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Logo of annbotAboutAuthor GuidelinesEditorial BoardAnnals of Botany
Ann Bot. Jun 2009; 103(8): 1165–1172.
Published online Mar 21, 2009. doi:  10.1093/aob/mcp063
PMCID: PMC2685306

The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals

Abstract

Background

In arabidopsis (Arabidopsis thaliana), FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC) play key roles in regulating seasonal flowering-responses to synchronize flowering with optimal conditions. FT is a promoter of flowering activated by long days and by warm conditions. FLC represses FT to delay flowering until plants experience winter.

Scope

The identification of genes controlling flowering in cereals allows comparison of the molecular pathways controlling seasonal flowering-responses in cereals with those of arabidopsis. The role of FT has been conserved between arabidopsis and cereals; FT-like genes trigger flowering in response to short days in rice or long days in temperate cereals, such as wheat (Triticum aestivum) and barley (Hordeum vulgare). Many varieties of wheat and barley require vernalization to flower but FLC-like genes have not been identified in cereals. Instead, VERNALIZATION2 (VRN2) inhibits long-day induction of FT-like1 (FT1) prior to winter. VERNALIZATION1 (VRN1) is activated by low-temperatures during winter to repress VRN2 and to allow the long-day response to occur in spring. In rice (Oryza sativa) a VRN2-like gene Ghd7, which influences grain number, plant height and heading date, represses the FT-like gene Heading date 3a (Hd3a) in long days, suggesting a broader role for VRN2-like genes in regulating day-length responses in cereals. Other genes, including Early heading date (Ehd1), Oryza sativa MADS51 (OsMADS51) and INDETERMINATE1 (OsID1) up-regulate Hd3a in short days. These genes might account for the different day-length response of rice compared with the temperate cereals. No genes homologous to VRN2, Ehd1, Ehd2 or OsMADS51 occur in arabidopsis.

Conclusions

It seems that different genes regulate FT orthologues to elicit seasonal flowering-responses in arabidopsis and the cereals. This highlights the need for more detailed study into the molecular basis of seasonal flowering-responses in cereal crops or in closely related model plants such as Brachypodium distachyon.

Key words: Flowering, vernalization, photoperiod, day length, VRN1, VRN2, FLC, FT, cereals, arabidopsis, MADS

SEASONAL FLOWERING-RESPONSES

Plants co-ordinate flowering with optimal seasonal conditions to maximize reproductive success. In tropical regions many plants flower during the cooler seasons of the year to avoid the extreme heat of summer. Conversely, in temperate regions many plants flower during spring to avoid damage to floral organs by freezing winter temperatures. One mechanism by which plants synchronize flowering with optimal seasonal conditions is by sensing changes in day length, or photoperiod. Many plants growing in the tropics flower as day length decreases, whereas many plants from temperate regions flower in response to increasing day length. Another important seasonal cue that regulates flowering time is temperature. In temperate regions warmer conditions can accelerate flowering in spring. Furthermore, many plants from temperate regions flower only after they experience an extended period of cold, or vernalization. This minimizes the risk of frost damage to cold-sensitive reproductive organs. Often plants respond to a combination of day length, vernalization and temperature to ensure optimal timing of flowering.

Studies of the model plant arabidopsis (Arabidopsis thaliana) have provided insights into the molecular pathways controlling these seasonal flowering-responses. Efforts are now being made to extend this understanding to other plants, including cereal crop species such as rice (Oryza sativa), wheat (Triticum aestivum) and barley (Hordeum vulgare). In this review, the molecular pathways controlling seasonal flowering-responses in arabidopsis will be compared and contrasted with those of cereals and related grasses.

SEASONAL CONTROL OF FLOWERING IN ARABIDOPSIS

In arabidopsis three main seasonal flowering-responses have been studied; the day-length response, the vernalization response and the thermo-sensitive flowering response.

The day-length flowering-response pathway of arabidopsis

Flowering of arabidopsis is accelerated by long days. The key to the long-day flowering response is the activation of FLOWERING LOCUS T (FT) (Fig. 1A; reviewed in Imaizumi and Kay, 2006; Jaeger et al., 2006; Zeevaart, 2006; Turck et al., 2008). FT encodes a ‘mobile florigen’ (Kardailsky et al., 1999; Kobayashi et al., 1999; Corbesier et al., 2007). The FT gene is expressed in the leaves in long days and the FT protein travels to the apex, where it interacts with another protein FD to activate the expression of genes that promote floral development, such as the MADS box gene APETALLA1 (AP1) (Abe et al., 2005; Wigge et al., 2005; Corbesier et al., 2007). This accelerates the transition towards reproductive development.

Fig. 1.
A comparison of the molecular pathways regulating flowering time in (A) arabidopsis, (B) rice and (C) temperate cereals. Vernalization and long days promote flowering in arabidopsis and temperate cereals wheat and barley (A, C), whereas short days promote ...

Expression of FT is activated by CONSTANS (CO) (Fig. 1A; Koornneef et al., 1991; Onouchi et al., 2000; An et al., 2004). CO mRNA is expressed with a diurnal rhythm, peaking in the late afternoon, and the CO protein is stabilized by light (Suarez-Lopez et al., 2001; Valverde et al., 2004). In long days the peak of CO mRNA level occurs during daylight, where the CO protein is stabile, enabling CO to induce FT expression (Valverde et al., 2004). This does not happen when days are short, where the peak in CO mRNA expression occurs in darkness, resulting in low CO stability (Valverde et al., 2004; Jang et al., 2008).

The CO protein consists of a zinc finger domain and a CCT domain [CO, CO-like and TIMING OF CAB1 EXPRESSION 1 (TOC1)] (Putterill et al., 1995; Robson et al., 2001). CCT domains are predicted to form a structure similar to the HEME ACTIVATING PROTEIN2 protein (HAP2) of yeast (McNabb et al., 1995; Wenkel et al., 2006), which forms a complex with HAP3 and HAP5 to bind to the CCAAT box; a promoter motif required for up-regulation of many eukaryotic genes (McNabb et al., 1995). In arabidopsis, CO interacts with AtHAP3 and AtHAP5, through the CCT domain, and together these proteins might form a complex to regulate expression of FT (Wenkel et al., 2006).

Genes encoding factors involved in the perception of daylight, or the control of the circadian clock, contribute to the proper regulation of the day-length response in arabidopsis by controlling the activity of CO (Suarez-Lopez et al., 2001; Yanovsky and Kay, 2002; Valverde et al., 2004; Imaizumi et al., 2005). GIGANTEA (GI) is regulated by the circadian clock, and binds to the promoter of the CO gene as part of a larger protein complex to promote expression of CO in the late afternoon (Sawa et al., 2007). Phytochromes and cryptochromes interact to control the stability of CO protein and to maximize the activity of the CO protein when high mRNA levels coincide with daylight (Valverde et al., 2004).

The vernalization flowering-response pathway of arabidopsis

Certain ecotypes of arabidopsis require prolonged cold, or vernalization, to promote rapid flowering. In these ecotypes, flowering is delayed by the floral repressor FLOWERING LOCUS C (FLC) until plants are vernalized (Fig. 1A; Michaels and Amasino, 1999; Sheldon et al., 1999). FLC encodes a MADS box transcription factor that binds to sites within the FT gene to repress transcription and suppress the long-day flowering response (Michaels and Amasino, 1999; Sheldon et al., 1999; Michaels et al., 2005; Helliwell et al., 2006). FLC also represses a second floral promoter, SUPPRESSOR OF OVER EXPRESSION OF CONSTANS 1 (SOC1), another MADS box transcription factor that acts downstream of CO (Hepworth et al., 2002; Michaels et al., 2005; Helliwell et al., 2006).

When plants are vernalized, expression of FLC decreases (Michaels and Amasino, 1999; Sheldon et al., 1999). This allows long-day induction of FT and SOC1, and thus the long-day flowering response (Fig. 1A; Hepworth et al., 2002; Michaels et al., 2005). Vernalization-induced repression of FLC involves the Polycomb Repression Complex 2 (PRC2; Schubert et al., 2006; Wood et al., 2006; De Lucia et al., 2008). This complex modifies histones in the chromatin at the FLC locus, and causes an increase in the level of tri-methylation at the lysine 27 residue of the histone 3 tail (H3K27me3; Schubert et al., 2006; Sung et al., 2006; Greb et al., 2007; Finnegan and Dennis, 2007; De Lucia et al., 2008). H3K27me3 is a chromatin modification that in other organisms, such as in Drosophila melongaster and in mammals, is associated with long-term inactivation of gene expression (Cao and Zhang, 2004). A gene that is required for the PRC2-targeted repression of FLC is VERNALIZATION INSENSITIVE3 (VIN3), which encodes a cold-induced Plant Homeodomain (PHD) protein that interacts with members of the PRC2 complex (Sung and Amasino, 2004; Wood et al., 2006; De Lucia et al., 2008). Long-term repression of FLC provides a memory of cold and allows plants to retain the ability to respond to long days after winter until days lengthen during spring (Sheldon et al., 2000).

FRIGIDA (FRI) is required to maintain high levels of FLC expression, and to maintain the vernalization requirement (Koornneef et al., 1994; Lee et al., 1994; Johanson et al., 2000). Natural variation in FRI function is an important determinant of vernalization requirement in different ecotypes of arabidopsis (Johanson et al., 2000). Other regulators of FLC include the so called autonomous pathway genes, which were originally defined by mutations that delay flowering irrespective of day length (for reviews, see Simpson, 2004; Marquardt et al., 2006). These include LUMINIDEPENDENS (LD), FCA, FY, FPA, FVE, FLOWERING LOCUS D (FLD) and FLK. FLD, for example is a histone deacetylase that normally reduces FLC expression levels (Sanda and Amasino, 1996; He et al., 2003). FLD mutants cause elevated FLC activity and delay flowering regardless of day length (Sanda and Amasino, 1996).

The thermo-sensitive flowering response pathway

Flowering of arabidopsis is delayed at cooler temperatures (16 °C compared with 23 °C; Blazquez et al., 2003). This flowering response might be important to delay flowering during early spring if temperatures are too low for optimal reproductive growth. FT expression is elevated at high growth temperatures (Blazquez et al., 2003) and plants that lack FT (ft mutants) show little acceleration of flowering at elevated growth temperature, so acceleration of flowering by higher growth temperatures is likely to act through FT (Balasubramanian et al., 2006). This does not require CO, so another mechanism must induce FT in response to high temperatures (Balasubramanian et al., 2006). Consistent with this hypothesis warmer growth conditions (27 °C compared with 23 °C) accelerate flowering in short days where CO is less active (Balasubramanian et al., 2006).

The SHORT VEGETATIVE PHASE (SVP) gene is required for delayed flowering in cool conditions (Lee et al., 2007). Expression of FT and SOC1 is elevated in svp mutants, particularly at 16 °C, and both genes are required for the early flowering phenotype of svp mutants (Lee et al., 2007). Thus, SVP normally delays flowering at sub-optimal temperatures by repressing FT and SOC1 (Fig. 1A). Recently it has been shown that SVP interacts with FLC, and is required for FLC to bind and repress both FT and SOC1 (Li et al., 2008). Conversely, FLC is also required for the action of SVP (Li et al., 2008). It seems that both these MADS box transcription factors are members of a protein complex that represses FT and SOC1 to regulate multiple seasonal flowering-responses in arabidopsis. In addition to affecting the thermo-sensitive flowering response, svp mutations dramatically reduce the vernalization requirement in arabidopsis (Li et al., 2008).

The autonomous pathway genes FCA and FVE also influence the effects of growth temperature on flowering time, and fca or fve mutants are late flowering at high growth temperatures (Blazquez et al., 2003; Balasubramanian et al., 2006). This might be caused by elevated SVP expression levels, as svp mutants suppress the delay of flowering at high temperatures in fca and fve mutants (Lee et al., 2007). Other pathways that control FT activity can influence the effect of growth temperature on flowering time. For example, the activities of light receptors, which influence entrainment of the clock or the activity of CO (and therefore FT expression levels) can also influence the thermo-sensitive flowering response (Guo et al., 1998; Blazquez et al., 2003). Similarly, two PSEUDO RESPONSE REGULATOR (PRR) genes, PRR7 and PRR9, required to entrain the circadian clock to both light and temperature are likely to affect both day-length and temperature regulation of flowering time (Salome and McClung, 2005).

ARE THE ROLES OF ARABIDOPSIS FLOWERING TIME GENES CONSERVED IN CEREALS?

Genes homologous to those that control seasonal flowering-responses in arabidopsis have been identified in cereal crop plants and related forage grasses. FT-like genes have been identified in wheat, barley, rice, maize (Zea mays) and Lolium (Lolium perenne or L. temulentum) (Kojima et al., 2002; King et al., 2006; Yan et al., 2006; Faure et al., 2007; Danilevskaya et al., 2008). CO-like genes have also been identified in these plants (Yano et al., 2000; Griffiths et al., 2003; Martin et al., 2004; Miller et al., 2008). Cereal homologues of arabidopsis genes involved in the diurnal regulation of CO activity (GI, TOC, genes encoding phytochromes or cryptochrome; Childs et al., 1997; Izawa et al., 2000; Hayama et al., 2002; Dunford et al., 2005), the photoperiod response (SOC1 and FD; Lee et al., 2004; Li and Dubcovsky, 2008), the vernalization or autonomous pathways (VIN3, FCA, FY; Lee et al., 2005; Lu et al., 2006; Fu et al., 2007) and the thermo-sensitive flowering response (SVP; Schmitz et al., 2000; Kane et al., 2005; Sentoku et al., 2005; Trevaskis et al., 2007; Fornara et al., 2008; Lee et al., 2008) have also been identified. As outlined below, there are differences in the way many of these genes function in monocot plants compared with arabidopsis.

The day-length response of rice, a short-day grass

Rice, one of the world's most important cereal crops, is generally grown in warmer climates. Unlike arabidopsis, rice flowers preferentially under short days and does not require vernalization to flower, which implies key differences in the molecular mechanisms controlling the timing of flowering in rice versus arabidopsis.

Genes corresponding to a number of flowering time QTLs have been identified in rice. These include Heading date 3a (Hd3a), which has been identified as an orthologue of the arabidopsis FT gene (Fig. 1B; Kojima et al., 2002). Hd3a is expressed in leaves and the Hd3a protein is transported to the shoot apex where it accelerates floral development (Tamaki et al., 2007). Thus, Hd3a mediates the main output of the day-length pathway in rice and fulfils a role similar to FT in arabidopsis (Fig. 1B; Kojima et al., 2002, 2008). Unlike FT, which is expressed in long days, Hd3a is expressed in short days (Kojima et al., 2002; Tamaki et al., 2007). This is a critical difference between the seasonal flowering-responses of arabidopsis and rice (Fig. 1B).

A second flowering time QTL, Heading date 1 (Hd1; also known as SE1) has been identified as a CO homologue (Yokoo et al., 1980; Yano et al., 2000). Hd1 is expressed with a diurnal rhythm which, like CO in arabidopsis, peaks in the afternoon and presumably results in high Hd1 activity late in the afternoon in long days (Fig. 1B). The rice orthologue of GI (OsGI) has a diurnal rhythm of gene expression, and over-expression of OsGI is associated with higher expression of Hd1 (Hayama et al., 2002, 2003). Thus, OsGI might regulate diurnal expression of Hd1, similar to the regulation of CO by GI in arabidopsis. Unlike CO, which activates FT, high Hd1 expression in long days is not associated with increased expression of Hd3a (Fig. 1B; Hayama et al., 2003).

Why high Hd1 expression is associated with low expression of Hd3a in long days is unclear. One possibility is that Hd1 has an identical function to CO, but other factors modify the activity of the day-length flowering-response pathway in rice. Such a factor might have been mapped to the Ghd7 locus (Fig. 1B; Xue et al., 2008). Ghd7 is predicted to encode a protein with a zinc finger and a CCT domain, which is expressed predominantly during the light period in long days (Fig. 1B). GHD7 represses Hd3a, and delays flowering in long days (Xue et al., 2008). If Ghd7 is deleted, expression of Hd3a is activated in long days (Xue et al., 2008). This suggests that the day-length response pathway of rice retains the capacity to activate expression of Hd3a in long days but this is normally suppressed by GHD7 (Fig. 1B). A critical experiment will be to determine if this occurs through Hd1 (i.e. does a null hd1 suppress early flowering of a line that lacks Ghd7 in long days?).

Lines that lack a functional Hd1 gene flower later in short days compared with wild-type plants. This shows that Hd1 does play a role in promoting flowering in short days (Yano et al., 2000; Kojima et al., 2002), but Hd1 explains only a small proportion of the total acceleration of flowering in short days, suggesting that other factors are more important for the short-day flowering response. Another QTL in rice has been localized to the Early heading date 1 (Ehd1) gene, which encodes a B-type response regulator, a type of protein involved in signal transduction in plants and other organisms (Hwang et al., 2002; Doi et al., 2004). Ehd1 is expressed with diurnal rhythm in short days, but is expressed at low levels in long days (Fig. 1B; Doi et al., 2004). In short days Ehd1 promotes expression of Hd3a and a related FT-like gene Rice FT1 (RFT1; Doi et al., 2004). Ehd1 is thought to act independently of Hd1 (Doi et al., 2004).

Expression of Ehd1 is up-regulated by the MADS box gene OsMADS51 (Kim et al., 2007); over-expression of OsMADS51 is associated with increased expression of Ehd1 and the opposite is observed when OsMADS51 expression is reduced (Fig. 1B; Kim et al., 2007). OsMADS51 also promotes expression of Hd3a, possibly through Ehd1 (Fig. 1B). OsMADS51 is itself regulated by OsGI, and reduced expression of OsGI is associated with lower expression of OsMADS51 (Kim et al., 2007). So OsMADS51 might act as an intermediate between OsG1 and Ehd1, to promote expression of Ehd1 with a diurnal rhythm in short days (Fig. 1B). The Oryza sativa INDETERMINATE1 gene (OsId1, RId1 or Early heading date 2) is also required for expression of Ehd1 and Hd3a and for the promotion of flowering by short days (Matsubara et al., 2008; Park et al., 2008; Wu et al., 2008).

There are no homologues of Ghd7, OsID1, Ehd1 or OsMADS51 in arabidopsis. It seems that the different seasonal flowering responses of rice compared with arabidopsis might result from the activity of genes not found in arabidopsis.

The day-length response in temperate cereals, long-day grasses

Generally temperate cereals, such as wheat and barley, flower more rapidly in long days due to acceleration of the transition to reproductive growth and more rapid inflorescence development after this transition. As in rice and arabidopsis, this day-length flowering response appears to involve the activation of an FT-like gene, FT-like 1 (FT1), which is induced in the leaves in long days (Turner et al., 2005; Fig. 1C). CO-like genes have also been identified in barley (HvCO1 and HvCO2), wheat (TaHD1 and TaHD2), maize (conz1) and Lolium (LpCO3) (Griffiths et al., 2003; Nemoto et al., 2003; Martin et al., 2004; Miller et al., 2008). TaHd1 complements the rice Hd1 mutant, and LpCO3 complements the co mutation (Martin et al., 2004), suggesting that the function of CO is conserved between the grasses and arabidopsis. Similarly, the roles of GI-like genes are probably conserved between wheat, barley, rice and arabidopsis (Hayama et al., 2002, 2003; Dunford et al., 2005; Zhao et al., 2005).

In temperate cereals natural variation in day-length sensitivity is controlled primarily by PHOTOPERIOD1 (PPD1). PPD1 encodes a protein with a CCT domain which belongs to the pseudo-response regulator (PRR) family. PPD1 shows a diurnal rhythm of gene expression (Fig. 1C; Turner et al., 2005). Some varieties of barley carry a non-functional version of PPD1 (ppd-h1). These show reduced expression of FT1 (HvFT1) and a weak acceleration of flowering in long days (Turner et al., 2005). Conversely, some varieties of wheat carry versions of PPD1 that have altered diurnal rhythm (Beales et al., 2007). These have increased expression of FT1 and flower rapidly in short days, reducing the apparent impact of long days on flowering time (Beales et al., 2007). Altered PPD1 activity might influence day-length sensitivity by altering expression of CO-like genes (Turner et al., 2005). PPD1 is related to the PRR7 gene of arabidopsis, which has a role in both light and temperature entrainment of the circadian clock, so PPD1 might also influence thermo-sensitive flowering responses in cereals, in addition to regulating day-length response.

Whereas in rice Ehd1 promotes expression of Hd3a in short days no Ehd1 orthologues have been identified in temperate cereals. This might be one reason that FT1 is not expressed in short days in wheat and barley. Another key difference between rice and the temperate cereals is the vernalization-response pathway which, as discussed below, down-regulates a Ghd7-like gene to promote expression of FT1 in long days.

The vernalization response of temperate cereals

Many varieties of wheat, barley, oats (Avena sativa) and rye (Secale cereale) require vernalization to flower. The vernalization response in these cereals appears to have evolved independently to the vernalization response of arabidopsis. No FLC-like MADS box genes have been identified in temperate cereals. Instead, the delay of flowering prior to winter in vernalization-responsive wheat and barley varieties is mediated by the VERNALIZATION2 (VRN2) gene (Takahashi and Yasada, 1971). VRN2 encodes a protein with a zinc finger and a CCT domain, related to Ghd7, which is expressed in long days with a diurnal pattern (Yan et al., 2004; Dubcovsky et al., 2006; Trevaskis et al., 2006). VRN2 delays flowering by inhibiting expression of FT1 (Fig. 1C; Hemming et al., 2008). Once plants have been vernalized, expression of VRN2 decreases and plants are able to respond to long days (Yan et al., 2004; Karsai et al., 2005; Dubcovsky et al., 2006; Trevaskis et al., 2006; Hemming et al., 2008).

Down-regulation of VRN2 in vernalized plants is likely to be mediated by VERNALIZATION1 (VRN1) (Fig. 1C; Trevaskis et al., 2006; Hemming et al., 2008). VRN1 is a FRUITFULL-like MADS box gene that is essential for flowering in temperate cereals (Danyluk et al., 2003; Trevaskis et al., 2003; Yan et al., 2003; Preston and Kellogg, 2008; Shitsukawa et al., 2007). VRN1 is initially expressed at low levels but is induced by vernalization (Fig. 1C; Danyluk et al., 2003; Trevaskis et al., 2003; Yan et al., 2003; von Zitzewitz et al., 2005). After vernalization, increased VRN1 activity is associated with rapid inflorescence initiation (Hemming et al., 2008). Expression of VRN1 is associated with down-regulation of VRN2 and up-regulation of FT1 in long days (Fig. 1C; Hemming et al., 2008). Thus, VRN1 appears to act through two mechanisms to trigger flowering in vernalized plants: (1) acceleration of the transition to reproductive growth at the shoot apex; (2) activation of the long-day response in leaves.

In some varieties of wheat and barley, VRN1 is active without vernalization, so plants do not need to over-winter to flower (Danyluk et al., 2003; Trevaskis et al., 2003; Yan et al., 2003). This can be caused by mutations in the promoter of the VRN1 gene, or by deletions and insertions within the first intron (Yan et al., 2003; Fu et al., 2005; von Zitzewitz et al., 2005; Cockram et al., 2007; Szucs et al., 2007). Presumably these regions contain sequences required to maintain low-levels of VRN1 activity prior to winter, although how this occurs is unclear. The full-length first intron of VRN1 is not required for low-temperature induction of this gene (Trevaskis et al., 2007), suggesting that, although the first intron is required for repression of VRN1, the low-temperature response is controlled by other regions of the gene.

Increased activity of FT1 can also bypass the requirement for vernalization in cereals. This can occur through two mechanisms. In varieties where VRN2 is deleted, long days induce FT1 and trigger flowering without vernalization (Yan et al., 2006; Hemming et al., 2008). Alternatively, mutations in the FT1 gene itself can cause elevated expression of this gene (Yan et al., 2006). In wheat, an insertion in the promoter of the FT1 gene causes increased FT1 expression (identified genetically as dominant alleles of the VRN3 locus; Yan et al., 2006). This bypasses the delay of flowering by VRN2 and allows plants to flower rapidly without vernalization. A similar association between dominant alleles of VRN3 and elevated FT1 expression occurs in barley (Yan et al., 2006), although the molecular basis for this increased expression of FT1 is unclear (Hemming et al., 2008).

Genetic variation in VRN1, VRN2 and FT1 (VRN3) has been used to breed temperate cereals suitable for different climates. For example, varieties that do not require vernalization can be sown in warm climates where vernalization is unlikely to occur, and can also be sown in spring and will flower without over-wintering.

The thermo-sensitive flowering response of temperate cereals

Flowering time is regulated by ambient temperatures in temperate cereals. For example, einkorn wheat (Triticum monococcum) flowers more rapidly at 23 °C than at 16 °C, a similar temperature-sensitive flowering response to that of arabidopsis. It is not clear whether SVP-like genes delay flowering at low ambient temperatures in cereals, however. Three SVP-like genes have been identified in barley: Barley MADS1 (BM1), BM10 and Hordeum vulgare VEGETATIVE TO REPRODUCTIVE TRANSITION 2 (HvVRT2) (Schmitz et al., 2000; Kane et al., 2005; Trevaskis et al., 2007). Expression of these genes increases rapidly at low-temperatures, suggesting a role for SVP-like genes in regulating temperature responses (Fig. 1C; Trevaskis et al., 2007). When over-expressed in barley, BM1 and BM10 inhibit floral meristem identity and delay heading by slowing inflorescence development after the transition to reproductive growth (Trevaskis et al., 2007). HvFT1 and the day-length response pathway regulate this stage of development, but is not known whether BM1 or BM10 represses HvFT1. A role in regulation of the vernalization response has been suggested for HvVRT2 (Kane et al., 2005), but this now seems unlikely (Trevaskis et al., 2007), and while there is some evidence that HvVRT2 might interact with the promoter of HvVRN1 (Kane et al., 2007), the functional significance of such interactions is unclear.

An Earliness per se gene that reduces the influence of temperature on flowering time has been identified and mapped in einkorn wheat (Fig. 1C; Bullrich et al., 2002; Appendino and Slafer, 2003; Lewis et al., 2008). Cloning of this gene might offer further insight into how ambient temperatures influence flowering time in cereals.

HOW USEFUL IS ARABIDOPSIS AS A MODEL FOR UNDERSTANDING THE REGULATION OF FLOWERING TIME IN CEREALS?

Arabidopsis will continue to provide insights into how flowering time is regulated in cereals. One area where arabidopsis will likely have a large impact is in unravelling the interactions between CCT domains and HAP proteins, where the availability of different mutants will be invaluable in determining the functions of the many members of these conserved gene families. In other areas, arabidopsis is less useful as a model for the study of seasonal flowering-responses in cereals, since it lacks many of the genes that regulate flowering in cereals, such as VRN2 and Ehd1. Furthermore, FLC-like genes are not found in cereals, so homologues of arabidopsis genes that influence flowering time by regulating FLC might have different roles. For example, VIN3-like genes have been identified in wheat (Fu et al., 2007) but it is not clear whether these genes regulate flowering time in the absence of any FLC-like genes.

The grass Brachypodium distachyon has been developed as an alternative model system for cereals and is likely to have similar seasonal flowering-responses to those of cereals (Opanowicz et al., 2008). In most respects cereal crop species are themselves amenable to molecular genetic studies. The rice genome has been sequenced, rice can be genetically transformed, and there are many tools available for genomic analysis, such as high density micro-arrays. Similarly, many genomic tools have been developed for barley and wheat; both are transformable and sequencing of the wheat and barley genomes is underway. For cereal crop species there is also detailed understanding of their physiology and extensive genetic resources; including mapping populations, collections of different genotypes and detailed pedigree information. This raises the question of how much value Brachypodium will be as a model species? It seems that Brachypodium will be useful as a laboratory model for basic aspects of grass biology, for high-throughput genetic analysis in simple growth conditions for example, but to a large extent crops such as rice, wheat and barley require no model species. This is particularly true for the study of traits such as flowering time where research can be directly linked with field traits and crop performance.

CONCLUSIONS

Plants respond to environmental cues such as day length, vernalization and ambient temperature in order to flower under the most favourable conditions. Arabidopsis has been used extensively to study the pathways involved in flowering, which are now well understood in this plant. Recent efforts to extend the understanding of flowering-time pathways in cereals have highlighted key differences between the flowering time pathways of arabidopsis and cereal crops, and shown that seasonal flowering-responses are to a large extent controlled by different genes in cereals. This highlights the need to study flowering-time pathways directly in cereal crop species or in a model species that is more closely related to cereals such as Brachypodium.

ACKNOWLEDGEMENTS

We thank our colleagues M. Hemming, S. Oliver and D. Bond for helpful discussions and comments in the improvement of the manuscript. We gratefully acknowledge the GRDC for their continuing support of our research. This work was supported by the CSIRO Division of Plant Industry, the CSIRO Office of the Chief Executive and by a PhD scholarship to A.G. from the College of Sciences at the Australian National University.

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