish between spring and fall, thereby flowering at
their preferred season. For instance, ecotypes of the facultative long-day
(LD) plant Arabidopsis become competent to flower after being exposed to
prolonged cold temperature in winter. The signaling event involved in this
cold-induced developmental transition to flowering is known as the vernal-
ization pathway. In Arabidopsis, these three major pathways (autonomous,
photoperiodic, and vernalization) controlling flowering time interact in such
a manner that the autonomous pathway prevents flowering during the
vegetative growth phase by repressing floral induction despite day length
(Fig. 1). In winter, the cold-induced vernalization pathway represses the
expression of critical components of the autonomous pathway, thereby
relieving the inhibition of flowering, which nonetheless will not proceed
until long days activate the photoperiodic pathway that promotes flowering.
Repression of the autonomous pathway by the vernalization pathway is
epigenetic; thus, gene silencing is maintained through mitotic cell divisions
until the epigenetic imprinting is reset during meiosis; this reestablishes the
default repression of flowering by the autonomous pathway in the next
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4 H.J. Park et al.
[(Figure_1)TD$IG]
Photoperiod
ROS
GI
UV
Gibberellic acid Salt Vernalization
ABA
Cold
Drought CO
FLC Autonomous
?
Floral integrators
Meristem identity genes
Figure 1 Environmental stresses affect flowering time in Arabidopsis. Flowering time

or transition to flowering is regulated by the interplay of environmental inputs and
autonomous elements. The signals from different pathways are integrated by floral
pathway integrators (SOC1, FT, and LFY), which then activate floral meristem identity
genes, including LFY and AP1. When plants are exposed to various environmental
stresses, including cold, light, reactive oxygen species, and salinity, flowering timing is
influenced (in grey). The positive and negative regulatory components are presented as
arrows and bars, respectively.
generation of plants. Thus, vernalization is a cold-mediated epigenetic

switch that prevents floral transition in the fall season but permits flowering
in the following spring (Fig. 1).
Recent research has shown that in addition to the well-characterized
pathways described earlier, plants have the ability to adjust the duration of
various phases of growth such as the vegetative phase, days to flowering, and
duration of seed development in response to environmental (abiotic) stresses.
This tuning allows them to protect vulnerable growth phases from harsh or
stressful environments (Sunkar et al., 2007). Damage caused during the
flowering phase of a plant is irreversible and can cause reproductive failure
(Sunkar et al., 2007). Thus, alteration of flowering time is often observed in
stressful environments as a compensatory mechanism (Wada and Takeno,
2010). The number of flowers as well as inflorescence architecture can
be altered, leading to reduced seed production. This enables the plant to
efficiently use its resources to produce at least a few viable seeds. Since the
physiology of the plant is largely controlled by the circadian clock, the clock
is associated with the plant’s ability to cope with environmental stresses.
Flowering time is an important trait in breeding for crop performance in
different environments (Jung and Müller, 2009). In addition, flowering time
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loci have been associated with quantitative trait loci (QTLs) for tolerance to
drought or cold stress (Ducrocq et al., 2008; Sehgal et al., 2012), and salt stress
responses share signaling pathways with cold, drought, and ABA signaling
pathways (Han et al., 2013; Wuriyanghan et al., 2009; Ying et al., 2014).
Thus, understanding the molecular mechanisms by which plants connect the
response to abiotic stresses such as salinity or cold with developmental
decisions associated with flowering is of fundamental interest. Here we
integrate recent insights into the ways in which plant responses to abiotic
stresses are associated with flowering time regulation, particularly through
GIGANTEA (GI), a photoperiodic flowering pathway and circadian clock
regulator in Arabidopsis.
3. KEY MOLECULAR REGULATORS OF FLOWERING TIME
A comprehensive coverage of all molecular constituents of pathways

controlling flowering time lies outside the scope of this review. Recent
reviews of the intricate regulatory networks leading to flowering include
those by Andres and Coupland (2012) and Johansson and Staiger (2015).
Here we will briefly describe the interplay between critical signal transmit-
ters that act in the various pathways that control flowering time in the model
plant Arabidopsis and that, as we show later, integrate environmental stress
inputs to modify flowering time (Fig. 1).
After a period of vegetative growth, plants initiate flowering via a
developmental switch by which the shoot apical meristem (SAM) starts
to produce flowers instead of leaves. The formation of flowers requires the
activation of the floral meristem identity genes, including LEAFY (LFY)
and APETALA1 (AP1). As explained earlier, flowering time is regulated by
day length (photoperiod pathway), prolonged periods of cold (vernaliza-
tion pathway), the autonomous pathway, and hormonal inputs involving
gibberellic acid (GA), or gibberellin, a growth regulator that promotes
flowering (GA pathway) (Fig. 1) (Putterill et al., 2004). Signals transduced
from these inputs converge to modulate the expression of the floral inte-
gration genes SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1)
and FLOWERINGLOCUST (FT) that act in concert to initiate flowering
by activating the floral identity genes LFY and AP1 (Putterill et al., 2004).
Similar to many crop plants, Arabidopsis is an LD plant. Thus, Arabidopsis
plants bloom as days lengthen and when exposed to light for more than 12 h.
The LD photoperiod and the circadian clock promote flowering through the
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6 H.J. Park et al.
transcription factor CONSTANS (CO). The circadian clock and factors

involved in light perception regulate CO transcript levels (Sawa et al.,
2007). The precise timing of the expression of CO is necessary for day length
discrimination and photoperiodic flowering. CO transcripts are the highest
during daytime during long days when CO protein is stable, considering that
CO is rapidly degraded in the dark by the ubiquitination and proteasome
degradation machineries (Jang et al., 2008). The accumulation of the CO
protein results in the sequential transcriptional induction of the floral inte-
grator genes FT and SOC1. FT, a small mobile protein produced in leaves
under inductive photoperiods, moves to SAM to promote flower formation
together with SOC1, which is locally produced in response to FT accumu-
lation. A major player in the circadian clock maintenance and elicitation of
photoperiod-dependent flowering is the plant-specific protein GI. GI con-
trols flowering mainly by positively regulating the time of day during which
CO and the floral integrator FT are expressed. In addition, both GI gene
expression and GI protein abundance are regulated by the clock, such that GI
levels peak toward the middle of the day during long days. The GI protein
forms a complex with the F-box E3 ubiquitin ligase FLAVIN-BINDING,
KELCH REPEAT, F-BOX 1 (FKF1) to mediate the degradation of
CYCLING DOF FACTORs (CDFs), which are repressors of CO and FT
transcription (Fornara et al., 2009; Sawa et al., 2007).
Vernalization promotes flowering through negative regulation of the
expression of the transcriptional repressor FLOWERING LOCUS C
(FLC), which suppresses the transcription of the floral integrator genes
SOC1 and FT (Hepworth et al., 2002; Johanson et al., 2000; Michaels
and Amasino, 2001). Repression of FLC by the vernalization pathways
involves gene silencing by repressive chromatin-modifying complexes, lead-
ing to histone methylation. The autonomous pathway comprises a combi-
nation of factors involved in RNA processing and epigenetic regulation,
which also downregulate the transcription of the floral repressor FLC to
ensure developmental commitment to flowering, irrespective of day length
or temperature. Accordingly, the expression of components of the autono-
mous pathway is not affected by these environmental inputs (Simpson,
2004). Loss-of-function mutants in the autonomous flowering pathway
exhibit the overexpression of FLC, resulting in late flowering; however,
the mechanisms regulating FLC differ from those operating in vernalization
(Simpson, 2004).
GA promotes the expression of floral integrators such as FT and TWIN
SISTER OF FT (TSF) independently of CO and GI under long days
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(Porri et al., 2012), but GA function is more critical during short days
because mutants defective in GA biosynthesis and signaling, such as ga1-3,
fail to flower under short-day conditions (Wilson et al., 1992). Two negative
regulators of GA signaling, SPINDLY (SPY) and DELLA proteins, regulate
flowering. Loss-of-function DELLA mutants show early flowering under LD
conditions (Galvão et al., 2012). The spy-4 mutation suppresses the delayed
flowering phenotype of gi-2 mutants by restoring transcript levels of CO and
FT, indicating a genetic interaction between SPY and GI (Tseng et al., 2004).
4. ABIOTIC STRESSES AFFECTING FLOWERING TIME
The standard view holds that under stress, plants accelerate the
transition to the reproductive stage to ensure seed production, albeit with
fewer progeny than what the plant could produce under nonstress condi-
tions (Table 1). This stress-induced flowering has a biological benefit as it
ensures next-generation progeny (Wada and Takeno, 2010). Indeed, high
Table 1 Stress-induced flowering.

Plant species Stress factors References
Arabidopsis thaliana Salicylic acid Martı́nez et al. (2004)
(long-day plant) Wada et al. (2010)
High temperature Balasubramanian et al.
(2006)
Low nitrate Castro Marı́n et al. (2011)
ROS He et al. (2004)
Spoel and van Ooijen
(2014)
Pharbitis nil/Japanese morning Poor nutrition Shinozaki et al. (1988)
glory (short-day plant) Wada et al. (2010)
Low temperature Ishimaru et al. (1996)
High-irradiance Shinozaki et al. (1994)
condition
Lemna paucicostata/duckweed Drought, osmotic, Shimakawa et al. (2012)
(short-day plant) heat stress Takimoto et al. (1994)
Citruslatifolia/Tahiti lime Water stress and Southwick and Davenport
low temperature (1986)
Glycine max/soybean; Triticum Drought Desclaux and Roumet
aestivum/wheat; Hordeum (1996)
vulgare/barley McMaster and Wilhelm
(2003)
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8 H.J. Park et al.
temperature, low nitrate concentration, and presence of salicylic acid (SA)

and reactive oxygen species (ROS) promote the flowering of Arabidopsis
during long days (Balasubramanian et al., 2006; Castro Marı́n et al.,
2011; He et al., 2004; Martı́nez et al., 2004; Spoel and van Ooijen,
2014; Wada et al., 2010). Japanese morning glory (Pharbitis nil) and duck-
weed (Lemna paucicostata), which are short-day plants, flower early under
unfavorable conditions such as low temperature and drought (Ishimaru
et al., 1996; Shimakawa et al., 2012; Takimoto et al., 1994). However,
the reality is far more complex, and various stresses can promote either
early or delayed flowering depending on the species and environmental
conditions (Wada and Takeno, 2010). For example, drought delays flower-
ing in maize (Zea mays L.), rice (Oryza sativa L.), and quinoa (Chenopodium
quinoa Wild.) (Abrecht and Carberry, 1993; Geerts et al., 2008), whereas
it hastens flowering in soybean (Glycinemax L.), wheat (Triticumaestivum L.),
and barley (Hordeum vulgare L.) (Desclaux and Roumet, 1996; McMaster
and Wilhelm, 2003).
In addition, stress tolerance in vegetative and reproductive tissues or
stages is not always correlated (Salem et al., 2007). For instance, during
the vegetative growth phase, wheat and barley can acclimatize to cold when
exposed to nonfreezing low temperatures and can thus survive in extremely
cold winter. However, the capacity for acclimation is reduced toward the
reproductive phase (Fowler et al., 2001; Limin and Fowler, 2006). Many
flowering time loci have been found to be associated with QTLs for toler-
ance or resistance to abiotic stresses such as drought or cold (Ducrocq et al.,
2008; Sehgal et al., 2012), and mutations in genes that encode the flowering
time regulators confer altered stress-tolerant phenotypes.
4.1 Temperature
High temperature can delay flowering in Brachypodium distachyon (Boden
et al., 2013). Furthermore, heat, particularly in the hot summer season or
high temperatures at night, delays flowering, particularly in commercial
horticultural short-day plants such as chrysanthemum (Wang et al., 2008),
poinsettia (Schnelle et al., 2006), and okra (Tenga and Ormrod, 1985).
In the LD plant Arabidopsis, high temperature (27°C instead of 23°C)
even under short-day conditions induces early flowering (Balasubramanian
et al., 2006). This process involves the MADS-box transcription factors
SHORT VEGETATIVE PHASE (SVP), FLOWERING LOCUS M (FLM),
and FT (Balasubramanian et al., 2006; Pose et al., 2013). SVP is a floral
repressor of FT (Lee et al., 2007). The lower temperature–induced late
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flowering cannot be found in svp mutants. Instead, svp mutants flower early,
particularly at 16°C, and SVP overexpressors flower late, particularly at
23°C, by direct binding of SVP to the FT promoter region, repressing FT
transcription (Lee et al., 2007). FLM is subject to temperature-dependent
alternative splicing, and the two splice variants FLM-β and FLM-δ compete
to interact with the floral repressor SVP. FLM-β is the prevalent splice variant
at 16°C, whereas FLM-δ dominates at 27°C (Balasubramanian et al., 2006;
Pose et al., 2013). At lower temperatures, SVP–FLM-β is dominant, result-
ing in repressed flowering, whereas at higher temperatures, FLM-δ in the
SVP–FLM-δ complex does not allow SVP to bind to the promoter of
SEPALLATA3 (SEP3)/AGAMOUS-like MADS-box transcription factor
AGL9 (Balasubramanian et al., 2006; Gregis et al., 2009; Pose et al., 2013).
Although at high temperature (27°C), Arabidopsis flowers earlier
(Balasubramanian et al., 2006), at lower temperature (16°C), its flowering is
delayed compared with the flowering time at 23°C in LD conditions
(Blazquez et al., 2003). Delayed flowering in response to lower temperature
involves autonomous pathway genes such as FCA and FVE (Ausin et al., 2004;
Blazquez et al., 2003; He et al., 2003). fac-1 and fve-1 mutants flower at a
similar time at 23 and 16°C, respectively, suggesting that these two genes are
involved in temperature-regulated flowering. FCA is a nuclear RNA-binding
protein regulating mRNA 3’ polyadenylation and splicing (Quesada et al.,
2003), and FVE is a component of the histone deacetylase (HDAC) complex
(Ausin et al., 2004; Jeon and Kim, 2011). FCA pre-mRNA undergoes
transcriptional and posttranscriptional processes with alternative polyadenyla-
tion and alternative splicing. The fully spliced FCA-γ transcript is functional
for flowering time regulation (Quesada et al., 2003), and functional FCA-γ
and its protein are more abundant at 23°C than at 16°C (Jeon and Kim, 2011).
Heat-inducible HEAT SHOCK PROTEIN 101 (HSP101), which is
required for thermotolerance (Hong and Vierling, 2001; Queitsch et al.,
2000), is also involved in flowering time and inflorescence number (Tonsor
et al., 2008), although the underlying mechanism remains unknown.
lov1-1D, a gain-of-function mutation in LONG VEGETATIVE PHASE,
NAC (NAM, ATAF1/2, and CUC2)-domain transcription factor, and
LOV1 overexpressors exhibit late flowering only in long days and are hyper-
sensitive to freezing temperature (Yoo et al., 2007). LOV1 delays flowering
time by negatively regulating CO in a GI-independent manner, and cold
tolerance is conferred by the upregulation of cold stress response genes such
as COR15a and KIN1, without affecting the expression of CBF/DREB1
(Yoo et al., 2007).
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10 H.J. Park et al.
Plants with loss-of-function mutation in HIGH EXPRESSION OF

OSMOTICALLY RESPONSE1 (HOS1), which is a RING E3 ligase and
negative regulator of cold response, flower earlier than the wild-type as a
result of reduced FLC expression and higher abundance of CO protein under
cold conditions (Lee et al., 2001; Lazaro et al., 2012; Jung et al., 2012, 2013)
(for details, see Section 5.2).
4.2 Drought and ABA

Drought delays flowering and influences the development of reproductive
organs and flowering by affecting the expression of genes involved in stress
response and development in Arabidopsis (Su et al., 2013). Interestingly, a
study of natural variation in drought stress response of 324 Arabidopsis natural
accessions has shown that summer annuals that flower within 75 days in long
days or early-flowering accessions are more drought-tolerant than winter
annuals (Bac-Molenaar et al., 2016). However, considering that early-flow-
ering accessions have larger rosettes, the genetic relationships among plant
size, flowering time, and drought should be taken into account (Bac-
Molenaar et al., 2016).
FLOWERING BHLH (FBH) proteins are CO transcriptional activators
that act by binding to the E-box cis-elements in the CO promoter
(Ito et al., 2012) and are subject to SUCROSE NONFERMENTING1
(SNF1)-related kinase2 (SnRK2)-mediated phosphorylation upon ABA treat-
ment (Wang et al., 2013a). EMPFINDLICHER IM DUNKELROTEN
LICHT1 (EID1)-like protein3 (EDL3), whose expression is induced upon
osmotic stress, high salinity, and ABA treatment, increases the transcription of
CO (Koops et al., 2011). These findings suggest the involvement of ABA in
CO-mediated flowering under drought stress.
4.3 Salinity
Salinity stress not only impairs plant growth but also delays flowering in many
species such as chickpea (Cicerarietinum L.) (Pushpavalli et al., 2015) and iris
(Iris hexagona) (Zandt and Mopper, 2002). Salt also affects the number of
inflorescences. For example, flowering time of Atlantic sea fennel (Crithmum
maritimum) was not significantly affected by salt treatment, but the number
of inflorescences decreased with salt concentration (Ventura et al., 2014).
The number of flowers of chamomile (Matricaria chamomile L.) have been
shown to decrease under salinity and drought, reducing flower weight
and essential oil production (Razmjoo et al., 2008). In addition, salt and
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dehydration stresses reduce the size of flowers in ornamental crops

(Bahadoran and Salehi, 2015).
In Arabidopsis, salt treatment reduces the expression of LFY, SOC1, FT,
and CO in a dose-dependent manner, resulting in late bolting, although a
low (up to 75 mM) concentration of NaCl did not delay the late flowering
time of co-2, whereas high salt concentration (100 mM) did (Li et al., 2007).
CO appears to be involved in salt-delayed flowering as early flowering of a
CO-overexpressing transgenic plant was not changed under salinity.
Application of exogenous GA could restore salt-induced late flowering,
suggesting crosstalk between a salinity stress-delayed CO/FT module and
GA-mediated flowering. In contrast, similarly to wild-type plants, the
expression of FLC, a floral repressor was enhanced and the flowering in
the £c mutant was delayed under high salt conditions, indicating that salinity
does not directly affect the high expression of FLC. Moreover, flowering of
fca-1, which is a mutant of FCA, an autonomous pathway floral regulator
acting upstream of FLC, was not affected (Li et al., 2007).
BROTHER OF FT AND TFL1 (BET), a member of the FT/
TERMINAL FLOWER1 (TFL1) family, delays flowering, and its expres-
sion is induced by abiotic stresses such as ABA, drought, and osmotic stress
(Chung et al., 2010; Yoo et al., 2010). Salt-delayed flowering did not occur
in a BFT-deficient mutant (Ryu et al., 2011). Moreover, fd-2, a loss-of-
function mutant of FD, was insensitive to high salt. BFT interacted with
the C terminus of FD, which is required for interaction with FT; thus, BFT
competes with FT to interact with FD and inhibits the formation of the
FT–FD complex (Ryu et al., 2014). Interestingly, ABA- and/or drought-
induced BET transcription seems to involve GI during both long and short
days as BFT diurnal expression was lost in a gi-2 mutant (Chung et al., 2010).
In the case of Arabidopsis, abiotic stresses, including salinity, cold, and
drought stresses, delay flowering (Li et al., 2007). However, halophytes
naturally grow in, or even require, environments with elevated or high
NaCl (>200 mM) (Flowers et al., 2010). The halophytes include some model
species such as Atriplex (A. vesicaria, saltbush), Salicornia (S. europaea, glasswort),
Mesembryanthemum (M. crystallinum, common ice plant), Rhizophora (R. stylosa,
red mangrove), and Suaeda (S.maritima), that can grow in concentrations of up
to 1 M NaCl (Ushakova et al., 2005). The Arabidopsis relativesThellungiella sal-
suginea and Schrenkiella parvula (formerly Thellungiella parvula) flower earlier
when grown under high Na+ concentrations, strongly suggesting that delayed
flowering in a high Na+ environment is genetically controlled (Andres and
Coupland, 2012).
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12 H.J. Park et al.
4.4 Nutrients
Although the effects of sugar on flowering time have been studied, the
regulatory explanation is unclear. Furthermore, sugar promotes flowering
in some but not in other plants, depending on species, genotype, and
growth conditions (Gibson, 2005). Exogenous sucrose promotes flower-
ing; even in dark growth conditions, sucrose treatment can promote flow-
ering of late-flowering mutations in autonomous and LD-dependent
photoperiodic pathways, for example, fca and fve and co-3 and gi-3 but
not ft (Roldán et al., 1999).
Trehalose-6-phosphate (T6P), which is synthesized from glucose-6-
phosphate and UDP-glucose by trehalose-6-phosphate synthase (TPS) and
is converted to trehalose by trehalose-6-phosphatephosphatase (TPP), plays
various roles in sugar metabolism and plant development (Tsai and
Gazzarrini, 2014). A mutant defective in T6P synthesis is late flowering
during long days, owing to the low expression of FT but not of CO
(Gómez et al., 2010; Wahl et al., 2013). The expression of FT at the end
of the day is decreased in plants with lower T6P amounts and the level of FT
transcripts is rescued in an inducible TPS1-expressing plant, GVG:TPS1,
suggesting that T6P positively activates the expression of FT (Wahl et al.,
2013). However, at SAM, T6P can promote flowering independently of FT
by inhibiting a floral repressor, miRNA156 (Wahl et al., 2013). miRNA156
targets the transcription factors SQUAMOSA PROMOTER-BINDING
LIKEs (SPLs), which promote flowering at the shoot apex and in leaves by
activating MADS-box floral regulators and miRNA172, respectively (Wang
et al., 2009; Wang, 2014). Targets of miRNA172 include floral repressors,
AP2-like transcriptional factors (see Section 5.4). In addition, T6P inhibits
the activity of SnRK1 in sugar metabolic regulation in flowering; genes
upregulated by T6P are downregulated by SnRK1 and vice versa (Zhang
et al., 2009). Under sugar starvation or sugar-limiting conditions, Arabidopsis
SNF1 kinase homolog 10 (AKIN10), the catalytic subunit of SnRK1, delays
flowering by inactivating IDD8 transcription, and the INDETERMINATE
DOMAIN (IDD)-containing transcription factor IDD8 promotes flowering
by modifying sugar metabolism (Jeong et al., 2015). IDD8 enhances the
expression of SUS4 by directly binding to the promoter of SUS4, thereby
promoting flowering. Thus, SnRK1-overexpressing plants and idd8 mutants
exhibit similar delayed flowering, whereas IDD8- and SUS4-overexpressing
plants and idd8SUS4ox are early flowering during long days (Jeong et al.,
2015; Seo et al., 2011).
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Nitrate-limiting conditions promote flowering during normal

(12-h light/12-h dark) and short days (8-h light/16-h dark). Moreover,
low nitrate can stimulate flowering even of late-flowering mutants in the
photoperiod, GA, and autonomous floral signaling pathways. For example,
the triple mutant fca-1co-2ga1-3 and mutants deficient in FT, LFY, and SOC1
flower earlier under low nitrate, indicating that early flowering under low
nitrate conditions ensures the reproduction of seeds even during short days
(Castro Marı́n et al., 2011). Consistently, nitrate reductase (NR)-deficient
plants such as nia1nia2 mutants with lower nitric oxide (NO) content flower
earlier with fewer rosette and cauline leaves and days to bolting (Seligman
et al., 2008). Secondary signaling molecules or metabolites, including ROS
or reactive nitrogen species induced by abiotic stresses, affect flowering time
through ascorbate/dehydroascorbate (Asc/DHA) and glutathione/glutathi-
one disulfide (GSH/GSSG) redox pairs and NO (He et al., 2004; Spoel and
van Ooijen, 2014). OXIDATIVE STRESS 2 (OXS2), a zinc finger protein,
is translocated under stress from the cytosol to the nucleus, where it directly
binds to the promoter of the floral integrator gene SOC1 and activates its
own expression (Blanvillain et al., 2011). NO represses the floral transition by
increasing FLC transcription (He et al., 2004). SA, which is important for
plant pathogen defense, promotes stress-induced flowering (Banday and
Nandi, 2015; Martı́nez et al., 2004; Wada et al., 2010; Wada and Takeno,
2010). The flowering of a short-day plant, P. nil, is promoted in
stress environments even under LD conditions (Shinozaki et al., 1988).
The metabolic pathway from trans-cinnamic acid to SA via benzoic
acid and not chlorogenic acid (CGA) is involved in stress-induced flowering
in P. nil (Hatayama and Takeno, 2003). Arabidopsis HEAVY METAL-
ASSOCIATED ISOPRENYLATED PLANT PROTEIN3 (HIPP3), a
nuclear zinc-binding protein, is induced in response to abiotic stress or
infection of Pseudomonas syringae pv tomato and is repressed under drought
and ABA treatment (Zschiesche et al., 2015). Its overexpressor shows delayed
flowering, but the mechanism remains unknown (Zschiesche et al., 2015).
Arabidopsis mutants deficient in the biosynthesis of ascorbate flower earlier
owing to higher expression of floral regulators in the photoperiodic flower-
ing pathway, including GI and CO, during long days (Kotchoni et al., 2009)
and at high SA levels during both long and short days (Barth et al., 2006).
Consistently, increased ascorbate amounts in Arabidopsis delay flowering
(Attolico and De Tullio, 2006). Moreover, high temperature–induced
early flowering of an Oncidium hybrid orchid involves the upregulation of
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14 H.J. Park et al.
cytosolic ascorbate peroxidase (cytAPX1) with a consequent high ROS

amount and low ascorbate ratio (Chin et al., 2014). Indeed, Arabidopsis
cytosolic APX1-deficient mutants exhibit late flowering when grown at
22°C during short days and even when transferred to high (30°C) temper-
ature to induce flowering (Chin et al., 2014). The overexpression of
OgcytAPX1 in Arabidopsis induces flowering under the same conditions
(Chin et al., 2014).
5. STRESS-SIGNAL INTEGRATION BY MAJOR FLOWERING

TIME REGULATORS
Recent research has shown that the key flowering time regulators
FLC, CO, and GI are hubs connecting the different stress pathways and
flowering. In this section, we will describe how each of these regulatory
nodes connects and integrates abiotic stress response and flowering time in
Arabidopsis (Fig. 2).
5.1 FLC Integrating Cold and ABA Into Autonomous and

Vernalization Pathways
FLC, the floral repressor acting in the autonomous and vernalization path-
ways, integrates responses to ABA, cold, and salinity through the genetic
and epigenetic regulation of its expression under stress, thereby delaying
flowering until environmental conditions improve or adaptation to the stress
environment is achieved [Fig. 2(A)]. Under stress conditions leading to the
accumulation of the phytohormone ABA, flowering is delayed through
ABSCISIC ACID-INSENSITIVE MUTANT 5 (ABI5), a bZIP transcrip-
tion factor involved in seed germination (Razem et al., 2006). ABI5 binds
to the FLC promoter in an ABA-dependent manner to upregulate FLC
transcription and delay the transition to flowering (Wang et al., 2013b).
The phosphorylation of ABI5 by SnRK2 is important for this process as
ABA fails to delay flowering in transgenic plants expressing the nonpho-
sphorylatable mutant protein ABI52AS145AT201A (Wang et al., 2013b).
The expression of FLC is also influenced by salinity stress via mechanisms
involving chromatin modifications (Zhang et al., 2011b). Shk1-BINDING
PROTEIN1 (SKB1)/PROTEIN ARGININE METHYLTRANSFERASE5
(PRMT5) associates with chromatin and mediates the symmetrical dimethyla-
tion of histone H4 on arginine 3 (H4R3sme2) (Zhang et al., 2011b). SKB1-
mediated histone modification of the FLC locus suppresses the expression
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[(Figure_2)TD$IG]
(A) (B) (C)
Vernalization ABI5
HOS1 Low red: far-red light
(cold, day) COPI UV
(night) Cold
Autonomous
pathway PhyA and PhyB
RNA interference UVR8
(miRNA169) CO
FLC
COPI
STO
FT SOC FT
HY5
HY5
AP1 LFY Shade avoidance
response
Photomorphogenesis UV-response
Flowering tolerance Salt tolerance
(D) (E)
Red light
Cold
GA Salt
PhyB
CBF1 SOS2 GI
GI Salt
Drought
SOS2-SOS3 (long days)
? ABA
SPY DELLA High temperature
(GAI, RGA, RGL) (short days) miRNA172
Salt ?
? SOS1 activation
CO GA /salt tolerance
Hypocotyl Cold tolerance
signaling
growth WARK44 TOE1 FT/ TSF
PIF3/PIF4 ABA tolerance
FT
Drought escape
Drought tolerance
Salt tolerance response (flowering)
Photomorphogenesis
Figure 2 FLC, CO, DELLA, and GI serve as hubs integrating the stress signals to flowering.
(A) FLC, a floral repressor implicated in both the autonomous pathway and vernalization,
integrates ABA, cold, miR169, and epigenetic regulation. ABA delays flowering through
FLC expression. CO (B) and STO (C) integrate light signaling and photoperiod pathways
with salt and cold stresses. (D) DELLAs integrate GA regulation of flowering and salt and
cold stresses. (E) GI is implicated in various stress responses, including salt stress,
drought, and ABA.
of FLC and promotes flowering. Salt or ABA displaces SKB1 from FLC
chromatin, reduces the level of H4R3sme2, enhances FLC transcription, and
delays flowering. Salt-induced displacement of SBK1 also alleviates the repres-
sion of stress-responsive genes, and yet, the skb1 mutant is hypersensitive to ABA
and salt because of the suppressed expression of stress-responsive genes, includ-
ing RD29A, RD29B, and COR47 as well as the ABA signaling negative regu-
lator HOMOLOGY TO ABI1 (HAB1) (Zhang et al., 2011b). However, this
stress sensitivity is unique to the skb1 mutant and is not shared by other late-
flowering mutants in the autonomous pathway, including £c (Zhang et al.,
2011b). Indeed, the £c mutant showed normal stress tolerance and the combined
£c and skb1 mutations did not show additive effects on stress sensitivity, indicating
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16 H.J. Park et al.
that the compromised salt stress response of skb1 was not related to FLC
deficiency. Instead, the growth retardation and stress sensitivity of the skb1
mutant were linked to defects in the mRNA splicing machinery (Zhang
et al., 2011b). Posttranslational modifications of SKB1 have not been reported;
thus, the signals regulating the nucleo-cytoplasmic partition of SBK1 and
chromatin occupancy remain poorly understood.
The overexpression of cold-inducible C-REPEAT (CRT)/
DEHYDRATION-RESPONSIVE ELEMENT (DRE)-BINDING
FACTOR1 (CBF) results in late flowering owing to higher expression of
the flowering repressor FLC, suggesting that cold and low temperatures
delay flowering through FLC (Seo et al., 2009). Moreover, the autono-
mous floral promoting pathway components FVE and FLD repress FLC
expression through histone modification around the FLC chromatin under
cold stress. The ALTERED COLD-RESPONSIVE GENE1 (ACG1) was
identified as a negative regulator of the CBF/DREB cold stress response
pathway. The acg1 mutation enhanced the expression levels of cold-respon-
sive genes and improved cold acclimation (Kim et al., 2004). Interestingly,
acg1 flowered late during both long and short days because of the high
expression of FLC. The acg1 mutation proved to be a null allele of the
autonomous pathway gene FVE, a component of the HDAC complex
involved in transcriptional repression (Ausin et al., 2004; Kim et al.,
2004). Chromatin immunoprecipitation analysis showed that ACG1/
FVE binds to the FLC and COR15A chromatin, suggesting that the
HDAC complex containing FVE promotes cold stress response and cold-
delayed flowering by influencing the deacetylation of the histone proteins
at FLC and COR15A loci under cold conditions (Jeon and Kim, 2011; Kim
et al., 2004). Daily intermittent cold treatment (4°C for 2–5 h each day),
which is distinct from the sustained cold typical of vernalization, increased
FLC transcript levels and delayed flowering. However, similar to skb1,
the effect of the acg1/fve mutation on the expression of cold stress-respon-
sive genes was independent of FLC (Kim et al., 2004).
The autonomous pathway component FLD is a histone demethylase that
interacts with HISTONE DEACETYLASE6 (HDA6) (He et al., 2003; Yu
et al., 2011). The enhanced transcription of FLC in both hda6 and £d mutants
(He et al., 2003; Liu et al., 2007; Wu et al., 2008) and the greater levels of
H3 acetylation and H3K4 trimethylation at the FLC locus in these mutants
(Yu et al., 2011) indicate a functional interplay between HDAC and
demethylase activities in flowering time control. HDA6 transcription is
induced under cold conditions (To et al., 2011), suggesting that cold stress
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leads to further repression of FLC through FLD and HDA6-mediated

histone H3 modification.
Another histone variant, H2A.Z, mediates the modification of chro-
matin at FLC in response to ambient temperature. The loss of H2A.Z from
FLC chromatin causes early and premature flowering (during both long
and short days) owing to decreased FLC levels in arp6 and pie1 mutants
deficient in ACTIN-RELATED PROTEIN6 and PHOTOPERIOD-
INDEPENDENT EARLY FLOWERING1, which encode components
of the SWP1 ATP-dependent chromatin remodeling complex that deposits
H2A.Z in the nucleosome (Deal et al., 2005, 2007; March-Dı́az and
Reyes, 2009; Kumar and Wigge, 2010). Phenotypic and biochemical
analyses of the arp6-10 mutant indicated that warm ambient temperature
(27°C) during short days induced flowering by decreasing H2A.Z occu-
pation on FLC chromatin.
miRNAs appear to have critical functions in abiotic stress responses and
floral induction (Han et al., 2013). miRNA169 is highly expressed under
various stress conditions such as low temperature (Lee et al., 2010), high
salt (Zhao et al., 2009), drought (Zhang et al., 2011a), low nitrogen (Zhao
et al., 2011), and UV-B radiation (Zhou et al., 2007). miRNA169 targets
and suppresses transcripts encoding nuclear factor Y (NF-Y)-family tran-
scription factors, in turn reducing the expression of the floral repressor FLC
and resulting in stress-induced early flowering (Xu et al., 2014). Nuclear
transcription factor Y, alpha (NF-YA), a transcriptional regulator, is involved
not only in flowering but also in drought tolerance and ABA response
(Warpeha et al., 2007; Xu et al., 2014).
Collectively, the aforementioned results indicate that although FLC is a
focal regulatory node integrating and synchronizing genetic responses to
environmental stress and phase transition to floral development, thereby
maximizing plant fitness, the flowering time regulators acting in the auton-
omous pathway are not stress-tolerance determinants per se.
5.2 CO Integrating Light Signaling and Photoperiod Pathways

With Salt and Cold Stresses
The RING finger E3 ubiquitin ligase HOS1, which mediates the degrada-
tion of INDUCER OF CBF EXPRESSION 1 (ICE1), a cold-activated
transcription factor of the CBF genes (Chinnusamy et al., 2003; Dong et al.,
2006; Ishitani et al., 1998; Lee et al., 2001), targets the CO protein for
degradation under cold stress, resulting in suppressed expression of FT and
delayed flowering (Jung et al., 2012). The early flowering of the hos1 mutant
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18 H.J. Park et al.
during both long and short days is repressed by a co mutant exhibiting delayed
flowering (Lazaro et al., 2012), suggesting that the CO-HOS1 module
integrates photoperiod and temperature signals into the flowering pathways
during short-term low-temperature periods (Jung et al., 2012) [Fig. 2(B)].
CO may also integrate light and photoperiod pathways with drought
tolerance and ABA responses through the NF-Y family of transcription
factors. NF-Y transcription factors are heterotrimeric complexes comprising
subunits NF-YA, NF-YB, and NF-YC. As shown earlier, abiotic stress–
induced miRNA169 targets the transcripts of NF-YA subunits, in turn reduc-
ing the expression of the floral repressor FLC and resulting in stress-induced
early flowering (Xu et al., 2014). In addition, three NF-YC isoforms
(NF-YC3, NF-YC4, and NF-YC9) that are required for flowering physi-
cally interact with CO and are genetically required for CO-mediated floral
promotion in the photoperiodic pathway (Kumimoto et al., 2010).
UV-B (280–315 nm) light, a potential abiotic stress factor, delays flower-
ing, particularly in bee-pollinated plants (Sampson and Cane, 1999).
However, UV-C light (100–280 nm) stress promotes flowering through
SA, which induces early flowering (Martı́nez et al., 2004). UV-B is inte-
grated into the network, regulating flowering time through CO. On expo-
sure to UV-B, the inactive photoreceptor UVB-RESISTANCE 8 (UVR8)
homodimer is converted to an active monomer that interacts in a UV-B-
dependent manner with CONSTITUTIVE PHOTOMORPHOGENIC1
(COP1), a repressor of light-signaling mediators (Favory et al., 2009; Jang
et al., 2008; Liu et al., 2008). The COP1–UVR8 complex requires inter-
action with SUPPRESSOR OF PHYA-105 (SPA1) for UV-B signal relay
(Heijde et al., 2013; Huang et al., 2013). SPA proteins, which act in concert
with COP1 to suppress photomorphogenesis in the dark, also interact with
the floral inducer CO to regulate photoperiodic flowering (Laubinger
et al., 2006). SPA proteins are essential for the inhibition of flowering during
noninductive short days by preventing the accumulation of CO. The spa
mutations cause early flowering only during short days by the stabilization
of CO and enhanced expression of FT mRNA, particularly in the dark
(Laubinger et al., 2006).
SALT TOLERANCE (STO)/B-BOX PROTEIN24 (BBX24) is a zinc
finger-like protein similar to CO that was isolated on the basis of its ability to
alleviate salt sensitivity of a yeast calcineurin mutant (Lippuner et al., 1996).
Salt does not induce STO transcription, but STO overexpression in trans-
genic plants results in elevated salinity tolerance (Nagaoka and Takano,
2003). Cold and UV-B induce STO transcription (Jiang et al., 2012;
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Soitamo et al., 2008). STO affects flowering time; the overexpression of

STO promotes flowering during both long and short days by enhancing FT
and SOC1 transcription and repressing FLC transcription (Li et al., 2014).
Although STO interacts with COP1 upon UV treatment, the interac-
tion of STO with HY5 is attenuated on exposure to UV, suggesting that
STO acts as a negative regulator of UV-B mediated photomorphogenesis
by interacting with COP1 and HY5 (Jiang et al., 2012). Moreover, com-
pared with wild-types, red (R) light-induced STO transcript expression is
reduced in phyA, phyB, and phyA phyB mutants; however, in far red (FR)
light, the STO level in phyB mutants approaches the level found in wild-
types (Indorf et al., 2007). Interestingly, the STO protein localizes to the
nucleus in a light-dependent manner and interacts with light-signaling
components such as ELONGATED HYPOCOTYL5 (HY5) and COP1
(Indorf et al., 2007) [Fig. 2(C)].
5.3 DELLAs Integrating GA Regulation of Flowering With Salt

and Cold Stresses
DELLA proteins, whose name is derived from the conserved N-terminus
D-E-L-L-A amino acid motif, belong to a subgroup of plant-specific GRAS
(GAI, RGA, and SCARECROW) proteins. Arabidopsis has five DELLA
proteins: GIBBERELLIC ACID INSENSITIVE (GAI), REPRESSOR
OF GA1 (RGA), RGL1, RGL2, and RGA-LIKE (GRL3). DELLAs
are nuclear proteins that act as growth repressors throughout the life
cycle of higher plants. GAs promote cell proliferation and expansion by
triggering the degradation of growth-repressing DELLA proteins (Locascio
et al., 2013). DELLAs are also negative regulators in the GA signaling
pathway. GA is recognized by the GA receptor protein GIBBERELLIN
INSENSITIVE DWARF1 (GID1), which interacts with and induces the
degradation of DELLA via E3 ubiquitin ligases such as rice SKP1-CULLIN-
F-box with F-box protein GID2 (SCFGID2), Arabidopsis SCF with F-box
SLEEPY1 (SCFSLY1), and the 26S proteasome (Sun, 2010).
Salinity slows plant growth by reducing the levels of endogenous GA and
blocking the GA-induced degradation of DELLAs (Achard et al., 2006,
2008a; Magome et al., 2008). Although a quadruple DELLA mutant defi-
cient in RGI, RGA, RGL1, and RGL2 is relatively tolerant to salt in short-
term experiments, the growth restraint conferred by DELLA proteins is
beneficial in stress environments in the long term and ultimately promotes
survival by favoring adaptation over growth. Salt-induced late flowering is
suppressed in DELLA loss-of-function mutants because the transcript levels
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20 H.J. Park et al.
of LFY, a floral identity gene, are not reduced in contrast to those of salt-
treated wild-type plants (Achard et al., 2006). Thus, salt delays flowering
because the growth restraint imposed by stabilized DELLAs lengthens the
vegetative phase and because of the reduced transcription of LFY by an
unknown mechanism that requires DELLA.
DELLAs also gate cold-induced late flowering. The cold-inducible tran-
scriptional activator CBF1 induces the expression of a set of genes responding
to low temperature (the CBF regulon). CBF1 also enhances the accumula-
tion of DELLAs through the upregulation of GA2-oxidases (GA2ox), which
deactivate bioactive GAs (Achard et al., 2008a). The late flowering of CBF1
overexpressors is suppressed in a della mutant (CBF1-OX gai rga) (Achard
et al., 2008b). The delayed flowering induced by the stress hormones
ABA and ethylene is also repressed in della mutants, suggesting that stress
signals relayed by these two phytohormones are integrated at the level of
DELLA function (Achard et al., 2006, 2007). Together, these observations
indicate that environmental stress delays flowering at least in part via the same
mechanism that contributes to the inhibition of vegetative growth.
In Arabidopsis, warmer ambient temperatures (27 vs. 22°C) overcome late
flowering during short days via a mechanism that involves the floral pathway
integrator FT and PHYTOCHROME INTERACTING FACTOR4
(PIF4) (Balasubramanian et al., 2006; Kumar et al., 2012). PIF4 upregulates
FT in a temperature-dependent manner. In the absence of GA, DELLAs
interact with PIF3 and PIF4 and inhibit the DNA binding of PIFs to their
targets (de Lucas et al., 2008; Feng et al., 2008). In the presence of GA, the
degradation of DELLA and PIF4 is mediated by SCFSLY1 and PhyB, respec-
tively (de Lucas et al., 2008). PIF4 regulates ambient temperature–mediated
floral induction through direct activation, particularly within 12–27°C
(Kumar et al., 2012) Cold temperature delays flowering, but a della mutant
flowers earlier than wild-types at 12°C (Kumar et al., 2012). Thus, DELLA
may regulate FT through PIF4 as DELLA controls PIF4 DNA-binding
activity (de Lucas et al., 2008) and PIF4 induces FT transcription under high
temperature (Kumar et al., 2012) [Fig. 2(D)]. Recently, PIF4 and H2A.Z
have been reported as positive regulators of flowering in response to tem-
perature by promoting the expression of FT (Kumar and Wigge, 2010;
Kumar et al., 2012). The bHLH transcription factor PIF4 activates the
expression of FT by directly binding to the promoter of FT at high (27°C)
temperature during short days, and PIF4 expression increases at higher
temperature (Kumar et al., 2012). The occupancy of the histone H2A.Z
variant or H2A.Z-containing nucleosomes on the FT promoter where PIF4
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binds decreases with increasing temperature, suggesting that the H2A.Z

nucleosome is a limiting factor in the binding of PIF4 to the promoter of
FT (Kumar and Wigge, 2010).
5.4 GI Integrating Photoperiod With Drought, Cold, and Salt

Stresses
GI is a large nucleoplasmic protein encoded by a conserved single gene in
many (likely all) plant species (Berns et al., 2014; Fowler et al., 1999; Huq
et al., 2000; Park et al., 1999). GI is involved in the photoperiod-dependent
pathway for flowering regulation and affects plant tolerance to drought (Han
et al., 2013; Riboni et al., 2013), cold (Cao et al., 2005; Fornara et al., 2015;
Xie et al., 2015), salt (Kim et al., 2013), and herbicide (Cao et al., 2006;
Kurepa et al., 1998). GI also contributes to circadian clock control, light
signaling (phyB and cryptochrome signaling) (Huq et al., 2000; Oliverio
et al., 2007), hypocotyl elongation (Kim et al., 2012; Tseng et al., 2004), blue
light-mediated stomatal opening (Ando et al., 2013), and carbohydrate
metabolism and signaling (Dalchau et al., 2011). Various gi mutant alleles
exhibit distinct pleiotropic phenotypes (Table 2). Natural alleles of GI
show distinct phenotypes under the same environmental conditions (Xie
et al., 2015). For instance, two polymorphic BrassicarapaGI alleles, R500 and
IMB211, rescued the late flowering of the Arabidopsisgi-201 mutant, although
BrGIIMB211 complemented gi-201 under exposure to cold and salt stress and
BrGIR500 did not (Xie et al., 2015).
GI is implicated in cold stress response. GI expression is induced by cold
(Cao et al., 2005; Fowler and Thomashow, 2002). However, different gi
mutants in different ecotype backgrounds exhibit varying sensitivity or
tolerance to cold and freezing (Cao et al., 2005; Fornara et al., 2015). The
null mutant gi-3 in the background of Landsberg erecta is hypersensitive to
freezing owing to a sugar deficiency attributed to elevated starch accumula-
tion and low levels of soluble sugars in leaves (Cao et al., 2007). This finding
suggests that GI mediates a cold stress response through a CBF-independent
pathway, considering the absence of marked differences in CBF genes and
their regulons, although the late flowering of the gi-3 mutant is delayed to a
large extent by cold (Cao et al., 2005). However, the gi-201 and gi-100
knockout mutants in the Col-0 background have significantly higher toler-
ance to freezing than wild-types (Fornara et al., 2015; Xie et al., 2015). The
freezing tolerance of gi-100 is due to the upregulated expression of cold-
regulated genes, including RD29A/COLD REGULATED 78 (RD29A/
COR78), COR15A, COR15B, KIN1, and KIN2 (COLD-RESPONSIVE 6.6)
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22 H.J. Park et al.
Table 2 Pleiotropic phenotypes of Arabidopsis gi mutants and functions of GI.

Description References
gi mutants show light-dependent resistance Cao et al. (2006)
to paraquat-induced oxidative stress, Kurepa et al. (1998)
possibly due to high superoxide dismutase
and ascorbate peroxidase.
gi mutants have longer hypocotyls than Huq et al. (2000)
wild-types under constant red light or far
red light, suggesting GI involvement in
PhyB signaling.
gi mutants are sensitive to cold and have Cao et al. (2005)
lower amounts of cold-induced sugars. Dalchau et al. (2011)
GI was proposed to act as a component of
sucrose-signaling networks.
gi mutants exhibit circadian phenotypes. GI Fujiwara et al. (2008)
interacts with F-box protein, Mas et al. (2003)
ZEITLUPE, which is involved in the Kiba et al. (2007)
degradation of TIMING OF CAB Kim et al. (2007)
EXPRESSION 1 (TOC1). TOC1
represses many circadian genes, including
CCA1, PRRs, and LUX.
gi mutants flower late. GI regulates Sawa et al. (2007)
flowering and the circadian clock Sawa and Kay (2011)
through posttranslational control. GI Suarez-Lopez et al.
forms a complex with FKF1, which (2001)
degrades CDFs, a repressor of CO, a Valverde et al. (2004)
central activator of photoperiodic
flowering. GI also directly promotes FT
expression.
Mutants of SPINDLY, which encodes a GI Tseng et al. (2004)
interactor, are tolerant to high salt and Qin et al. (2011)
drought.
gi mutants are tolerant to salt. GI associates Kim et al. (2013)
with the SALT OVERLY SENSITIVE 2
(SOS2) and SOS3 complex. GI is
degraded upon salt stress and releases
SOS2, which activates SOS1 and sodium
efflux out of cells, suggesting that GI is a
negative regulator of salt stress response.
gi mutants are sensitive to drought and lose Han et al. (2013)
the drought escape response (the ability of Riboni et al. (2013)
plants to complete their life cycle before
stress conditions lead to death).
(continued )
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Table 2 Pleiotropic phenotypes of Arabidopsis gi mutants and functions of GI.—cont'd

Description References
On loss of GI function, gi-100 shows Fornara et al. (2015)
freezing tolerance due to upregulated
CBF and CBF regulon expression.
cdf1235 mutants reduce the cold tolerance
of gi-100 with reduced transcript level of
cold-related genes, suggesting that GI-
CDF module regulates cold response.
gi-2 and gi-3 mutants exhibit less wall Edwards et al. (2010)
ingrowth deposition in phloem
parenchyma transfer cells, and high light-
or cold-induced wall ingrowth
development is impaired in the gi-2
mutant.
gi-2 suppresses leaf variegation of immutans, Putarjunan and
which is mutated in PTOX, a plastid Rodermel (2014)
membrane-localizing plastoquinol
oxidase in thylakoid redox, and
cytokinins seem to be involved as this
suppression of variegation in imgi-2
occurs because of the upregulation of
cytokinin-related genes. The variegation
of im is rescued by treatment with the GA
inhibitor paclobutrazol (PAC), which
increases the expression of cytokinin-
related genes but delays flowering. GA
treatment and the spy mutant can rescue
the late flowering of imgi-2, suggesting
that GI plays a role in regulating thylakoid
redox through cytokinin and GA
interaction.
The long circadian period induced by Fe Chen (2013)
deficiency is ameliorated in the gi-2
mutant.
Light-induced stomatal opening is reduced Ando et al. (2013)
in the gi-1 mutant. Failure of light-
induced stomatal opening and ABA- and
calyculin A (CA)-induced stomatal
closure of phot1phot2 is rescued by the
addition of GI. CA is the type1/2A
protein phosphatase inhibitor inhibiting
the blue light-dependent activation of
H+-ATPase in guard cells.
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24 H.J. Park et al.
during both short and long days (Fornara et al., 2015). The basis for this
GI polymorphism, and the ecotype dependency of cold tolerance is presently
unknown.
Under LD conditions and drought stress, GI transcripts and miRNA172
are both upregulated, causing the suppressed expression of the targets of
miRNA172, WRKY44, and TARGET OF EAT1 (TOE1), in turn resulting
in drought tolerance (Han et al., 2013). The expression of miRNA172
depends on GI but does not require CO. In addition, miR172 promotes
flowering by posttranscriptionally repressing APETALA2 (AP2)-like
genes, including TOE1, TOE2, TOE3, SCHLAFMEŁTZE (SMZ), and
SCHNARCHZAPFEN (SNZ), which encode floral repressors, except
for TOE3 (Aukerman and Sakai, 2003; Jung et al., 2007, 2014). Plants
overexpressing miRNA172 show early flowering during both long and
short days, suggesting that miRNA172 regulates photoperiodic flowering
in a CO-independent manner (Jung et al., 2007) [Fig. 2(E)].
GI appears to integrate salt stress and the GA-dependent pathway
through SPY and miR172. SPY, an O-linked β-N-acetylglucosamine
transferase acting as a negative regulator of GA signaling, also acts as a
component of the clock (Achard and Genschik, 2009; Silverstone et al.,
2007). The specific protein interaction of GI and SPY affects flowering
time and circadian stomatal dynamics (Sothern et al., 2002; Tseng et al.,
2004). The loss-of-function spy mutant attenuates late flowering mediated
by gi-2 by increasing the transcription of CO and FT in gi-2 mutants
(Tseng et al., 2004). The spy mutant plants exhibit a high-GA phenotype
and enhanced tolerance to drought and salt (Qin et al., 2011). SPY may add
an O-linked β-N-acetyl glucosamine to DELLA proteins; thus, DELLA
proteins are potential targets of SPY [Fig. 2(D)]. In addition, ABA-induced
miRNA172, whose abundance is regulated by GI, targets the mRNAs
encoding GA-specific transcriptional regulators, GAMYBs, AtMYB33,
and AtMYB101, which in turn bind to a GA-response element in the
LEAFY gene promoter (Achard et al., 2004; Reyes and Chua, 2007).
Thus the GI-mediated GA-dependent pathway for flowering is also asso-
ciated with the salt stress response.
Another direct link between GI and salinity stress has recently been
reported (Kim et al., 2013). The relationship reveals direct regulation of
ionic homeostasis through GI. GI partners in a protein–protein interaction
with the SNF1-related Ser/Thr protein kinase SALT OVERLY
SENSITIVE2 (SOS2), a known key element of the SOS pathway
(Liu et al., 2000). This interaction strongly reduces or prevents SOS2
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activation of SOS1, a plasma membrane–localized Na+/H+ antiporter,

under regular nonstress conditions. SOS1 functions in the efflux of Na+
from roots and loading of Na+ into the xylem to decrease cellular Na+
content under salt stress (Olı́as et al., 2009; Shi et al., 2002). Salt stress induces
proteasomal degradation of GI, thereby releasing the SOS2 protein, which
then becomes available to interact with the calcium-binding protein SOS3, a
myristoylated, EF-hand containing protein, homologous to the regulatory
subunit of yeast calcineurin (Ishitani et al., 2000; Liu and Zhu, 1998). The
SOS2–SOS3 complex in turn activates SOS1 (Quintero et al., 2002, 2011).
Arabidopsis plants overexpressing GI are more salt-sensitive than wild-types,
whereas gi mutants are markedly salt-tolerant. This observation strongly
supports the inference that salt-induced activation of the SOS2 kinase pro-
motes the activation of the Na+/H+ antiporter SOS1 and that this activation
increases salt tolerance. Thus, stress-induced release of SOS2 from interac-
tion with GI modulates the dynamic behavior of SOS2. The amount of
GI and its degradation are controlled by the clock (Fujiwara et al., 2008; Kiba
et al., 2007; Kim et al., 2007; Mas et al., 2003; Yu et al., 2008). Thus, the salt
stress response may also be associated with clock functions, thereby bridging
pathways previously considered unrelated. The SOS components appear to
have no involvement in flowering under nonstress conditions. However,
under stress (50 mM NaCl), the sos3-1 mutant exhibits delayed flowering
(50 mM) (Li et al., 2007). This finding is consistent with the observation that
SOS3 associates with GI (Kim et al., 2013). Taken together, these findings
suggest that SOS3 also contributes to linking salinity stress and flowering.
Additional evidence that GI engages in a direct connection with abiotic
stress responses is that the late flowering of the gi-3 mutant is further delayed
under cold and that GI regulates cold acclimation independently of CBFs,
whose cold-induced expression is in turn regulated by the circadian clock
(Cao et al., 2005; Fowler et al., 2005). This finding suggests that GI is
involved in cold acclimation signaling pathway(s) or plays a protective
function against cold. A recent study of GI involvement in freezing toler-
ance contradicts the role of GI in the CBF-independent pathway for cold
stress response (Fornara et al., 2015). gi-100 shows freezing tolerance owing
to the upregulated expression of CBF and CBF regulons such as the cold-
regulated genes COR15A, COR15B, and KIN1. However, loss-of-function
of CDF genes, which act downstream of GI in the photoperiod-dependent
flowering pathway and promote the expression of the floral regulators CO
and FT, is sensitive to freezing because of the reduced transcription of
cold-related genes. This finding indicates that the GI-CDF module
ARTICLE IN PRESS
26 H.J. Park et al.
regulates cold stress response by controlling the expression of transcription

factors for cold stress responses but CDF does not control the circadian
period, considering that cdf mutants do not affect the circadian period of
the gi mutant, although the exact molecular mechanism remains unknown
(Fornara et al., 2015).
6. ROLE OF GI IN INFLUENCING FLOWERING TIME AND

CIRCADIAN CLOCK COMPONENTS
Rather than directly regulating the various stress responses, GI may

affect various stress-responsive pathways through the circadian clock by trans-
mitting stress signals to the circadian clock [Fig. 3(A)]. The circadian clock
regulates GI expression, and GI itself is a component of the clock. Indeed, GI
transcription is under circadian control, and the GI protein affects the clock by
interacting with and regulating the stability of the circadian oscillator TIMING
OF CAB EXPRESSION1 (TOC1). GI transcription is under circadian
control and peaks 8–10 h after the start of the day. GI protein levels, controlled
by dark-induced proteolysis, closely follow the levels of the GI transcript
(David et al., 2006). The amplitude, timing, and duration of the GI peak
depend on day length (Fowler et al., 1999). GI mutation alters the amplitude
and period length of the expression of the circadian oscillator genes
CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED
HYPOCOTYL (LHY). The gi mutants are also defective in light signaling
to the clock (i.e., input to the clock). The light-regulated association of GI
with the light-sensing F-box protein ZEITLUPE (ZTL) is responsible for
dark-dependent proteasomal degradation of TOC1 (Mas et al., 2003; Kim
et al., 2007). This degradation in turn regulates the transcription of CCA1 and
LHY. Mutational inactivation of GI also affects clock outputs and leads to late
flowering during long days but not during short days (Fowler et al., 1999).
Moreover, abiotic stresses affect the expression of GI and/or abundance
of the GI protein. GI transcription can be regulated by stresses as well. GI is
transcriptionally induced by cold stress (Cao et al., 2005; Fowler and
Thomashow, 2002) and drought (Han et al., 2013) but not by salt, mannitol,
or ABA (Cao et al., 2005). The regulation of GI expression by sucrose
levels suggests a link between the metabolic status and the circadian clock
(Dalchau et al., 2011). Imazethapyr (IM), a chiral herbicide, does not change
the circadian phase of GI but decreases the amplitude of core oscillators
(CCA1 and LHY) and upregulates GI transcripts. Consequently, the
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[(Figure_3)TD$IG]
(A)
ZT12
Maximal drought stress
Maximal heat stress

TOC1
ELF4
GI LUX Maximum
ZTL
sensitivity to
ROS level peaks GI
ELF3 pathogen infection
TOC1
Solar radiation peaks PRR5 PRR5 ELF3 ELF4

and maximum stomatal
LUX
opening PRR7 ZT18
PRR7
PRR9
CCA1
PRR9
LHY
Light-harvest gene peaks
LHY
CCA1
Maximum starving and cold stress
ZT0
(B)
Inputs
Outputs
Gene expression
Cytosolic calcium cycling
Stresses Stomatal opening
Freezing Hypocotyl growth
NaCl Petal opening
Drought Cotyledon/leaf movement
Flowering
ROS
Pathogen
Figure 3 The Arabidopsis circadian clock and environmental conditions/stresses. (A) The
biological clock regulates photoperiodic flowering and is entrained by the environment.
The Arabidopsis clock has three integrated feedback loops that maintain the rhythm,
amplitude, and phase of the clock. Transcriptional loops with both positive and negative
regulators form the robust, interlocking, self-regulatory circadian clock mechanism. The
clock oscillators that make up the main loops include CCA1, LATE ELONGATED
ARTICLE IN PRESS
28 H.J. Park et al.
photoperiod signaling pathway with GI-CO-FT and LHY can promote

early flowering (Qian et al., 2014).
Here the question arises whether GI directly controls stress responses or
indirectly through the circadian clock. In other words, GI may be the
mediator of the crosstalk between the circadian clock and environmental
stress signal input, and the clock outputs are shown as physiological adapta-
tions to the surrounding environment. In fact, the circadian clock affects
stomatal dynamics, shade avoidance responses, and metabolic activity asso-
ciated with the photoperiod as well as defense against pathogens (Dalchau
et al., 2011; Hong et al., 2013; Hotta et al., 2007; Müller et al., 2014; Seung
et al., 2012; Wang et al., 2011) [Fig. 3(B)]. Stomatal aperture reflects the
integrated effects of factors such as ABA, Ca2+, and ROS as well as light
quality and quantity and the phase of the circadian clock. Microarray expres-
sion analyses have shown that approximately 30% of transcripts are under
◂ HYPOCOTYL (LHY), and TIMING OF CAB EXPRESSION 1 (TOC1/PRR1). The Myb

transcription factors CCA1 and LHY, which are expressed in the morning, negatively
regulate the expression of TOC1, an evening-expressed transcriptional repressor and
one of five pseudo response regulators (PRRs) (Alabadí et al., 2001; Huang et al., 2012).
The transcript abundances of PRRs oscillate with their circadian periods. The expression
of PRR9, PRR7, PRR5, PRR3, and PRR1/TOC1 peaks in succession, at 2-h intervals from the
dawn to evening (Mizuno and Nakamichi, 2005). PRR proteins appear to share partially
redundant functions as higher-order prr mutants exhibit circadian phenotypes,
although single mutants show only minor defects of circadian rhythm (Nakamichi et
al., 2005a,b; Salomé and McClung, 2005). PRR9, PRR7, and PRR5 repress the transcription
of CCA1 and LHY (Nakamichi et al., 2010). TOC1/PRR1 overexpression negatively
regulates GI transcripts (Makino et al., 2002), but the interaction of ZTL with the GI
protein stabilizes ZTL, which degrades TOC1 and PRR5 (Fujiwara et al., 2008; Kiba et al.,
2007; Kim et al., 2007; Mas et al., 2003). In addition, ZTL regulates the protein levels and
nucleocytoplasmic distribution of GI (Kim et al., 2013). EARLY FLOWERING 3 (ELF3),
EARLY FLOWERING 4 (ELF4), and the GARP transcription factor LUX ARRHYTHMO/
PHYTOCLOCK1 (LUX/PCL1) form the evening complex (EC), which binds to the
promoters of target genes PIF4, PIF5, and PRR9 (Chow et al., 2012; Helfer et al., 2011;
Herrero et al., 2012; Nusinow et al., 2011) (B) The Arabidopsis circadian clock is entrained
by light/dark cycles and warm/cold temperature cycles, which a plant experiences
during the day and night. Plants are also exposed to environmental and abiotic
stresses, including freezing, salt, drought, UV, and pathogen infection. Plants harvest
light and open stomata for photosynthesis in the day when they are exposed to various
stresses such as H2O2, heat, and drought. After sunset, hypocotyl growth, conversion of
starch to sucrose, and respiration occur, corresponding to the time at which cold/
freezing stress and nutrient starvation typically occur. These stresses serve as input
signals that are integrated into the clock. The clock regulates the circadian rhythms of
physiological and biochemical processes in cells by gating, meaning that the time when
stress is encountered can influence the stress response.
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clock control (Covington et al., 2008; Hubbard et al., 2009; Michael et al.,
2008). The expression of stress-responsive genes such as salt-, drought-, and
osmotic stress–regulated genes are under circadian control (Covington et al.,
2008; Harmer et al., 2000; Kreps et al., 2002; Marcolino-Gomes et al., 2014;
Wilkins et al., 2010). For example, transcripts of CBFs and the CBF regulon
exhibit circadian rhythm. The cold-induced expression of CBF1-3 genes
(DREB1B, C, and A, respectively), which in turn regulate the transcription
of cold, drought, and salinity response genes (Liu et al., 1998), depends on
the time of day at which plants are exposed to low temperature, suggesting
that cold-induced CBF expression is gated by the clock (Dong et al., 2011;
Fowler et al., 2005; Nakamichi et al., 2009). The cold induction of CBF
transcripts is much greater at ZT4 than at ZT16 (Fowler et al., 2005). The
transcription of CBFs and the CBF regulon is impaired in cca1-11/lhy-21
double mutants, suggesting that the circadian regulation of CBF-mediated
cold response requires CCA1 and LHY. In the morning, CCA1 and LHY
bind to CBF promoters and positively regulate the transcription of CBF so
that CBFs peak shortly after the peaking time of CCA1 and LHY1
(Dong et al., 2011). RESPONSIVE TO DESICCATION 29 (RD29A,
COR78), which is highly induced by abiotic stresses such as salt, drought,
and cold via an ABA-dependent pathway, is under clock control (Mockler
et al., 2007; Msanne et al., 2011). Salt-induced expression of RD29A is
higher during the day than during the night (Kim et al., 2013). A range of
nutrient and ion transporters such as sucrose transporters, nitrate transpor-
ters, potassium transporters, copper transporters, and zinc transporter pre-
cursors is under circadian regulation (Haydon et al., 2011; Perea-Garcı́a
et al., 2016).
7. CONCLUSIONS
The question of how plants integrate or coordinate various environ-

mental inputs or stresses into flowering pathways has been addressed from the
perspective of plants’ capability to avoid or escape stresses, adapt to stresses, or
follow tolerance strategies. In most cases, abiotic stress signaling cascades
appear to influence the transcriptional level of floral integrators such as FT
and LFY, thereby delaying flowering time or promoting floral pathways.
In addition, flowering time regulators, including FLC, CO, DELLA, and
GI, serve as major hubs that connect abiotic stresses with flowering time
regulation. However, these regulatory pathways are not linear under specific
ARTICLE IN PRESS
30 H.J. Park et al.
abiotic stress conditions. Rather, various signaling cascades are associated

with one another and the various environmental inputs are transmitted
downstream together and merged by floral integrators that control flowering
time. Among the major hubs coordinating abiotic stresses with flowering
time, GI appears to be a key node integrating flowering and abiotic stress
response, considering that it is involved in the regulation of many processes in
response to cold stress, drought, and salinity. At the same time, GI integrates
the photoperiod with the circadian clock. Thus, it mediates stress responses
directly through association with stress response pathway components and
indirectly by affecting the expression of the clock components. Furthermore,
stress-responsive genes are under clock regulation.
ACKNOWLEDGMENTS
Our work was supported by grants from the National Research Foundation of Korea
(NRF) funded by the Korean Government (MSIP No. 2013R1A2A1A01005170) and
Next-Generation BioGreen21 Program (SSAC, grant PJ01105101), Rural Development
Administration, Republic of Korea. H.J. Park and W.-Y. Kim were supported by the Basic
Science Research Program through the National Research Foundation of Korea (NRF)
funded by the Ministry of Science, ICT & Future Planning NRF-2013R1A1A3013245
and NRF-2015R1D1A1A02061979, respectively.
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Molecular Interactions Between Flowering Time and

Chapter in International review of cell and molecular biology · September 2016

Woe Yeon Kim Jose M Pardo

SEE PROFILE SEE PROFILE

Plant circadian rhythm View project

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Molecular Interactions Between

International Review of Cell and Molecular Biology,

2 H.J. Park et al.

Plants species, primarily crops, most of which originated in the sub-

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 3

environmental cues to ensure successful reproduction. In this review, we will

2. DEVELOPMENTAL AND SEASONAL CONTROL OF

4 H.J. Park et al.

Meristem identity genes

Figure 1 Environmental stresses affect flowering time in Arabidopsis. Flowering time

generation of plants. Thus, vernalization is a cold-mediated epigenetic

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 5

3. KEY MOLECULAR REGULATORS OF FLOWERING TIME

A comprehensive coverage of all molecular constituents of pathways

6 H.J. Park et al.

transcription factor CONSTANS (CO). The circadian clock and factors

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 7

4. ABIOTIC STRESSES AFFECTING FLOWERING TIME

Table 1 Stress-induced flowering.

8 H.J. Park et al.

temperature, low nitrate concentration, and presence of salicylic acid (SA)

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 9

10 H.J. Park et al.

Plants with loss-of-function mutation in HIGH EXPRESSION OF

4.2 Drought and ABA

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 11

dehydration stresses reduce the size of flowers in ornamental crops

12 H.J. Park et al.

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 13

Nitrate-limiting conditions promote flowering during normal

14 H.J. Park et al.

cytosolic ascorbate peroxidase (cytAPX1) with a consequent high ROS

5. STRESS-SIGNAL INTEGRATION BY MAJOR FLOWERING

5.1 FLC Integrating Cold and ABA Into Autonomous and

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 15

16 H.J. Park et al.

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 17

leads to further repression of FLC through FLD and HDA6-mediated

5.2 CO Integrating Light Signaling and Photoperiod Pathways

18 H.J. Park et al.

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 19

Soitamo et al., 2008). STO affects flowering time; the overexpression of

5.3 DELLAs Integrating GA Regulation of Flowering With Salt

20 H.J. Park et al.

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 21

binds decreases with increasing temperature, suggesting that the H2A.Z

5.4 GI Integrating Photoperiod With Drought, Cold, and Salt

22 H.J. Park et al.

Table 2 Pleiotropic phenotypes of Arabidopsis gi mutants and functions of GI.

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 23

Table 2 Pleiotropic phenotypes of Arabidopsis gi mutants and functions of GI.—cont'd

24 H.J. Park et al.

Molecular Interactions Between Flowering Time and Abiotic Stress Pathways 25

activation of SOS1, a plasma membrane–localized Na+/H+ antiporter,

26 H.J. Park et al.

regulates cold stress response by controlling the expression of transcription