Journal of Plant Physiology 214 (2017) 1627

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Journal of Plant Physiology

journal homepage: www.elsevier.com/locate/jplph

Review article

Plant hormone signaling in owering: An epigenetic point of view MARK

Gerardo Campos-Rivero, Pedro Osorio-Montalvo, Rafael Snchez-Borges, Rosa Us-Camas,

Ftima Duarte-Ak, Clelia De-la-Pea
Unidad de Biotecnologa, Centro de Investigacin Cientca de Yucatn, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: Reproduction is one of the most important phases in an organisms lifecycle. In the case of angiosperm plants,
Auxins owering provides the major developmental transition from the vegetative to the reproductive stage, and
DNA methylation requires genetic and epigenetic reprogramming to ensure the success of seed production. Flowering is regulated
miRNAs by a complex network of genes that integrate multiple environmental cues and endogenous signals so that
Histone modications
owering occurs at the right time; hormone regulation, signaling and homeostasis are very important in this
Flowering
Phytohormone
process. Working alone or in combination, hormones are able to promote owering by epigenetic regulation.
Some plant hormones, such as gibberellins, jasmonic acid, abscisic acid and auxins, have important eects on
chromatin compaction mediated by DNA methylation and histone posttranslational modications, which hints at
the role that epigenetic regulation may play in owering through hormone action. miRNAs have been viewed as
acting independently from DNA methylation and histone modication, ignoring their potential to interact with
hormone signaling including the signaling of auxins, gibberellins, ethylene, jasmonic acid, salicylic acid and
others to regulate owering. Therefore, in this review we examine new ndings about interactions between
epigenetic mechanisms and key players in hormone signaling to coordinate owering.

1. Introduction
Successful reproduction ensures a species survival. All organisms
humans, animals, insects, plants, fungi need to reproduce, either
sexually or asexually. In the case of angiosperms, owering is the major
developmental transition from the vegetative to the reproductive stage,
and requires genetic and epigenetic reprogramming throughout seed
production (Amasino, 2010; Andrs and Coupland, 2012; Blmel et al.,
2015). Internal and external factors such as day length (photoperiod-
ism), temperature (vernalization), and hormones mediate the initiation
of cell dierentiation in the apical meristem in order to achieve each
reproductive stage (Amasino, 2010; An et al., 2004; Burgarella et al.,
2016; Kazan and Lyons, 2016; Reeves and Coupland, 2001; Sun et al.,
2014).
In Arabidopsis thaliana, the transition from the vegetative to the
reproductive stage is made by the suppression of leaf production and
the establishment of a oral fate in the apical meristems (Koornneef
et al., 1998). When the plant has passed from the juvenile to the adult
phase and from the vegetative to the reproductive stage, the plant can
be induced to ower. Flowering is regulated by an integrated network
of several chemical and genetic pathways, where CONSTANS (CO) in
the presence of light is a key regulator of ower promotion through the
activation of FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVER-
EXPRESSION OF CONSTANS 1 (SOC1) in long-day (LD) conditions
(Putterill et al., 2004; Samach et al., 2000; Suarez-Lopez et al., 2001;
Valverde et al., 2004). FT is a crucial mobile signal known as origen
that activates meristem identity genes and SOC1, which encodes to a
MADS-box transcription factor, is present in the inorescence meristem
(Kardailsky et al., 1999; Kobayashi et al., 1999; Samachet al., 2000;
Turck et al., 2008). SOC1, although it is activated by CO, can also be
repressed by FLOWERING LOCUS C (FLC), a repressor of the oral
transition (Michaels and Amasino, 1999, 2001; Mouradov et al., 2002).
On the other hand, in short-day (SD) conditions, Heading date (Hd) 1
and 3a encode genes similar to those found in the long-day pathway.
Hd1 encodes to an orthologue of Arabidopsis CO, while Hd3a is similar
to FT (Kojima et al., 2002; Yano et al., 2000). The owering time the
timing of the transition from vegetative to reproductive development
is aected by environmental conditions as well as hormonal action
(Davies, 1995; Denay et al., 2017; Koornneef et al., 1998).
Dierent studies indicate the importance of the interactions among
dierent plant hormones, such as ethylene (ET), indole-3-acetic acid
(IAA), cytokinins (Cks) and abscisic acid (ABA) for ower induction in

Corresponding author at: Unidad de Biotecnologa, Centro de Investigacin Cientca de Yucatn, Calle 43 No. 130 x 32 y 34, Col. Chuburn de Hidalgo, 97205 Mrida, Yucatn,
Mexico.
E-mail addresses: ingcampos43@gmail.com (G. Campos-Rivero), pedro.osorio@cicy.mx (P. Osorio-Montalvo), rcsb88@gmail.com (R. Snchez-Borges),
rosa.us@cicy.mx (R. Us-Camas), fatima.duarte@cicy.mx (F. Duarte-Ak), clelia@cicy.mx (C. De-la-Pea).

http://dx.doi.org/10.1016/j.jplph.2017.03.018
Received 10 October 2016; Received in revised form 6 March 2017; Accepted 29 March 2017
Available online 31 March 2017
0176-1617/ 2017 Elsevier GmbH. All rights reserved.
G. Campos-Rivero et al.
A. thaliana (Domagalska et al., 2010; Matsoukas, 2014), apples (Sanyal
and Bangerth, 1998) and Pharbitis nil (Frankowski et al., 2014; Ksy
et al., 2008). It is also known that hormonal signaling has an important
role in owering through the regulation of FLC, CO and FT. For
instance, salicylic acid (SA) is involved in the regulation of the
transcription of CO, FLC, FT and SOC1 (Martnez et al., 2004).
Intriguing discoveries have shown that the late owering phenotype
of SA-decient plants correlates with a 23-fold expression of FLC,
decreasing the levels of FT compared with wild-type plants in LD or SD
conditions. Furthermore, the dynamic change in the expression of these
genes involves chromatin modications (Berr et al., 2015; Blmel et al.,
2015, Hepworth and Dean, 2015; Kang et al., 2015; Pic et al., 2015;
Sun et al., 2014). For instance, the expression of FLC and FT in
Arabidopsis are epigenetically regulated (Hepworth and Dean, 2015;
Ietswaart et al., 2012; Swiezewski et al., 2009). Some reports highlight
the function of the Polycom Repressive Complex 2 (PRC2) in the
silencing of the oral repressor FLC locus by the histone mark
H3K27me3 during a prolonged period of cold (Buzas et al., 2011; De
Lucia et al., 2008; Yuan et al., 2016), while others claim that the
regulation of FLC is accomplished by the reduction of H3K4me2 levels
in this gene (Liu et al., 2010; Liu et al., 2007a). In fact, both regulatory
histone marks are involved in the regulation of FLC by a coordinated
association of the PRC2 and Flowering Locus D (FLD) complexes (Shaq
et al., 2016). FLD gene encodes a histone demethylase that mediates the
enzymatic demethylation of H3K4me2 and facilitates deacetylation of
histone H4 in FLC chromatin (Liu et al., 2007a), although Jin et al.
(2008) found that the sumoylation/desumoylation activity of FLD could
control histone acetylation/deacetylation by an unknown mechanism.
2. Epigenetic modications and plant hormone regulation in
owering
Covalent modication of cytosine residues by DNA methyltransfer-
ase enzymes allows the incorporation of a methyl group at the 5
position of the pyrimidine ring of the cytosines in order to establish the
DNA methylation state of the chromatin (Allis et al., 2015; Bird, 1986;
De-la-Pea et al., 2015). Histone modications phosphorylation,
acetylation, methylation, ubiquitination, etc. also work on chromatin
compaction by writers and erasers that can modify the histone tails
of the nucleosome (Allis et al., 2015). On the other hand, miRNAs,
which are small, endogenous and non-translated single-strand RNA
(2124 nucleotides), can regulate gene expression by guiding the
cleavage of complementary mRNA targets (Bartel, 2004; Jones-
Rhoades et al., 2006). Epigenetic mechanisms, which regulate tran-
scription acting on chromatin conformation that are determined by
DNA methylation, histone posttranslational modications and chroma-
tin remodeling, have been documented in owering (Jeong et al., 2015;
Liu et al., 2016; Teotia and Tang, 2015) and hormone regulation
(Yamamuro et al., 2016). Also, a recent review examined the participa-
tion of miRNAs during these processes (Hong and Jackson, 2015; Liu
et al., 2009). Therefore, for this review, we chose to focus on how DNA
methylation, histone modications and miRNAs cooperate with plant
hormone signaling to coordinate owering in higher plants.
2.1. Auxins
The plant hormone auxin is necessary for normal plant growth and
development, as it regulates a variety of developmental processes such
as cell elongation and division, organ patterning, root and shoot
development and tropic responses to light and gravity (Dinesh et al.,
2016; Kasahara, 2015). In higher plants, the main natural auxin is
indole-3-acetic acid (IAA), which is synthesized in young leaves,
cotyledons, expanding leaves and root tissues (Ljung et al., 2001);
however, indole-3-butyric acid (IBA) and 4-chloroindole-3-acetic acid
(4-Cl-IAA) are also natural auxins. The synthetic auxins naphthalene-1-
acetic acid (NAA) and 2,4-dichlorophenoxyacetic acid (2,4-D) are
17
Journal of Plant Physiology 214 (2017) 1627
metabolically more stable and commercially available and are highly
used in plant in vitro culture techniques. Nevertheless, they do not share
their mechanism of action with native IAA (Simon and Petrsek, 2011),
and the concentrations used for in vitro purposes could have dierent
outcomes (Us-Camas et al., 2014).
The exposure to dierent concentrations of synthetic auxins causes
epigenetic changes that aect the normal development of owers
(Jaligot et al., 2000). For instance, the mantled phenotype of the
African oil palm (Elaeis guineensis Jacq.), which is characterized by
abnormalities in its oral development, can result in altered sensitivity
and/or response to the auxins/cytokinin ratio (Eeuwens et al., 2002;
Jaligot et al., 2011). The appearance of mantled owers was found to
increase when high concentrations of kinetin (0.25 mg l1) and low
concentrations of the synthetic auxin NAA (0 or 0.1 mg l1) were used.
On the contrary, when high levels of NAA (0.5 mg l1) were used, a
reduced incidence of mantled owers was observed (Eeuwens et al.,
2002). It has been suggested that kinetin induces DNA hypomethyla-
tion, generating the mantled phenotype, while NAA causes DNA
hypermethylation, resulting in the opposite phenotypic eect
(Eeuwens et al., 2002; Jaligot et al., 2011; Jaligot et al., 2000). There
is a positive correlation between a reduction in global DNA methylation
(from 5% to 2.5%) and the appearance of the mantle phenotype (Jaligot
et al., 2000).
A strict control of auxin homeostasis and the maintenance of an
appropriate level of IAA is important for normal growth and develop-
ment (Davies, 2010). IAA is transported to the growing regions and,
normally, high IAA content correlates with intense cell division (Ljung
et al., 2001; Tanaka et al., 2006). The polar movement of IAA allows a
dierential distribution or gradient of auxin within the plant tissues,
and these changes are dynamic during developmental processes such as
owering (Cheng and Zhao, 2007; Tanaka et al., 2006). PIN-FORMED
(PIN) proteins are important components of auxin eux and their
subcellular localization guides the ow of auxins (Tanaka et al., 2006).
In Arabidopsis, the pin-formed mutant pinl-1, which disrupts the normal
polar transport of auxins, fails to form the oral primordia and presents
a pin-shaped inorescence devoid of owers (Okada et al., 1991). This
condition can be reversed when IAA is applied exogenously, inducing
oral formation (Reinhardt et al., 2000). The met1-6 mutants also
present defects in the establishment of an auxin gradient, a highly
perturbed PIN1 promoter activity, and a late-owering phenotype (Xiao
et al., 2006). Floral primordium initiation not only requires a local
maximum of auxin but also the activity of AUXIN RESPONSE FACTOR
MONOPTEROS (MP/ARF5) (Przemeck et al., 1996; Yamaguchi et al.,
2013) and, like PIN1 mutants (Okada et al., 1991), MP mutants form
naked inorescence stalks lacking owers (Przemeck et al., 1996). MP
targets are key regulators of oral growth initiation such as LFY,
AINTEGUMENTA (ANT) and AINTEGUMENTA-LIKE 6 (AIL6) (Elliott
et al., 1996; Krizek and Eaddy, 2012; Schultz and Haughn, 1991; Wu
et al., 2015; Yamaguchi et al., 2013). Wu et al. (2015) suggest that
under high levels of auxin, MP recruits SWI/SNF proteins, implicated in
transcriptional control via chromatin remodeling, to regions of chro-
matin that contain genes involved in ower formation. This changes the
chromatin state that enables the transcriptional activation of genes
promoting the initiation of ower primordium (Wu et al., 2015).
The involvement of histone modications in the transcriptional
regulation of auxin target genes has also been documented (Wu et al.,
2015). It has been reported that auxin treatments lead to an increase of
H3K9ac in LFY and FILAMENTOUS FLOWER (FIL) loci, which causes an
increase in mRNA accumulation of both genes, promoting oral
primordium initiation (Wu et al., 2015). On the other hand, only in
the absence of auxin application do the transcriptional co-repressor
TOPLESS (TPL) and HDA19 occupy the MP-bound sites at the LFY and
FIL in the inorescence apices, preventing transcription of these genes
(Wu et al., 2015). SWI/SNF ATPases subgroup BRAHMA (BRM) and
SPLAYED (SYD) activities increase in accessibility at the MP target for
ower primordium initiation. Plants generated using syd-5 mutants
G. Campos-Rivero et al. Journal of Plant Physiology 214 (2017) 1627

Fig. 1. Participation of cytokinins (Cks), DNA methylation and miRNAs in oral transition. In the vegetative stage, the plant has low levels of Cks due to CKX action, a cytokinin oxidase
involved in CK catabolism. During ower initiation, the endogenous biosynthesis of dihydrozeatin riboside and isopentenyladenine, two kinds of Cks involved in cell growth and
expansion in the oral bud, increases; the levels of DNA methylation as well as auxins decrease while the expression of ARF6 and ARF 8 are reduced due to the action of miR167. When the
oral organs are formed, the levels of DNA methylation rise, as well as the expression of ARF6 and ARF8.

display a dramatic owerless state known as pins that is characteristic
of auxin pathway mutants (Wagner and Meyerowitz, 2002; Wu et al.,
2015). ChIP analysis in the inorescences show that MP and BRM/SYD
exhibit a similar binding pattern in the loci of regulators of ower
primordium initiation FYC, FIL, ANT and TARGET OF MONOPTEROS 3
(TMO3), and this pattern is required for their transcriptional activation
(Wu et al., 2015).
On the other hand, the signaling pathway in response to auxin has
also been regulated by miRNAs. MiR393 targets ve genes that belong
to the TRANSPORT INHIBITOR RESPONSE 1 (TIR1) family (Sunkar and
Zhu, 2004), a positive regulator of auxin signaling. These genes target
the ARF transcriptional repressor, AUXIN/INDOLE-3-ACETIC ACID
(Aux/IAA), for degradation (Quint and Gray, 2006; Tan et al., 2007).
MiRNAs are complementary to several members of the ARF family and
direct theirs mRNA cleavage (Jones-Rhoades and Bartel, 2004; Rhoades
et al., 2002). MiR167 targets ARF6 and ARF8, while miR160 targets
ARF10, ARF16 and ARF17 (Allen et al., 2005; Kasschau et al., 2003;
Mallory et al., 2005; Rhoades et al., 2002). The Gretchen Hagen 3
(GH3)-like early auxin response encodes auxin-conjugating proteins.
Proper transcriptional regulation of this response requires that ARF17
mRNA levels be regulated by miR160 (Mallory et al., 2005; Park et al.,
2007; Staswick et al., 2005). 5mARF17 plants have ve mutations
within the miR160-complementary domain of an ARF17 genomic clone.
These plants have an increase in the levels of expression of ARF17, and
show a reduced accumulation of GH3.5 and several oral defects,
including accelerated owering time, reduced petal size, abnormal
stamen structure, rosette serration and reduced fertility (Mallory et al.,
2005). On the other hand, transgenic plants expressing a miR160-
resistant form of ARF10, which has four mutations in the miR160 target
site within ARF10, have owers with elongated and contorted petals
and twisted siliques (Liu et al., 2007b).
2.2. Cytokinins
Cks are N6-substituted purine derivate molecules that function as
growth regulators and are involved in many developmental and
physiological processes, regulating the proliferation and dierentiation
of plant cells and delaying senescence in owering plants (Perilli et al.,
2010). The involvement of Cks during oral transition has not been
dened completely, but it is known that they control cell division and
dierentiation in the oral meristem (Jacqmard et al., 2003). In
Arabidopsis, it was found that the Ck homeostasis aects Ck accumula-
tion in the meristem, regulating the size and activity of the shoot apical
meristem. One important aspect of CK homeostasis is its degradation.
Among the cytokinin oxidase/dehydrogenase enzymes (CKX) that
catalyze the degradation, CKX3 and CKX5 are involved in the regula-
tory activity of the reproductive meristems of A. thaliana (Bartrina
et al., 2011). ckx3 ckx5 double mutants form larger inorescence and
oral meristems, and normally the expression of CKX3 and CKX5 in the
WT is focused on the central WUSCHEL domain and a broad region of
the meristem, respectively. Therefore, the phenotype observed in these
double mutants and the Bartrina et al. (2011) expression analysis
suggest that the Ck signal denes the stem cell niche and delays cellular
dierentiation (Bartrina et al., 2011). In fact, in Arabidopsis it has been
observed that when the oral stimulus starts, the endogenous content of
Ck in leaves and phloem sap increases rapidly (Corbesier et al., 2003;
Stern et al., 2003). On the other hand, exogenous Ck application to
vegetative plants that grow in SD can induce various cellular and
molecular changes associated with oral transition (Bernier et al.,
2002).
There are few studies that connect Ck with epigenetic regulation of
the owering process; in fact, the participation of Ck in epigenetic
mechanisms is not completely understood. In azalea, the Ck dihydro-
zeatin riboside and isopentenyladenine are associated with the end of
dormancy and the initiation of owering through DNA methylation

18
G. Campos-Rivero et al.
(Meijon et al., 2011). Meijon et al. (2011) observed that global DNA
methylation levels decrease before ower initiation; however, when the
oral organs are formed the global DNA methylation suers a
hypermethylation. The authors suggest that Ck is an epigenetic factor
that might control gene expression during oral transition, proposing
that Ck induces demethylation (Fig. 1). Li et al. (2008) found a delayed
owering phenotype in Arabidopsis knockdown mutants of SAHH (S-
adenosyl-L-homocysteine hydrolase) that could be related to a reduc-
tion in DNA methylation, which aects Ck signaling genes. SAHH is a
key enzyme in maintenance of the methylation that in Arabidopsis
mutants provokes the overproduction of Ck, avoiding owering (Li
et al., 2008).
However, previous work in Arabidopsis suggests an important role
for Ck in epigenetic regulation via histones (Kim et al., 2013). In the
SDG2 mutants sdg2-5, a decrease in transcript levels of a cytokinin
inducible gene, ARABIDOPSIS RESPONSE REGULATOR 9 (ARR9), was
observed. Furthermore, in WT (Col-0 ecotype) the application of
100 M of zeatin for 30 min led to an increase in H3K4 trimethylation
in the ARR9 coding region, along with an increase in H3K9/14
acetylation (Kim et al., 2013). This result suggests that the histone
H3K4 methyltransferase SDG2, and probably a histone acetylase, are
required for ARR9 activation upon hormone treatment, and the Cks
would participate in the regulation of hormone responsive genes.
The regulation of Ck by epigenetic control via miRNAs during the
owering process has been observed in an indirect form, since the
process depends on auxin interaction. The expression of AUXIN
RESPONSE FACTORS ARF6 and ARF8 in oral organs of Arabidopsis is
regulated by miRNA167 (Wu et al., 2006), and increased levels of
miRNA167 result in the same oral phenotypes as reduced ARF6/8
expression (Ru et al., 2006). These defects were observed in arf6 arf8
double mutants (Rubio-Somoza and Weigel, 2011). These mutants
present owers with retarded organ development in the three outer
whorls, the sepals, petals, and anthers. ARF6 and ARF8, which regulate
ower maturation (Nagpal et al., 2005), modulate the expression of
auxin-related genes, but they are involved in limiting the extent of Ck
activity in the meristem, and thus some of the oral defects in the
meristems of arf6 arf8 double mutants can be attributed to a decrease in
auxin activity and an increase of Ck activity in the meristem (Rubio-
Somoza and Weigel, 2011). The consequence of ARF6/8 deciency is
the expanded expression of positive meristem regulators involved in Ck
action, such as class 1 KNOTTED1-LIKE HOMEOBOX (KNOX1) genes,
SHOOTMERISTEMLESS (STM) and BREVIPEDICELLUS (BP) (Tabata
et al., 2010). Also, it has been suggested that KNOX1 and BP can be
repressed by the accumulation of auxins (Hay et al., 2006; Tabata et al.,
2010). Therefore, there is a crosslink between Ck activity and ARF
regulation controlled by auxin players via miRNA167 (Fig. 1).
On the other hand, in Arabidopsis, miRNA172 overexpression
causes early owering and defects in oral organ identity (Park et al.,
2002b), and it has been suggested that this miRNA regulates owering
time and oral organ identity by down-regulating APETALLA 2 (AP2)-
like target genes (Aukerman and Sakai, 2003). AP2 is a oral meristem
identity gene controlling Arabidopsis ower homeotic gene expression,
ower development and seed development. AP2-like genes such as
TARGET OF EAT1 (TOE1) and TOE2, which contain putative miR-
NA172 target sites, are involved in owering repression and cause late
owering (Aukerman and Sakai, 2003). The down-regulation of
miRNA172 by Cks, which results in an increased AP2 protein level,
was found to lead to oral patterning defects that include proliferation
of numerous petals, stamens and carpels, indicating loss of oral
determinacy (Aukerman and Sakai, 2003; Liu and Chen, 2009). It is
worth mentioning that miRNA172 is also induced by ABA (Han et al.,
2013) (see below).
2.3. Gibberellins
GAs regulate seed development, stem elongation, leaf expansion
19
Journal of Plant Physiology 214 (2017) 1627
and oral transition (MacMillan, 2001) and they have an important role
in one of the major owering pathways (Teotia and Tang, 2015). Many
GAs have been reported in plants but only GA1, GA3, GA4 and GA7
function as bioactive hormones; non-bioactive forms act as precursors
for the bioactive and are inactive metabolites (MacMillan, 2001;
Yamaguchi, 2008). In plants, GA1 is the main bioactive form, found
in dierent tissues, that controls dierent development processes such
as seed germination, stem elongation, leaf growth and ower develop-
ment (MacMillan, 2001; Yamaguchi, 2008).
GAs are closely associated with DELLA proteins such as GAI (GA-
insensitive), RGA (Repressor of ga1-3), RGL1 (RGA-like 1), RGL2 and
RGL3, key transcriptional regulators inhibiting GA responses in
Arabidopsis (Hussain and Peng, 2003; Sun and Gubler, 2004). GAI
and RGA are repressors of plant growth that can be antagonized by GA
addition (Koornneef and van der Veen, 1980). GAs regulate develop-
ment and fertility of owers by suppressing the function of DELLA
proteins (Cheng et al., 2004). Moreover, the loss of activity of any of the
components of GA biosynthesis and signaling can cause defects in
owering (Iuchi et al., 2007; Sun and Kamiya, 1994; Wilson et al.,
1992). For instance, ga1-3 (gibberellin-insensitive1-3) mutants are de-
cient in the GA1 gene, which encodes to a ent-kaurene synthetase an
enzyme involved in the rst step of GA biosynthesis and either never
ower, or show a delay in owering time during short-day conditions
(Sun and Kamiya, 1994; Wilson et al., 1992).
Although there is little evidence linking DNA methylation and GA,
there are interesting indications of the pharmacological eects of GA
biosynthesis inhibitors (chlormequat chloride and paclobutrazol) and a
DNA methylation inhibitor (5-azacytidine) in owering as well as DNA
methylation content. For instance, in azalea, the application of chlor-
mequat chloride and paclobutrazol causes a signicant decrease in 5-
mdC (5-methyldeoxycytidine) levels (more than 5%), disturbing the
levels of several GAs (GA1, GA3, GA4, GA7, GA9; GA20) during oral
transition (Meijon et al., 2011). On the other hand, 5-azacytidine
treatment in precocious trifoliate orange (Poncirus trifoliata L. Raf)
induces the expression of the LEAFY homologue gene (CiLFY) (Zhang
et al., 2014). It is known that LFY gen is a central regulator of owering
that controls the switch from a vegetative to a reproductive phase
during plant development, and its expression is induced by GAs
(Blazquez et al., 1997). Accordingly, locus-specic methylation analysis
of the CiLFY indicated that the proportion of the three dierent DNA
methylation cytosine-sequenced contexts (CG, CHH and CHG; where H
is A, T or C) were reduced during the early owering of precocious
trifoliate orange, suggesting that in this perennial plant demethylation
events occur during the transition from the juvenile to the adult stage
(Zhang et al., 2014).
In the case of HPMs, a genome-wide proling has revealed that
many genes in the GA pathway were dierentially regulated by
H3K27me3 (Charron et al., 2009; Zhang et al., 2012). PICKLE (PKL)
encodes a putative ATP-dependent Chromodomain-Helicase-DNA-bind-
ing domain (CHD3), a chromatin remodeling enzyme in A. thaliana that
promotes H3K27me3 (Zhang et al., 2008; Zhang et al., 2007). The Pkl
mutant presented increased owering time and delayed anther dehis-
cence, similar phenotypes to those observed in mutants with defects in
the GA biosynthesis or response (Ogas et al., 1999). Henderson et al.
(2004) found that the exogenous application of GA3 to pkl plants
reduced the owering time for more than a week compared with the
control pkl plants. However, when endogenous levels of bioactive GA
forms were measured in the pkl plants, they did not show any reduction,
suggesting that PKL is involved in the perception but not in the
biosynthesis of GA. All of these results suggest an important role in
chromatin structural modications for GA biosynthesis and signaling
response that can regulate owering. GA promotes the destruction of
DELLA (Fu et al., 2004; Harberd, 2003), while reduced GA levels cause
increases in accumulation of DELLA (King et al., 2001; Silverstone
et al., 2001). A very recent report found that there is a close interaction
between DELLA proteins and PKL in the regulation of GA signaling
G. Campos-Rivero et al.
Fig. 2. The molecular mechanism suggested for FLOWERING LOCUS C (FLC) expression through the regulation of DELLA proteins mediated by gibberellins (GA). Reduced GA levels cause
increases in accumulation of DELLA, while increasing levels of GA promote the destruction of DELLA. DELLA proteins interact with FLC, repressing owering transition by inhibiting FT
and SOC1. DELLA proteins interact with the chromatin remodeling protein PICKLE (PKL), which recruits PRC2, in the regulation of GA signaling, presumably by the increase of the
repressing mark H3K27me3.
(Park et al., 2017), presumably by the increase of the repressing mark
H3K27me3 (Zhang et al., 2012; Zhang et al., 2008). In a dierent study,
it was found that DELLA proteins can also interact with FLC to repress
owering transition (Li et al., 2016a). However, it is now known that
FLC chromatin can be silenced by the histone mark H3K27me3 due to
the action of PRC2 (Buzas et al., 2011; De Lucia et al., 2008; Yuan et al.,
2016). Furthermore, there is an indirect regulation of PcG target genes
by PKL (Aichinger et al., 2011). Therefore, in a hypothetical model, it is
very likely that DELLA proteins interact with PKL, which recruits PRC2.
Thus, PRC2 increases H3K27me3 levels in FLC, which regulate target
genes such as FT and SOC1 (Fig. 2).
Another important player in response to GA is GAMYB, a highly
conserved family of R2R3 MYB transcription factors implicated in the
GA signaling pathway and owering (Gocal et al., 2001; Woodger et al.,
2003). GAMYB binds to the GA-responsive elements of the -amylase
genes in aleurone cells (Gubler et al., 1999). In Arabidopsis, three
GAMYB-like genes, AtMYB33, AtMYB65, and AtMYB101, have been
reported (Gocal et al., 2001). The three GAMYB-like genes show
dierent expression patterns, with AtMYB33 predominantly expressed
in oral primordia, followed by ovules, immature anthers, and pollen
(Gocal et al., 2001). It was found that miR159 regulates the mRNA that
encode to the GAMYB protein by directing the cleavage of AtMYB33
transcripts that regulate owering by mediating GA responsiveness of
the LFY promoter (Achard et al., 2004). Over-expression of miR159a
causes a delay in owering time and generates a decrease in MYB33 and
LFY transcript levels; also, AtMYB33 can bind in vitro to the LFY
promoter (Achard et al., 2004). In rice, miR159 mediates the cleavage
of OsGAMYB and OSGAMYB- like genes (OsGAMYBL1) in anthers but
not in aleurone cells. During the dierent stages of anther development,
a negative correlation was found between a down-expression of miR159
and the levels of mRNAs for OsGAMYB and OsGAMYBL1. Also,
transgenic plants that over-express miR159 show more severe oral
abnormalities than the gamyb-1 mutant. These owers have malformed
shrunken and whitened anthers, a much-reduced lemma and palea, do
not develop stamen and pistil primordia, and are male-sterile (Tsuji
et al., 2006).
2.4. Abscisic acid
ABA is a sesquiterpenoide phytohormone involved in growth and
developmental processes, including the synthesis of seed storage
proteins and lipids, seed desiccation tolerance, and seed dormancy
and owering (Finkelstein, 2013; Shu et al., 2016; Trivedi et al., 2016).
It is known that some of the main exogenous factors inducing owering
20
Journal of Plant Physiology 214 (2017) 1627
are temperature and water stress. In some cases, water stress causes
early owering in Arabidopsis, probably by ABA accumulation in
response to this stress (Su et al., 2013; Verslues and Zhu, 2005; Wang
et al., 2013), and in other cases it can extend the vegetative stage by a
DELLA-dependent mechanism (Achard et al., 2006). During other kind
of stresses such as drought or high temperatures, ABA is more related to
the stomatal closing response (Shinozaki and Yamaguchi-Shinozaki,
2007). The loss of water can also trigger a response known as drought
escape (DE) (Sherrard and Maherali, 2006), which is a strategy
inducing early owering and seed production before the drought
becomes too severe (Su et al., 2013). Although ABA has been related
mostly to water stress, this hormone has also been considered as a oral
repressor, such as in the case of Arabidopsis, where it has been shown
that applying exogenous ABA delays owering time (Wang et al.,
2013). The overexpression of ABI5, an ABSCISIC ACID-INSENSITIVE
MUTANT 5, delays owering initiation by up-regulating FLC expression
(Wang et al., 2013). ABA INSENSITIVE 3 and 5 genes, which encode to
B3-type and basic leucine zipper (bZIP)-type transcription factors,
respectively, can regulate owering (Brocard et al., 2002; Finkelstein
et al., 2002; Hauser et al., 2011). Another protein that participates in
the control of owering is ABA HYPERSENSITIVE 1 (HAB1) (Saez et al.,
2004), a phosphatase type 2Cs (PP2Cs) and a negative regulator of ABA
signaling (Rodriguez et al., 1998). HAB1 expression has been found to
induce owering in Arabidopsis (Saez et al., 2004). Interestingly, the
same research group found that HAB1 interacts with the chromatin-
remodeling complex SWI/SNF (Saez et al., 2008). The authors conclude
that the nuclear interaction of HAB1 and the SWI/SNF chromatin
remodeling complex in the ABA-induced transcription is necessary for
ABA-responsive gene regulation.
Chromatin remodeling also involves modications in the histone
core, and it has been observed that in response to low temperature
stress, the levels of acetylation of histone H3 increase along with the
concentration of ABA (Bond et al., 2009). Another histone modication
implicated in the control of owering is H3K4me3. This histone
methylation, performed by the trithorax-like factor ATX1, has been
implicated in the regulation of ABA-dependent and independent
pathways (Ding et al., 2011). Furthermore, two genes E(Z) enhancer
of Zeste in rice, SDG711 and SDG718, which encode the PRC2, required
for H3K27me3, play a role in owering gene regulation in LD and SD
(Liu et al., 2014). The expression of SDG711 is induced under LD, while
that of SDG718 is induced under SLiu et al. (2014) found that both E(Z)
genes are able to repress OsLF, which is a repressor of Hd1 (Zhao et al.,
2011) (Heading date 1, an ortholog of the Arabidopsis CO promoter of
owering during SD), through an accumulation of H3K27me3 in OsLF
G. Campos-Rivero et al.
loci. Therefore, when SDG711 and SDG718 repress OsLF, Hd1 can be
expressed to promote owering. The function of these E(Z) genes
indicates that PRC2 are mediated by epigenetic repression of genes
involved in the photoperiod control of owering (Kim et al., 2007; Liu
et al., 2014).
Various miRNAs have also been documented to be involved in
owering by means of ABA signaling and regulation. For instance,
miR159, which is involved in oral development, controls the expres-
sion of MYB101 and MYB33 transcription factors by mediating their
cleavage and is also regulated by ABA (Achard et al., 2004; Gocal et al.,
2001; Reyes and Chua, 2007). MiR160, which controls oral morphol-
ogy by modulating the expression of an ARF10, is a potential ABA
regulatory miRNA molecule induced by ABA (Liu et al., 2007b; Yaish
et al., 2011). On the other hand, the overexpression of miR172c leads to
the reduction of water loss and the promotion of early owering by
modulating the expression of genes FT and LFY during conditions of LD
(Li et al., 2016b). It has been found that miR172, induced by ABA,
confers tolerance to drought by increasing sensitivity to ABA, speeding
up the drought response (Han et al., 2013).
2.5. Ethylene
ET is another important phytohormone related to processes of fruit
ripening, senescence of leaves, response to stress and the timing of
owering (Achard et al., 2007; Johnson and Ecker, 1998). ET is an
organic chemical compound consisting of only two carbon atoms linked
by a double bond, and it is present in all plant tissue, although the rate
of synthesis is tissue specic and depends on the state of development.
The synthesis of ET is increased in response to damage, and during
ripening and leaf excision, and it has been demonstrated that ET can
inhibit owering in Arabidopsis and P. nil (Frankowski et al., 2014;
Harpham et al., 1991; Ksy et al., 2008; Kieber, 1997). The role of
ethylene under SD has been described in P. nil as controlling owering
time (Frankowski et al., 2014). Arabidopsis mutants compromised in ET
biosynthesis are early owering (Tsuchisaka et al., 2009). Constitutive
triple response1(ctr1) mutants, which exhibit constitutive ET signaling,
are late owering under SD (Adams-Phillips et al., 2004). ET is thought
to delay owering by promoting the accumulation of DELLA proteins,
thereby interfering with the GA owering promotion pathway (Achard
et al., 2007).
During periods of cold, owering is delayed until conditions return
to normal; apparently the signal to delay may be given by ET (Alonso
and Ecker, 2001). These cold periods generate responses in regulating
both chromatin remodeling and the activation of miRNAs that control
the process of owering during the vernalization process, during which
ET is responsible for inhibiting owering in Arabidopsis and P. nil
(Crvecoeur et al., 2004; Fornara et al., 2010; Ksy et al., 2008). In
some cases, ET promotes owering. For instance, in Aechmea fasciata it
is speculated that a small burst of ET synthesis in the meristem triggers
owering, as in other bromeliads (Cong et al., 2013; Li et al., 2016c).
Changes in the transcriptome were reported in response to ET. The
analysis of the transcriptome reveals that some transcription factors are
upregulated in the adult plant and result in owering. Moreover, the
dierential expression of GI, DELLA, FT, AP2 and others indicated that a
complicated network participated in the induction of owering by ET
(Li et al., 2016c).
There is some evidence for a relation between epigenetic regulation
and synthesis of ET (Zhou et al., 2005). It is known that during cold
stress, the levels of ET increase, which may be related to processes of
vernalization (Chu and Lee, 1989; Zhao et al., 2014), which in many
cases are regulated by methylation or demethylation of DNA (Burn
et al., 1993; Sherman and Talbert, 2002; Yaish et al., 2011). In
Arabidopsis, the increase in ET due to cold temperatures can delay
bloom; however, once the temperature is again optimal, owering is
induced (Achard et al., 2007). On the other hand, it is known that the
expression of HDA6 and HDA19 (HDACs of Arabidopsis) can be induced
21
Journal of Plant Physiology 214 (2017) 1627
by ethylene (Zhou et al., 2005). In A. thaliana, HDA6 upregulates the
expression of FLC (Wu et al., 2008). In Brassica napus, HAD19 connects
the hormone response to pathogen pathways and oral induction
through a common epigenetic mechanism in response to changes in
the sensitivity to ethylene. The overexpression of HDA19 resulted in
increased expression of ethylene-regulated, pathogenesis-related genes
and increased the resistance to pathogen attack but delayed owering
time (Zhou et al., 2005). It is known that HAD19 can interact with
bnKCP1 (a putative factor harboring a kinase-inducible domain), which
is induced by cold and highly expressed in owers (Gao et al., 2003).
There is evidence in roses (Rosa hybrida Samantha) of the function
of ethylene in the control of ower development and owering time. ET
plays an important role in regulating petal cell expansion during the
rose ower opening (Ma et al., 2008). Changes in the expression of
miRNAs in response to ethylene have been described in rose, with ve
miRNAs (miR156, miR164, miR166, miR139) showing a close relation-
ship with ethylene and control of petal growth (Pei et al., 2013a).
Furthermore, RhNAC100, a homologous Arabidopsis transcription acti-
vation factor and cup-shaped cotyledon-domain transcription factor
gene, is rapidly induced by ethylene, and its accumulation reduces petal
size (Pei et al., 2013b). Pei et al. (2013a,b) suggest that ethylene
regulates cell expansion of the petals by ne-tuning the miRNA164/
RhNAC100. Thus, the growth of the ower is regulated by ethylene
signaling through the production of miRNAs. In Arabidopsis, miR166 is
dynamically controlled in its regulation of shoot apical meristem and
oral development (Jung and Park, 2007). Liu et al. (2009) describe a
set of miRNA that demonstrated down- and up-regulation when rice
was exposed to phytohormones. Two miRNAs showed response to
ethylene: the miR159, which was downregulated, and miR394, which
was up-regulated. There is evidence that miR159 is involved in the
control of owering time and is down-regulated by ethylene (Jin et al.,
2013; Liu and Chen, 2009; Liu et al., 2009). Ethylene down-regulates
miR159, promoting both the accumulation of GAMYB and owering by
reducing FLY expression (Liu and Chen, 2009).
2.6. Salicylic acid
SA belongs to a diverse group of phenolic compounds with an
aromatic ring and a hydroxyl group or its functional derivatives
(Raskin, 1992). It is believed that SA is a natural derivative of cinnamic
acid, an intermediate in the pathway, essential for the synthesis of the
phenolic compound shikimic acid. However, two possible pathways of
synthesis have been proposed: the decarboxylation of the cinnamic acid
side chain to generate benzoic acid, which undergoes hydroxylation at
the C-2 position, and the hydroxylation of cinnamic acid to o-coumaric
acid followed by its decarboxylation to SA. The conversion of cinnamic
acid to fumaric acid is catalyzed by the trans-cinnamate 4-hydroxylase
(Alibert et al., 1972). The synthesis of SA is regulated by PAL
(phenylalanineammonia-lyase) (Dixon and Paiva, 1995; Scott et al.,
2004), and this enzyme is involved in the regulatory mechanism of
stress-induced owering in P. nil (Wada et al., 2014; Wada et al., 2013).
SAs contribution to the regulation of owering has been known for
decades. Initially, it was found that 4 M of SA promotes the formation
of ower buds from tobacco callus (Lee and Skoog, 1965). The rst
suggestion that SA could act as an endogenous signal came from the
discovery of SA in the phloem of Xanthium strumarium L. during the
owering stage, but not in the vegetative stages (Cleland and Ajami,
1974). Furthermore, SA in concentrations of 310 M also stimulates
owering in various genera of the Lemnaceae family, plants under LD
and SD conditions, and plants insensitive to photoperiod (Khurana and
Cleland, 1992). However, subsequent studies have yielded contra-
dictory results on the role of SA in the induction of owering. In
2010, studies on Pharbitis nil suggested that owering was induced by
stress due to poor nutrition rather than light intensity. However, under
poor nutrition earlier owering was prevented by supplying amino-
oxyacetic acid (a phenylalanine ammonia-lyase inhibitor), but could be
G. Campos-Rivero et al.
restored by applying SA. Thus, it appears that in some plants SA is
necessary to induce owering, although not enough to induce it alone
(Wada and Takeno, 2010; Wada et al., 2010).
Moreover, exogenous application of 100 M of SA to Arabidopsis
wild-type plants causes a decrease in transcript levels of FLC, and the
irradiation of UV-C light-induced SA accumulation activates FT expres-
sion. Interestingly, although SA appears to be a repressor of the
expression of FLC, this process is not essential for the late owering
phenotype of SA-decient plants (Martnez et al., 2004). This adjust-
ment was discovered using mutant transgenic lines c-3 NahG, which
do not dier in owering time, compared to their parent plants grown
under LD and SD conditions. Similarly, the expression of other genes
such as CO and SOC1 in SA-decient plants is dierent in conditions of
SD and LD. For SA-decient plants grown in LD, transcript levels of CO
and SOC1 decreased by approximately 50% compared to the wild-type
plants. On the other hand, SA-decient plants grown in SD increased
the CO transcripts 23 times, but SOC1 expression did not change in
comparison with the wild-type plants (Martnez et al., 2004). Genetic
analysis of the interactions of these genes with SA during the photo-
period showed that exogenous SA (100 M) could reverse the late
owering phenotype of the mutant co-1, but this does not happen in the
mutant soc1 under LD. This evidence suggests that SA regulates
owering by interaction with the photoperiod-dependent pathway
through a separate CO-independent pathway (Martnez et al., 2004).
SUMO modication of target proteins in yeast and metazoans has
been implicated in the regulation of DNA repair, chromatin stability
and transcriptional regulation (Gill, 2005; Johnson, 2004). The SUMO
E3 ligase (SIZ1) gene is a key regulator of owering in Arabidopsis
through control of oral SA-mediated promotion, and the loss of
function in the mutant siz1 promotes an early owering phenotype.
This phenotype correlates with high levels of SA, expressing nahG
(bacterial salicylate hydroxylase), indicating that SIZ1 represses the
transition to owering mainly through suppressing SA-dependent oral
promotion signaling under SD (Jin et al., 2008) (Fig. 3). Interestingly,
increased FLC expression and late owering of the mutant owering
locus d (d) was not suppressed by siz1, suggesting that SIZ1 promotes
FLC expression by repressing FLD (an homolog of a human-lysine-
specic histone demethylase). Consistent with this, SIZ1 facilitates
sumoylation of FLD that can be suppressed by mutations in three
predicted sumoylation motifs in FLD. Furthermore, expression of
FLDK3R in d protoplasts strongly reduced FLC transcription compared
with the expression of FLD, and this was linked to reduced acetylation
of histone 4 in FLC chromatin (Jin et al., 2008). Therefore, SA not only
accelerates the transition from the vegetative to the reproductive phase
in stressed plants, but in non-stressed plants it is a regulator of
owering time. SA can act as a negative regulator of such oral
repressor genes as FLC and other components of the autonomous
owering pathway (Martnez et al., 2004; Wada et al., 2010).
Moreover, Pharbitisiss owering is induced by a single SD treat-
ment, and this induction is regulated by epigenetic mechanisms. It was
found that treatment with the DNA demethylating reagents 5-azacyti-
Fig. 3. The participation of salicylic acid (SA) in SUMO modication of FLOWERING LOCUS D (FLD). Low levels of SA promote the increase of the SUMO E3 ligase (SIZ1), which
facilitates sumoylation of FLD, decreasing its expression. Low expression of FLD promotes an increase in the activity of FLC, therefore repressing the transition to owering. On the other
hand, high levels of SA suppress the activity of SIZ1, increasing the expression of FLD and lowering the levels of FLC in order to promote owering.
22
Journal of Plant Physiology 214 (2017) 1627
dine and zebularine induce owering under LD conditions (Iwase et al.,
2010; Kondo et al., 2007; Takeno, 2010). This suggests that, under
stress conditions, the expression of PAL and the content of SA are up-
regulated, and this response induces DNA demethylation, controlling
the expression of owering-related genes.
2.7. Jasmonic acid
JA and its derivatives (named jasmonates) are lipid phytohormones,
oxygenated derivatives of linoleic and linolenic fatty acids (Wasternack
et al., 2013). The jasmonates biosynthetic pathway (the octadecanoid
pathway) has been extensively studied, and there is a wealth of
information about the type of enzymes involved in every step and
subcellular localization thereof (Berger, 2002; Mueller, 1997; Turner
et al., 2002). A key protein involved in JA signaling is JAZ, a
JAZMONATE ZIM-DOMAIN, which is a negative regulator of gene
expression induced by JA. On the other hand, COI1 (CORONATINE
INSENSITIVE 1) was identied in A. thaliana, and the corresponding
mutant coi1-1 is the most prominently controlled by JA signaling (Xie
et al., 1998). With the discovery of the JAZ proteins, it was possible to
explain the mechanism of JA perception, including identication of
(+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile) as the ligand of a JA receptor
(Fonseca et al., 2009).
JA and jasmonate molecules mainly have been described as signal-
ing molecules in plants that respond to stress, such as mechanical or
biotic injuries caused by exposure to ozone, drought or pathogen attack
(Berger, 2002; Farmer et al., 2003; Loyola-Vargas et al., 2012;
Overmyer et al., 2000; Rao et al., 2002). However, these are also
involved in various developmental processes such as nitrogen storage,
fruit ripening, senescence and owering (Creelman and Mullet, 1995;
Creelman and Mullet, 1997; Feussner et al., 1995; Staswick, 1990).
Synthesis and accumulation of JA has been reported in plant breeding
as a crucial process for oral development. Many reports have demon-
strated long male sterility in Arabidopsis plants with mutations for both
perception (coi1) and synthesis of JA (fad378, dad1, aos, opr3 acx1/5)
(Ishiguro et al., 2001; McConn and Browse, 1996; Park et al., 2002a;
Sanders et al., 2000; Stintzi, 2000; Xie et al., 1998). This sterility defect
is expressed in owers during the late stages of development
(Widemann et al., 2016). These genotypes are aected in lament
elongation ability, pollen maturation and anther dehiscence, thereby
preventing pollination and pistil receptivity (Ishiguro et al., 2001;
Nelson et al., 2012; Smyth et al., 1990).
The R2R3-MYB transcription factors MYC2/3/4/5 and MYB21/24
are JA-inducible and guarded by JAZ repressors, which have been
identied as governing proper stamen development in Arabidopsis
(Mandaokar et al., 2006; Song et al., 2011). JAZs interact with MYB21
and MYB24 to attenuate their transcriptional function; upon perception
of the JA signal, COI1 recruits JAZs to the SCFCOI1 complex for
ubiquitination and degradation through the 26S proteasome. MYB21
and MYB24 are then released to activate expression of various genes
essential for JA-regulated anther development and lament elongation
G. Campos-Rivero et al.
Fig. 4. Multiple hormones regulating owering time. ABA promotes owering by
activating FLOWERING LOCUS T (FT) through ABSCISIC ACID-INSENSITIVE MUTANT
5 (ABI5). Jasmonic acid (JA) inhibits owering through the action of CORONATINE
INSENSITIVE 1 (COI1). DELLA inhibits owering, and these proteins can be regulated
positively or negatively by gibberellic acid (GA), indole-3-acetic acid (IAA) and ethylene
(ET). Many chromatin remodeling players are involved in the regulation of FLOWERING
LOCUS C (FLC), FLD and DELLA. DELLA proteins not only interact with PICKLE (PKL) but
also with FLC by recruiting PRC2, which is responsible for increasing H3K27me3 in FLC
by regulating target genes such as FT and SUPPRESSOR OF OVEREXPRESSION OF
CONSTANS 1 (SOC1). FLD mediates the demethylation of H3K4me2, facilitating the
deacetylation of H4 in FLC chromatin. SUMO E3 ligase (SIZ1), which facilitates
sumoylation of FLD, can be inhibited by salicylic acid (SA). The seven hormones
discussed in this review are in blue, while those associated with chromatin remodeling
are in red. The dotted lines indicate interaction between proteins. (For interpretation of
the references to colour in this gure legend, the reader is referred to the web version of
this article.)
(Song et al., 2011). The general requirement of JA signaling in ower
development and fertility was more recently found to be conserved in
other plant species, but striking variations exist. For instance, in rice the
defects along the JA signaling pathway aect not only oret opening
and anther dehiscence but also spikelet development (Cai et al., 2014;
Xiao et al., 2014). In maize, JA biosynthetic mutants show earlier
ower developmental defects including sex determination of male
reproductive organs (Acosta et al., 2009; Yan et al., 2012). On the
other hand, the jai1 mutant in tomato is defective for the homolog of
the F-box protein COI1, which is female sterile (Li et al., 2004). In
Nicotiana attenuate (wild tobacco) mutants such as ir-aoc and ir-coi1 it
was found that JA-Ile coordinates metabolic networks required for
anthesis and oral attractant emission (Stitz et al., 2014). Consistent
with this genetic evidence for important roles in plant reproduction,
many jasmonates, including JA-Ile, have been found to accumulate
abundantly in owers of dierent species such as Petunia hybrida, Pinus
mugo, Vicia faba, Phaseolus vulgaris and others (Wasternack et al., 2013).
Furthermore, investigations in tomato revealed that JA-Ile and JA-Ile-
Me are present in distinct ower organs such as stalks and pistils (Hause
et al., 2000). On the other hand, CYP94C1, one of the three character-
ized cytochrome P450 enzymes, has been reported to be a JA-Ile
oxidation-mediator in ower maturation and ower opening
(Widemann et al., 2016).
The investigation of the epigenetic role in the regulation of JA
during owering has not been as extensive as the investigation of the
genetic role. However, important discoveries have been made. For
instance, HDA6, a HISTONE DEACETYLASE, is required for JA response
and owering in Arabidopsis (Wu et al., 2008). This deacetylase
23
Journal of Plant Physiology 214 (2017) 1627
regulates locus-directed heterochromatin silencing in cooperation with
MET1, possibly recruiting MET1 to specic loci, and thus forms the
foundation of silent chromatin structure for subsequent non-CG methy-
lation (To et al., 2011). Moreover, it was found that HDA6 physically
associates with FLD (Liu et al., 2012; Yu et al., 2011), which
participates in the deacetylation of FLC chromatin and thereby
represses gene expression (He et al., 2003; Wu et al., 2008). This
suggests that HDA6 is involved in JA response and owering in
Arabidopsis.
On the other hand, JA feeding studies and JA measurements
indicate that ARF6 and ARF8 expression in laments stimulates anther
dehiscence and regulates stamen and gynoecium maturation by indu-
cing JA production (Nagpal et al., 2005). The arf6 arf8 double-null
mutant impairs owering by forming infertile closed buds with short
petals, short stamen laments, and undehisced anthers that cannot
release pollen (Nagpal et al., 2005). Both ARFs, ARF6 and ARF8, are
targets of miR167 (Jones-Rhoades and Bartel, 2004), and they display
overlapping expression domains, interacting genetically and regulating
each others expression at both transcriptional and posttranscriptional
levels by modulating miR160 and miR167 availability (Gutierrez et al.,
2009). This complex regulatory network includes an unexpected feed-
back regulation of microRNA homeostasis by direct and indirect target
transcription factors (Gutierrez et al., 2009). Thus, ARF6 and ARF8,
induced by JA and under miR167 and miR160 control, may coordinate
the transition from immature to mature fertile owers.
3. Conclusion
The study of epigenetic mechanisms and their eects on the
regulation of various physiological, metabolic and molecular plant
processes represents a valuable new direction in plant biology, illumi-
nating aspects of plant nature that have long gone unnoticed or
misunderstood. From the biological, ecological and agricultural points
of view, a full understanding of the rules that govern the epigenetic
control of owering, so critical to reproduction and survival, is
necessary.
Here we showed that epigenetic regulate hormone signaling to
inhibit or promote owering. FLC and FLD can be regulated by dierent
epigenetic modications sumoylation, acetylation and methylation
under hormone signaling. For instance, FLC expression is upregulated
by HISTONE DEACETYLASE 6 (HDA6) protein but ET triggers the
expression of HDA6, which can interact with COI1 through JA signal-
ing. On the other hand, FLOWERING LOCUS D (FLD) suppresses FLC by
the demethylation of H3K4me2 and facilitating the deacetylation of H4
in this locus. A very active epigenetic player seems to be PRC2, which
adds H3K27me3 marks into FLD chromatin and recruits PICKLE in
order to interact with DELLA, facilitating the repression of FLC (Fig. 4).
Great progress has been made in understanding the role of
epigenetic regulation during the owering process. However, the vast
majority of research on hormonal regulation in owering has been done
in the model plant A. thaliana. Work on both model and non-model
plants is necessary to our understanding of how plant hormones control
owering through epigenetic gene regulation. As climate change
accelerates, its eects on owering induction will become increasingly
signicant. Now evidence suggests that proper epigenetic regulation of
plant hormone signaling is necessary for the correct transition from the
vegetative to the reproductive stage. Therefore, a better understanding
of global epigenetic regulation processes, including DNA methylation,
histone posttranslational modication and miRNAs, in a broader range
of plant species will guide us in developing plants better adapted to new
environmental challenges.
Conict of interest
The authors declare that they have no conict of interest.
G. Campos-Rivero et al.
Author contribution
C.D. conceived the idea. G.C.R., P.O.M., R.S.B., R.U.C., F.D.A. and
C.D. wrote the manuscript.
Acknowledgments
This study was supported by CONSEJO NACIONAL DE CIENCIA Y
TECNOLOGA (CONACYT) Mxico, scholarships 288867 to GCR,
549842 to POM, 271049 to RSB, 242997 to RUC and 255368 to FDA;
and grant CB2012-178149 to CD.
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