Journal of Experimental Botany, 64,(14): 4131-4141 (Nov 2013)
The regulation of seasonal flowering in the Rosaceae
Takeshi Kurokura, Naozumi Mimida, Nicholas H. Battey, Timo Hytönen

Abstract
Molecular mechanisms regulating the flowering process have been extensively studied in model annual plants; in perennials, however, understanding of the molecular mechanisms controlling flowering has just started to emerge. Here we review the current state of flowering research in perennial plants of the rose family (Rosaceae), which is one of the most economically important families of horticultural plants. Strawberry (Fragaria spp.), raspberry (Rubus spp.), rose (Rosa spp.), and apple (Malus spp.) are used to illustrate how photoperiod and temperature control seasonal flowering in rosaceous crops. We highlight recent molecular studies which have revealed homologues of TERMINAL FLOWER1 (TFL1) to be major regulators of both the juvenile to adult, and the vegetative to reproductive transitions in various rosaceous species. Additionally, recent advances in understanding of the regulation of TFL1 are discussed.


Seasonal flowering rose species have an indeterminate growth habit, and inflorescences are formed at the top of lateral shoots. Vegetative growth dominates from summer to autumn, when the floral transition begins in the axillary buds of newly developed vegetative shoots; then, after flower initiation in spring, these axillary buds bloom so that the process of flower initiation to flowering is completed within a few months (Fig. 1; Foucher et al., 2008; Iwata et al., 2012; Bendahmane et al., 2013).

In contrast to seasonal flowering, the continuous flowering habit (also called recurrent, perpetual, everbearing, or remontant flowering) is also known in rose and strawberry. The flowering phenotype of roses and strawberries classified in this category may vary from continuous flowering to occasional flowering (Stewart and Folta, 2010; Iwata et al., 2012; Heide et al., 2013). Unlike seasonal flowering types which have months of juvenile phase, perpetual flowering rose and strawberry start to flower in the first growing season and initiate new flowers until late autumn (Sønsteby and Heide, 2007; Foucher et al., 2008). The primocane raspberry cultivars show some similarities with perpetual flowering roses and strawberries. They have annual canes which are induced to flower in summer, and flowers grow out immediately so that fruiting occurs in the autumn (Carew et al., 2000; Sønsteby and Heide, 2009).


Regulation of flowering by vernalization and ambient temperature

Many plant species require a long period of cold (i.e. vernalization) before they can be induced to flower. In Arabidopsis, a MADS-box gene, FLOWERING LOCUS C (FLC), is the key flowering repressor regulated by vernalization (see Kim et al., 2009, for example). FLC represses flowering in a protein complex with another MADS-box protein, SHORT VEGETATIVE PHASE (SVP), by binding to the regulatory sequences of flowering time genes FT, FD, and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) (Searle et al., 2006; Li et al., 2008). In wheat and sugar beet, different repressors, VRN2 and BvFT1, respectively, have been shown to mediate the vernalization requirement by targeting flower-inducing FT homologues (Distelfeld et al., 2009; Pin et al., 2010).

In winter-annual Arabidopsis accessions, the high expression level of FLC is maintained by functional FRIGIDA (FRI) (Shindo et al., 2005; Geraldo et al., 2009). Winter chilling causes the silencing of FLC by modification of chromatin structure in a dose-dependent manner and enables flower initiation to take place in spring (Saleh et al., 2008; Angel et al., 2011). During vernalization, the transcription of the antisense of FLC, COOLAIR, is up-regulated to mediate the transcriptional silencing of the sense transcripts; then a protein complex, Polycomb repressor complex 2 (PRC2), deposits repressive histone marks including histone H3 lysine 27 trimethylation (H3K27me3) on the FLC locus, and subsequently FLC is stably silenced by LIKE HETEROCHROMATIN PROTEIN1 (LHP1) and VERNALIZATION (VRN2) (reviewed by Alexandre and Hennig, 2008; Ietswaart et al, 2012).

Not only chilling temperature but also warmer ambient temperature affects flowering time by controlling FT mRNA expression levels (Samach and Wigge, 2005). In Arabidopsis, genetic studies showed that late flowering at 16 °C, compared with 23 °C, is caused by FCA-dependent activation of SVP at cooler temperatures. Consequently, SVP binds to the CArG-box elements in the FT and SOC1 promoters to repress their expression (Lee et al., 2007; Li et al., 2008). Recent study has revealed that the temperature-dependent change in the proportion of histone variant H2A.Z relative to H2A in chromatin is a key mechanism regulating gene expression in response to small changes in temperature in the plant (Kumar and Wigge, 2010). H2A.Z is involved in the warm temperature activation of FT transcription, since it controls the accessibility of the FT promoter to the transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) (Kumar et al., 2012).