INTRODUCTION
Rice flowering time (heading date), which is affected by both endogenous and exogenous factors, is an important agronomic trait for regional and seasonal adaption. Heading on a proper time is the most critical step for grain production. Precocious flowering reduces the vegetative phase and leads to reduction of biological yield. On the other hand, delayed flowering could cause low seed setting percentage in cold late autumn or delay next planting season, which both results in production loss.
Florigen is produced in the leaf under inductive day length conditions and transported to the shoot apex where it triggers flowering transition (
Cajlachjan, 1937;
Corbesier et al., 2007;
Tamaki et al., 2007). Unlike only one florigen gene
FLOWERING LOCUS T (
FT) in Arabidopsis, rice evolves two florigen genes,
Heading date 3a (
Hd3a) and
RICE FLOWERING LOCUS T 1 (
RFT1), and at least two flowering pathways are developed to control the expression of florigens, the
Heading date 1 (
Hd1) pathway which is conserved between rice and Arabidopsis, and the
Early heading date 1 (
Ehd1) pathway which is unique to rice (
Doi et al., 2004) (Fig. 1). Numerous studies reveal that a large number of rice genes regulate flowering time through the two flowering integrators.
In Arabidopsis, some flowering regulators such as
FLC and
FT are reported to be regulated by various chromatin modifications (
He, 2009;
Liu et al., 2010). However, little is known in rice in this field. Recently, we characterized a major histone methyltransferase (HMTase) gene
SET DOMAIN GENE 724 (
SDG724), which is required for Histone H3 lysine 36 (H3K36) methylation, promotes rice heading, indicating that rice flowering could also be regulated by chromatin modifications (
Sun et al., 2012). In the past two years, more and more molecular genetic studies gave the clues on the chromatin modification mechanism in rice flowering pathways, we summarize here most recent advances towards understanding of genetic networks and epigenetic chromatin modifications in rice flowering time control.
TWO FLORIGEN GENES HD3A AND RFT1 IN RICE
Florigen, which has been hypothesized by many physiological studies, is believed to be produced in leaves by the inductive photoperiod, then moves to the shoot apical meristem (SAM) and triggers flowering transition. But this florigen has been eluded identification since it was first proposed for 70 years (
Cajlachjan, 1937). In 2007, it was firstly revealed that
FT encoded protein in Arabidopsis, is a leaf-derived long-distance signal directed to floral transition (
Corbesier et al., 2007).
In rice, there are 13
FT homologs in the genome (
Chardon and Damerval, 2005),
Hd3a and
RFT1 are two of them which were confirmed to act as florigen genes (
Komiya et al., 2008;
Komiya et al., 2009;
Tamaki et al., 2007). By fusing
Hd3a or
RFT1 with GFP, it was demonstrated that Hd3a or RFT1 protein was expressed in vascular tissue of leaves, and could be moved to SAM where they started flowering induction. As Hd3a-GFP was only detected in the SAM of plants grown under short day conditions (SD), RFT1-GFP was merely detected under long day conditions (LD) (
Komiya et al., 2009;
Tamaki et al., 2007). On the other hand,
Hd3a-RNAi (
RNA interference) plants significantly delayed heading date under SD but not LD,
RFT1-RNAi plants flowering was obviously delayed under LD but not SD oppositely. Furthermore, rice with knockout of both Hd3a and RFT1 caused at least 300 days late flowering under both SD and LD (
Komiya et al., 2009). All these data demonstrated that, unlike Arabidopsis, rice has two florigen genes,
Hd3a and
RFT1,
Hd3a is responsible for flowering under inductive SD, whereas
RFT1 is responsible for flowering transition under non-inductive LD. Although
Hd3a and
RFT1 are located in some chromosome and separated by only 11.5 kb in the genome, the fine-tuning of long day flowering by the H3K36me2/3 level of
RFT1 but not
Hd3a via SDG724, therefore,
RFT1 and
Hd3a which have functionally diverged to control flowering time under LD and SD conditions are partly due to a fine-tuned epigenetic mechanism (
Sun et al., 2012).
FLORIGEN REGULATED NETWORK
How flowering pathways are regulated differs in plants. In Arabidopsis, flowering is controlled by a small number of large-effect genes such as
FLC (
Salome et al., 2011), whereas in maize is controlled by many additive small-effect quantitative trait loci (QTLs) (
Buckler et al., 2009). Interestingly, rice combines both regulatory manners, including a few large-effect factors, such as
Hd1,
Ehd1, and
Grain number,
plant height and heading date 7 (
Ghd7), in addition to some small-effect QTLs and genes (
Ebana et al., 2011;
Tsuji et al., 2013) (Table 1).
So far, quite a number of QTLs controlling rice heading date (Hd) were identified and characterized using different segregating populations derived from crossing a japonica cultivar (
Nipponbare) and an indica cultivar (
Kasalath) (
Lin et al., 1998;
Yano et al., 1997). These QTLs include the major loci controlling photoperiodic flowering responses,
Hd1 (
Yano et al., 1997;
Yano et al., 2000),
Hd2/
Ghd7.1/
OsPRR37 (
Oryza sativa Pseudo-
Response Regulator 37) (
Koo et al., 2013;
Liu et al., 2013;
Shibaya et al., 2011;
Yamamoto et al., 2000;
Yan et al., 2013),
Hd3a (
Kojima et al., 2002),
Hd4/
Ghd7 (
Ghd7 for short) (
Koo et al., 2013;
Xue et al., 2008),
Hd5/
Days to heading 8/
Grain number,
Plant height,
and Heading date 8/
Late Heading Date 1 (
Hd5/
DTH8/
Ghd8/
LHD1) (
Dai et al., 2012;
Fujino et al., 2013;
Yan et al., 2011). Furthermore, backcross progenies derived from the same original cross allowed identification of other QTLs, such as
Hd6/
CK2 (
CASEIN KINASE 2) (
Ogiso et al., 2010;
Takahashi et al., 2001;
Yamamoto et al., 2000),
Hd14/
Ehd1 (
Doi et al., 2004),
Hd16/
EL1 (
Early flowering 1) (
Dai and Xue, 2010;
Hori et al., 2013;
Shibaya et al., 2011),
Hd17/
OsELF3/
EF7/
OsEF3/
Hd3b (
Hd17/
Oryza sativa Early Flowering 3/
Early Flowering 7/
Oryza sativa Early Flowering 3/
Hd3b,
OsELF3 for short) (
Hori et al., 2012;
Matsubara et al., 2012;
Saito et al., 2012;
Yang et al., 2013;
Zhao et al., 2012). Additionally, using rice near isogenic lines and mutants, more genes implicated in controlling flowering time have been identified and positioned into a regulatory network (
Brambilla and Fornara, 2013;
Itoh and Izawa, 2013;
Tsuji et al., 2011,
2013) (Fig. 2).
HD1-DEPENDENT PATHWAY
There is a similar molecular system for florigen control in Arabidopsis and rice (
Izawa, 2007;
Tsuji et al., 2011).
Hd1 and
Hd3a in rice are homologs of
CONSTANS (
CO) and
FT in Arabidopsis, respectively. As in Arabidopsis,
Hd1 acts upstream of
Hd3a (
Kojima et al., 2002;
Yano et al., 2000), and overexpression of a rice ortholog of Arabidopsis
GIGANTEA (
GI) which acts upstream of
CO, namely
OsGI, increased the expression of
Hd1 in the transgenic plants, followed by suppressing
Hd3a expression, resulting in late flowering under both SD and LD (
Hayama et al., 2003). Differently,
CO merely promotes
FT expression,
Hd1 plays a more enigmatic role in rice, which promotes flowering under SD, but represses flowering under LD (
Hayama et al., 2003;
Komiya et al., 2008;
Lin et al., 2000;
Tamaki et al., 2007). These results indicate that the core photoperiodic pathway composed of the three key flowering genes
OsGI/
GI-
Hd1/
CO-
Hd3a/
FT is conserved between rice and Arabidopsis, but its function has diverged during evolution to produce opposite flowering responses. While the photoperiodic pathway in Arabidopsis merely accelerates flowering under LD, in rice, it promotes flowering under SD and represses flowering under LD (
Takahashi and Shimamoto, 2011).
The reversible mechanism that
Hd1 functions as either an activator or suppressor of
Hd3a involves the action of the red-light photoreceptor phytochrome B (phyB), since mutations in
phyB or phytochrome chromophore synthesis, such as
photoperiod sensitivity 5 (
se5), attenuate this conversion and maintain
Hd1 as an activator under any photoperiodic conditions. On the other hand, though
Hd1-overexpressing plants delay flowering, Hd1 protein levels in these plants are not significantly altered (
Andres et al., 2009;
Ishikawa et al., 2011;
Izawa et al., 2002), thus it is speculated that LD light signals may modify the protein of Hd1 or Hd1 complex through phytochrome but not its expression levels, and convert it into a repressor of flowering. Therefore, uncovering of the biochemical function of Hd1 protein and the molecular nature of its dual activity will provide exciting insight into the control of photoperiodic flowering in rice.
Recently, it is deduced that Hd1 protein activity is possible affected by an additional posttranslational regulatory factor,
Hd6, which encodes a CK2 α-subunit (
Ogiso et al., 2010;
Takahashi et al., 2001). The delay flowering effect of Hd6 is observed only when Hd1 is functional, however, Hd1 is not phosphorylated by Hd6
in vitro (
Ogiso et al., 2010), suggesting that Hd6 phosphorylates unknown substrates that cooperate with Hd1 in the LD floral suppression pathway.
EHD1 DEPENDENT PATHWAY
In 2004, a novel regulatory
Ehd1-pathway which is not presented in Arabidopsis, is discovered in rice (
Doi et al., 2004).
Ehd1, encoding a B-type response regulator, is a floral promoter, and rice variety Taichung 65 (T65) without functional
Ehd1 allele delays flowering under both LD and SD (
Doi et al., 2004). As it has been shown that
Ehd1 contributes to flowering time by its expression levels (
Takahashi et al., 2009), thus fine-tuning of
Ehd1 expression is crucial for rice flowering at suitable time, and several flowering regulators have been identified to participate in this regulation.
Ghd7, which is important for increasing rice productivity and adaptability, is a major regulator of
Ehd1 and could delay flowering by repressing
Ehd1 under LD (
Takahashi et al., 2009;
Xue et al., 2008). As
Ghd7 encodes a CCT (CONSTANS, CO-like, and TOC1) domain protein, which shows very low homology to Arabidopsis genome, the
Ghd7-Ehd1 may be a unique pathway in rice (
Koo et al., 2013;
Xue et al., 2008). Further study shows that
Ghd7 and
Ehd1 can respectively set a daylength threshold for Hd3a expression, which is usually observed in SD plants but not in LD plants (
Itoh et al., 2010;
Takimoto and Ikeda, 1961), and this capacity of discernment in critical day length in rice greatly enriches the daylength-dependent regulated mechanism of florigen gene expression.
Until now, at least three genes,
Early heading date 3 (
Ehd3),
ELF3, and
Hd16/
EL1, were identified to control
Ghd7 expression in
Ehd1-pathway.
Ehd3 encodes a plant homeodomain (PHD) finger protein and is identified as one repressor of
Ghd7. Generally,
Ghd7 transcript reaches its highest level after seeding for two weeks, and then the expression is gradually reduced to a basal level, but in
ehd3 mutants,
Ghd7 expression level is always higher and delays heading date for more than one year under LD. Interestingly, under SD,
Ehd3 could promote
Ehd1 expression regardless of
Ghd7, suggesting a perplexed role of
Ehd3 (
Matsubara et al., 2011).
ELF3 in Arabidopsis is responsible for generating circadian rhythm and regulating photoperiodic flowering, consistently, its homolog in rice
OsELF3 is also required to sustain the robust oscillation, and lesions in
OsELF3 delay flowering under both SD and LD (
Saito et al., 2012;
Yang et al., 2013;
Zhao et al., 2012). Under SD,
OsELF3 promotes flowering mainly by repressing
Ghd7, because late flowering of
oself3 mutants can be rescued if
Ghd7 but not
Hd1 is mutated. Under LD,
oself3 mutants increase
OsGI and
Ghd7 expression, thus up-regulate
Hd1 and repress
Ehd1 expression, respectively, indicating that
OsELF3 influences photoperiodic flowering in both
Hd1 and
Ehd1 pathways (
Brambilla and Fornara, 2013;
Saito et al., 2012).
Hd16/
EL1, encoding a casein kinase I protein, is associated with the gibberellin-mediated flowering transition (
Dai and Xue, 2010). Deficient in
Hd16 weakens rice photoperiod sensitivity, but increases
Ehd1,
Hd3a, and
RFT1 expression under LD. Though the expression level of
Ghd7 is not significantly altered in
el1 mutants, the biochemical data indicate that
Hd16 acts as a flowering repressor by phosphorylation of
Ghd7 (
Dai and Xue, 2010;
Kwon et al., 2013).
OsLFL1 (
Oryzasativa LEC2 and FUSCA3 Like 1) encodesa putative B3 transcription factor, knockdown of
OsLFL1 does not affect flowering time, while ectopic overexpression of
OsLFL1 decreases
Ehd1 expression and results in late flowering (
Peng et al. 2007,
2008).
OsLFL1 is controlled by two members of MIKC-type MADS-box family,
OsMADS50 and
OsMADS56. Both
osmads50 mutants and
OsMADS56-overexpressing plants, which produce increased
OsLFL1 expression, showlate flowering phenotype (
Lee et al., 2004;
Ryu et al., 2009). Interestingly, OsMADS56 can interact with OsMADS50
in vitro, suggesting that the two MADS-box members tend to form a heterodimer complex and function antagonistically through
OsLFL1-
Ehd1 pathway under LD (
Ryu et al., 2009).
As mentioned in
Hd1-pathway, phytochrome is probably a primary cause of
Hd1-dependent suppression of rice flowering, but underlying molecular mechanism of phytochrome in
Ehd1-pathway is not well understood. Recent studies showed that
SE5 and
phyB also suppress
Ehd1 expression, and the
phyB-mediated suppression of
Ehd1 is confirmed to be repressed by a CONSTANS-like (COL) gene
OsCOL4 (
Oryza sativa CONSTANS-like 4) (
Andres et al., 2009;
Komiya et al., 2009;
Lee et al., 2010).
OsCOL4 expression is decreased in
osphyB mutants, and
osphyB oscol4 double mutants flower is similar to
osphyB single mutants, indicating that
OsCOL4 functions downstream of
OsphyB (
Lee et al., 2010).
Besides the above regulators,
Ehd1 expression is also modulated by other four flowering factors independently.
Indeterminate 1 (
ID1) is one of them, which expresses in leaf but induces flowering in the shoot meristem.
ID1 has been once thought to be involved in the florigen synthesis in maize (
Colasanti et al., 2006;
Colasanti et al., 1998), and its regulated mechanism has been exhibited in rice. Lesions in rice
RID1 (
Early heading date 2/
OsINDETERMINATE 1/
Rice INDETERMINATE 1,
Ehd2/
OsID1/
RID1, RID1 for short) lead to extremely late flowering phenotype, as well as decreased expression of
Ehd1 and downstream florigen genes under both SD and LD (
Matsubara et al., 2008;
Park et al., 2008;
Wu et al., 2008).
Ehd4 (
Early heading date 4), encoding a CCCH-type zinc finger transcriptional regulator, is expressed mostly in immature leaves and shows a similar diurnal expression pattern of
Ehd1 under both SD and LD.
Ehd4 up-regulates the expression of the florigen genes
Hd3a and
RFT1 through
Ehd1. Strikingly,
Ehd4 is highly conserved in both wild rice and cultivated rice, but homologs cannot be found in other species, suggesting that
Ehd4 is unique flowering regulator in
Oryza genus differed from other grass members during evolution (
Gao et al., 2013).
OsMADS51 is another MADS box gene, other than
Os-MADS50 and
OsMADS56, it acts downstream of
OsGI, transmits a promotion signal from
OsGI to
Ehd1 under SD. Though its null mutants showed late flowering phenotype followed by decreased expression of
Ehd1 and
Hd3a, ectopic expression of
OsMADS51 causes early flowering, accompanying with increased expression
Ehd1 and
Hd3a (
Kim et al., 2007).
Hd5/
DTH8/
Ghd8/
LHD1 encodes a putative HEMEACTI-VATOR PROTEIN 3 (HAP3) subunit of a CCAAT-box binding protein (HAP complex) that binds to CCAAT boxes in yeast and animals. Similar to
Hd1,
Hd5/
DTH8/
Ghd8/
LHD1 delayed flowering in rice under LD and promotes flowering under SD, but by regulating expression of
Ehd1 (
Dai et al., 2012;
Lin et al., 2003;
Wei et al., 2010;
Yan et al., 2011).
Most interestingly,
though
Hd5/
DTH8/
Ghd8/
LHD1 suppresses rice heading though
Ehd1, genetic analysis implies that
Hd5 requires functional
Hd1 to repress flowering under LD (
Nonoue et al., 2008), rising a question what is the relationship between
Hd1 and
Ehd1. Recent findings indicate that transcript level of
Ehd1 is down-regulated in
Hd1-overexpression transgenic lines, suggesting that, to some degree,
Hd1 is an upstream regulator of
Ehd1 expression, but how this crosstalk works is still undefined (
Ishikawa et al., 2011).
FLOWERING REGULATORS INDEPENDENT OF HD1 AND EHD1
Besides
Ehd1, T65 also bears a loss-of-function allele of
Hd1, but it could still flower in time and serves as a commercial rice variety, so there are must some other regulators independent of
Hd1 and
Ehd1 in rice flowering network (
Doi et al., 2004).
OsCO3 and
DTH2 are two of them, and promote flowering by regulating florigen genes. Though both of them are COL genes, they function under different photoperiodic conditions. Expressions of
Hd3a and
FT-like genes are decreased in the
OsCO3-overexpressing plants under SD without altered expression of other florigen upstream regulators, suggesting that
OsCO3 primarily controls flowering time under SD by negatively regulating the expression of florigen genes, independent of other known SD-promotion pathways (
Kim et al., 2008). For
DTH2, both association analysis and transgenic experiments indicate that two functional nucleotide polymorphisms that correlated with early heading and increased reproductive fitness under natural LD in northern Asia. Further combined population genetics and network analyses suggest that
DTH2 probably represents a target of artificial selection for adaptation to LD during rice domestication and improvement, demonstrating an important role of minor effect quantitative trait loci in crop adaptation and breeding (
Wu et al., 2013).
Although some
PRR genes are major components of the circadian oscillator, a rice
PRR gene
Hd2/
Ghd7.1/
OsPRR37 may down-regulate
Hd3a expression independent of any known pathways to suppress flowering under LD. As lesions in
Hd2/
Ghd7.1/
OsPRR37 cause early flowering phenotype, the japonica varieties harboring nonfunctional alleles of both
Ghd7 and
Hd2/
Ghd7.1/
OsPRR37 flower extremely early under natural LD, and make these varieties adapt to the northernmost rice cultivation regions. Further study implied that natural variations in
Hd2/
Ghd7.1/
OsPRR37 have contributed to the expansion of rice cultivation to temperate and cooler regions (
Koo et al., 2013;
Liu et al., 2013;
Yan et al., 2013).
Different from
Hd2/
Ghd7.1/
OsPRR37,
OsDof12 is LD-specific flowering repressor and encodes a DNA-binding with one finger (Dof) transcription factor which is involved in a variety of biological processes of plants. The transcriptions of
OsDof12 can express at different development stages, but strongly inhibited by dark treatment.
OsDof12-overexpressing plants flower earlier in consistent with the up-regulation of
Hd3a independent of other flowering genes under LD but not SD (
Li et al., 2009).
CHROMATIN MODIFICATIONS REGULATE FLOWERING IN RICE
Chromatin, which is composed by complexing DNA with histone, carries not only genetic, but also epigenetic information. In Arabidopsis, the expression of a major flowering repressor
FLC is regulated by a number of active and repressive chromatin modifications, such as histone tails methylation, acetylation, ubiquitination etc. In addition, histone modifications can also directly regulate the expression of florigen gene
FT, and the regulation manner of
FLC and
FT provides a paradigm for control of developmental regulators through chromatin modifications (
He, 2009). Currently, not so many data are available about that in rice, but molecular genetic studies indicated that rice flowering control also undergoes the complex chromatin modifications (Table 2).
ACTIVE CHROMATIN MODIFICATIONS AND RICE FLOWERING
S-Adenosyl-l-methionine is a universal methyl group donor involved in numerous transmethylation reactions, including histone methylation. Knockdown of rice
S-Adenosyl-l-methionine synthetase (
SAMS)
1,
2, and
3 greatly reduced the expression of
Ehd1,
Hd3a,
RFT1 and led to a late flowering phenotype. Moreover, the histone H3K4me3 and symmetric DNA methylation at these genes was significantly reduced, suggesting an association between epigenetic modification and flowering in rice, but more research are required on this relationship (
Li et al., 2011).
We have demonstrated that
SDG724, a histone methyltransferase gene which belongs to SET domain family Class II (
Ng et al., 2007), affected flowering time by mediating H3K36 methylation in rice.
SDG724 loss-of-function mutant
lvp1 showed a late flowering phenotype under both LD and SD, which was associated with the suppressed expression of
RFT1 and
Hd3a. Interestingly, only the chromosomal region of
RFT1, but not
Hd3a, reduced the level of H3K36me2/3 modifications which associated with the transcriptionally active chromatin state, although the two florigenic genes are closely linked in the genome and separated by only 11.5 kb (
Sun et al., 2012). This similar regulated way in
RFT1 is also found in a previous report that
RFT1 expression can be promoted through another active histone modification H3K9 acetylation around the transcriptional start site of its chromatin in
Hd3a-RNAi transgenic plants (
Komiya et al., 2008). In conclusion, both of the two findings suggest an epigenetic regulation mechanism through
RFT1. In addition,
SDG724 also affects the histone modification state at
OsMADS50 chromosomal region, thus all the results suggest a LD floral promotion pathway mediated by H3K36me2/3 deposition through
OsMADS50-
Ehd1-
RFT1 pathways in rice (
Sun et al., 2012).
Coincidentally, another member of Class II in SET domain family (
Ng et al., 2007),
SDG725, is also involved in promoting rice flowering through H3K36me2/3. In
SDG725 knockdown plants, the expression levels of
Ehd3,
RID1,
OsMADS50,
OsMADS51,
Ehd1,
Hd3a, and
RFT1 were all drastically reduced, but the
Ghd7 expression was increased, under either SD or LD. Different from
SDG724,
SDG725 is required for deposition of H3K36me2/3 at more flowering gene loci, such as
Ehd3,
RID1,
OsMADS50,
Hd3a, and
RFT1. Thus,
SDG724 and
SDG725 regulate both overlapped and specific flowering genes by mediating H3K36me2/3 deposition and promote rice flowering, which are different to the previously known function of these epigenetic marks in Arabidopsis flowering (
Sui et al., 2012;
Xu et al., 2008;
Zhao et al., 2005).
Very recently, another homolog of
SDG724,
OsTrx1, which belongs to SET domain family Class III (
Ng et al., 2007), might activate or maintain the active transcribed states of target genes, and was reported to delay flowering time under LD through
Ghd7 pathway but not
OsMADS50 and
Hd1 pathways (
Choi et al., 2014). Though expression of
Ehd3 that functions upstream of
Ghd7 is unchanged in
ostrx1 mutants, it was proved that OsTrx1 could bind to Ehd3
in vitro. Further study showed that PHD motif of OsTrx1 could bind to native histone H3 and the C-terminal end of SET domain of OsTrx1 has histone H3 methyltransferase activity, thus OsTrx1 and Ehd3 tend to form a complex to methylate downstream genes, but further studies are needed to illuminate its function in detail (
Choi et al., 2014).
REPRESSIVE CHROMATIN MODIFICATIONS AND RICE FLOWERING
Arabidopsis
VILs (
VIL,
VERNALIZATION INSENSITIVE),
VIN3, and
VRN5 are components of PRC2 (Polycomb Repressive Complex 2), mediating the H3K27 trimethylation at the
FLC locus to repress its expression and hence to induce flowering. In rice, a
VIL homolog gene
LC2/
OsVIL3 is considered as a possible component of PRC2 complex, and
lc2 mutants display late flowering along with the reduced expression of
Hd1 and
Hd3a under SD. Furthermore, consistent with the result that
OsLF (
Oryza sativa Late Flowering) directly repressed
Hd1 expression (
Zhao et al., 2011),
LC2/
OsVIL3 binds to the promoter region of
OsLF and represses the
OsLF expression via H3K27me3 methylation, thus eventually promotes flowering (
Wang et al., 2012).
OsVIL2 may be another
VILs member in rice PRC2 complex, and mutations in
OsVIL2 cause late flowering under both SD and LD. Different from
LC2/
OsVIL3, the late flowering phenotype is associated with increased
OsLFL1 and reduced
Ehd1,
Hd3a,
RFT1 expression. Furthermore, OsVIL2 can bind to native histone H3
in vitro and is directly associated with
OsLFL1 chromatin
in vivo, and H3K27me3 is significantly reduced on
OsLFL1 chromatin in
osvil2 mutants compared to the wild type, indicating that
OsVIL2 epigenetically represses
OsLFL1 expression to promote flowering in rice. Besides, OsVIL2 can physically interact with OsEMF2b, which may be also a member of PRC2. Similar to
osvil2, a null mutation of
OsEMF2b caused late flowering by increasing
OsLFL1 and decreasing
Ehd1 expression (
Wang et al., 2012;
Yang et al., 2012).
In short, similar to Arabidopsis, LC2/OsVIL3, OsVIL2, and OsEMF2b may function together with PRC2 to induce flowering by affecting histone modification H3K27me3, but their target flowering genes are different, indicating that a diverse flowering pathway regulated by PRC2 in rice flowering.
CONCLUSION AND PERSPECTIVES
Heading date is an important agronomic trait that determining rice to grow in different regions and seasons. In last two decades, tremendous progress has been made by the study of QTLs and genes controlling rice flowering, which not only identified the nature of the mobile signal florigen, but also unveiled a complex genetic network that controls florigen in rice. Hd3a and RFT1, two florigens regulated respectively rice flowering under SD and LD, are mainly controlled through Hd1 and Ehd1 pathways. However, as mentioned in various T65 with lack of both, rice also develops some additional pathways that could induce rice flowering.
Histone modification is very important for defining transcriptional regulation expression, thus plays a fundamental role in plant growth and development, as well as responding to various environmental conditions. These modification marks are dynamically “written” and “erased”, and then specifically recognized by the “readers” and instruct specific biological process, such as flowering. Very recently, a large number of studies have revealed that various ‘active’ histone modifications, H3K4 methylation, H2B monoubiquitination, H3K36me2/me3, histone deacetylation, and ‘repressive’ chromatin modifications, H3K4 demethylation, H3K9 methylation, H3K27 methylation, histone arginine methylation, are involved in modulating FLC expression in Arabidopsis. Though the regulation of FLC expression via chromatin modification provides a paradigm in flowering gene expression, whether there exists a major flowering regulator such as FLC in rice is still unknown (Fig. 1). Rice possibly has some new routes in its flowering control. In rice, a number of studies revealed the difference in chromatin modification mechanism in the past two years, ‘active’ H3K36me2/3, H3K4me3, H3K9 acetylation and ‘repressive’ H3K27me3 modifications mediate flowering time through Hd1 and Ehd1 dependent pathways, and our finding about SDG724 also suggests a LD floral promotion pathway that could be mediated via an epigenetic regulation of florigen RFT1 itself. All these data suggest that the target flowering genes of chromatin modifications are dispersed in both conserved and unique flowering pathways in rice. Taken together, all the progress in rice, along with Arabidopsis, provides a complete evolutionarily comparative view of genetic and epigenetic flowering mechanisms in plants until now.
Furthermore, in rice, some histone modification participators tend to function under SD and LD, but others like to function mainly under SD or LD, thus unveiling of histone modification mechanism in rice flowering might set a solution to verify the relationships between particular histone modifications and photoperiod environments. On the other hand, as a LD plant, Arabidopsis flowering is accelerated by LD, but SD plant rice flowers earlier under SD than under LD, further study will be helpful to distinguish the function and evolutionary process of histone modification in various photoperiodic plants. Thus, it would be of great interest to identify more chromatin modification regulators and their target genes in rice flowering in future.
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